Mammalian Dengue Virus Receptors

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Mammalian Dengue Virus Receptors Arturo Cabrera-Hernandez and Duncan R. Smith! Molecular Pathology Laboratory, Institute of Molecular Biology and Genetics, Mahidol University, Salaya Campus, 25/25 Phuttamonthol Sai 4, Salaya, Nakorn Pathom, Thailand 73710

Abstract It has been estimated that some 3 billion people live in areas at the risk of infection with the dengue virus, and that up to 100 million infections occur each year, making dengue the most common arthropod-borne viral disease. Humans become infected following the bite of an infected mosquito, and infection can either be essentially without symptoms, or can result in severe, life-threatening manifestations. The initial interaction between a susceptible host cell and the dengue virus is a critical determinant of cell tropism and thus of pathogenicity. As such, considerable effort has been expended on trying to determine the nature of the initial cell: virus interaction and in particular to identify the nature of the receptor proteins used by dengue virus to enter into the cell. Over the last few years a number of proteins, including DC-SIGN, GRP-78, the 37/67kDa high-affinity laminin receptor and heat shock proteins 70 and 90, have all been implicated as dengue virus receptors in a number of cell types. In addition, the specific role of heparan sulfate in dengue virus binding and internalization of dengue still remains to be fully elucidated. This review seeks to provide an overview of the current state of research into mammalian dengue virus receptors, as an increased understanding of which molecules can function as dengue virus receptors and how their expression leads to cell susceptibility will potentially provide novel insights into the pathogenic mechanism of dengue virus infection. Keywords: 37/67kDa high-affinity laminin receptor, DC-SIGN, Fc receptor, flavivirus, GRP78, heparan sulfate, HSP70, HSP90, L-SIGN.

Introduction Approximately 100 million people are believed to be infected with the dengue virus each year[1], making it the most prevalent arthropodborne viral disease. While the majority of these infections are believed to be asymptomatic, the infection may result in a febrile disease termed dengue fever (DF) or it may result in haemorrhagic manifestations, which are classified as either dengue haemorrhagic fever (DHF) or dengue shock syndrome (DSS) dependent upon severity[2]. Dengue virus is classified in the family Flaviviridae, genus

Flavivirus, and species dengue virus, and comprises of four antigenically distinct viruses termed DENV-1, DENV-2, DENV-3 and DENV4. The dengue viruses are enveloped positivesense single-stranded RNA viruses of approximately 11 kb that encodes for three structural proteins (core, pre-membrane and envelope) and seven nonstructural proteins (NS1, NS2A, NS2B, NS3, NS4A, NS4B and NS5) in one open reading frame[3]. The principal vectors of dengue virus transmission are Aedes aegypti and Aedes albopictus mosquitoes. The transmission of the

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dengue virus to humans occurs after the bite of an infected mosquito, and the subsequent ability of the virus to infect the host depends on the capacity of the virus to bind to, internalize into and productively infect target cells. The initial interaction between the dengue virus and host cells has been the focus of considerable efforts to isolate and characterize the molecules involved. As for other virus : cell systems[4], the initial dengue virus : cell interaction is believed to involve the concentration of dengue virus particle through an initial interaction with a low-affinity binding element before transfer to a second receptor protein able to bind and internalize the virus. In the last few years considerable insights into this mechanism have emerged, bringing with them the possibility of new strategies to stop dissemination of the virus, or to identify molecular markers linked to individuals at high risk of developing the severe forms of the disease.

The Role of Heparan Sulfate In 1997, Chen and colleagues identified the glycosaminoglycan molecule, heparan sulfate, as a non-specific receptor molecule responsible for dengue virus attachment in several cell lines[5]. Heparan sulfate is expressed in almost all cells types, and is composed of alternating hexuronic acid / D-glucosamine disaccharides, which contain different degrees and patterns of sulfation, forming a linear chain with a remarkable diversity in length and structural complexity. This structural diversity confers the ability to recognize a vast array of ligands and to participate in a wide variety of physiological functions[6,7]. A number of viruses[8-19], bacteria[20] and parasites [21-24] exploit the adhesive properties of heparan sulfate and use it as a binding molecule to attach to a target cell. The contribution of heparan sulfate expression to dengue virus entry has been 120

variously shown by (i) a significant decrease in dengue virus binding capacity after enzymatic removal of heparan sulfate[25-29]; (ii) a dose-dependent heparin binding inhibition[26,27,29,30-33]; and (iii) virus-binding assays in a mutant target cell lacking heparan sulfate expression[28,32]. In agreement with previous reports that showed a principal role of the dengue virus envelope protein in the initial binding to target cells[33,34], Chen and colleagues[5], delineated the participation of the envelope protein to domain III, and detected two potential consensus heparan sulfate binding motifs inside this domain (amino acids 284-310 and amino acids 386411). These observations were corroborated by studies that inhibited the binding and internalization of the dengue virus with monoclonal antibodies specific against this envelope protein region [35,36] or with recombinant soluble forms of envelope protein domain III[32]. Detailed in vitro and in vivo competition binding assays using a synthetic undecapeptide based on the epitope region recognized by the anti-protein E neutralizing monoclonal antibody, 4E11, identified a highly conserved region in all four serotypes (amino acids 306-314), as essential to the interaction with heparin, a structural homologue of heparan sulfate[37]; however, complementary roles for domains I and II cannot be excluded [30]. By contrast, the particular structural motifs in the heparan sulfate molecule that participate in the binding remain to be clarified. Binding assays employing recombinant E protein and heparan sulfate homologues have shown a minimum length requirement of 10 disaccharides with a flexible structure of at least 39Å, and a highly sulfated state for optimal binding[5,38], while enzymatic analysis suggest the additional presence of b-linked terminal glucose, galactose or fucose as well as sialic acid residues may also be required[26]. Studies using liver cell lines (HuH-7 and HepG2) have shown that the binding of the dengue virus Dengue Bulletin – Vol 29, 2005

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to liver cells is not saturatable[25,39] and in HuH7 cells this has been shown to be a consequence of heparan sulfate expression[25]. In contrast, Vero and LLC-MK cells have both shown to be saturatable, although binding can still be blocked in a dose-dependent fashion by heparin [26] . The dengue virus binding differences between hepatoma and kidney cell lines could possibly be related to the high degree of sulfation reported for heparan sulfate in liver cell lines or in human liver cells[40] that give liver cells a particularly high capacity for concentrating the virus at the membrane surface and could be related to the particular tropism of liver for dengue virus[5]. Interestingly, heparin does not inhibit recombinant E protein or dengue virus binding to insect cell lines[26,32], suggesting that the target cell as well as the serotype[29] may all influence the initial heparan sulfate-dengue virus binding interaction. Given the ubiquitous heparan sulfate expression at the membrane surface in almost all organs[6,7] but the restricted number of dengue virus-target organs, as well as the

divergence between the kinetics of dengue virus binding and dengue virus internalization[35] and the observation that the elimination/reduction of heparan sulfate significantly decreases but does not abolish completely the binding and internalization of the dengue virus[25,27-29], several groups have proposed the existence of additional receptors participating in concert during the internalization process [27-30] . It has been proposed therefore that heparan sulfate serves to concentrate the virus at the membrane surface and facilitate interaction of the virus with a second, high-affinity receptor [4,41], although the direct participation of heparan sulfate-proteoglycans in virus binding and entry cannot be excluded[25]. The identity of these high affinity receptor elements has been the object of considerable investigation, resulting in the identification of several characterized receptors as well as a number of potential candidate receptor proteins many of which have been identified by little more than a molecular mass. A summary of the known and potential dengue virus receptors is presented in the Table.

Table. Known and proposed dengue virus receptors in mammalian and insect cells

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Dengue Virus Receptors in Cells of the Myeloid Lineage Since the earliest reports implicating monocytes (MO) and macrophages (φ) in the pathogenesis of dengue infection[2,61], considerable effort has been undertaken to clarify their role during the course of the infection. MO/φ are a complex and heterogeneous population, derived from a common progenitor in bone marrow. As differentiation progresses, they migrate through the blood stream, finally distributing into the peripheral organs, where the particular microenvironment confers a distinctive macrophage’s characteristics resulting in different subsets of cells with specific characteristics and functions[62] as well as conferring a specific susceptibility to dengue virus infection. Thus, in a primary infection, only 1% to 2% of blood MO/φ are infected, whereas monocyte-derived dendritic cells (DCs) are highly susceptible and are productively infected, as has been shown by both in vitro and in vivo studies[63,64]. In contrast, Kupffer cells and Langerhans cells, the macrophages residing in the liver and skin respectively, can be infected but the infection is non-productive[64,65]. Blood MO/φ were defined as the principal target cells infected during a second infection with a heterologous DENV infection, and infection was shown to occur via the antibodydependent enhancement (ADE) mechanism[61,66]. The participation of receptors that recognize the constant region of IgG, FcγRI and FcγRII[51,52] were identified as key players during the process of ADE through the internalization of the complex formed between the anti-dengue antibody, the dengue virus and the Fc receptor, when the antibodies are either cross-reacting but not neutralizing or when the antibodies are present at sub-neutralizing concentrations[67]. Although important during the process of ADE, Fc receptors are not the 124

only dengue virus receptors expressed by macrophages. In one early work employing adherent human monocytes, Daughaday and colleagues [68] revealed the existence of receptors sensitive to trypsin, in addition to the trypsin insensitive Fc receptors. Subsequent work by Bielefeldt-Ohmann employing a virus overlay protein binding assay (VOPBA) to membrane proteins from the myelomonocytic cell line HL60 identified two dengue virusbinding non-Fc proteins of 40/45 and 70/75 kDa[44]. Remarkably, although the competitive inhibitor heparin decreased the HL60-dengue virus binding capacity, the opposite effect was reported after the enzymatic removal of HS supporting the co-participation of HS and the high affinity receptor during the binding process[30]. The identity of the high affinity receptor has remained elusive for several years, although several lines of research have revealed some clues about the identity of the receptor(s). Chen and colleagues[45] detected a CD14-dependent-LPS-inhibition during dengue virus binding to primary human blood MO/φ, suggesting that one CD14-coupledunidentified molecule acted as a dengue virus receptor. Moreno-Altamirano and colleagues[46] employing a DENV-2-bound Sepharose 4B column and VOPBA assays defined 4 proteins bands with molecular masses of 27, 45, 67 and 87 kDa on the cell surface of the primary human blood MO/φ, while in PMA-differentiated U-937 cells they detected only the 45 and 67 kDa bands whereas no bands were detected in undifferentiated U-937 cells. Interestingly, these results may support an earlier observation in which it was noted that there is an increase in the susceptibility to infection as the U-937 macrophage cell line differentiates [69] . Reyes del Valle and colleagues[56] employing a combination of E protein column affinity chromatography and VOPBA assay analysed membrane extracts Dengue Bulletin – Vol 29, 2005

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from the U937 cell line and the human neuroblastoma cell line SK-SY-5Y and detected 5 proteins bands with molecular masses of 45, 60, 75, 84 and 100 kDa. Mass spectroscopy analysis identified the 84 kDa band as Heat Shock Protein 90 (HSP90). HSPs are a family of highly conserved molecular chaperones with a broad intra-cellular location that assist the structure formation of proteins in vivo and participate in a number of normal, stress and pathological responses[70]. These properties are exploited by a number of different viruses to assist the correct folding and trafficking of viral proteins during the virus life cycle[71]. In addition to their intra-cellular location, some family members are located at the cell surface, enclosed in detergentresistant microdomains (lipids rafts)[72] where they participate in a variety of functions, including functioning as co-receptors for ligands or viruses [71,73] . Thus, Hsc70 and integrins αvβ3 and αxβ2 cluster during rotavirus binding[74], whereas GRP78, a HSP homolog, associates with the molecule MHCI and the integrin αvβ3 during coxsackievirus A9 (CAV-9) entry[75]. Additionally, HSP90 and HSP70 are known to associate at the cell surface membrane, participating in LPS (lipopolysaccharide) binding in the so-called “CD14-independent LPS receptor cluster”[76]. This observation, in the light of the LPSdependent- inhibition of DENV infection[45], permitted Reyes del Valle and colleagues[56] to infer and subsequently demonstrate the coparticipation of the lipid raft-associated HSP70 during DENV entry to the cell. Prolonged expression of HSP70 and HSP90 has been detected in animals exposed to fever range hyperthermia [77], and fever is a common symptom of dengue infection. It is interesting to speculate therefore that the dengue viruses’ ability to use HSPs may result in a higher infection potential during the fever period. The idea that circulating MO/φ are the primary target during DENV infection changed Dengue Bulletin – Vol 29, 2005

after several groups reported the finding that DCs are highly susceptible to infection by the dengue virus[63,78-80]. This quickly led to the identification in immature human DCs of the dendritic cell-specific intercellular adhesion molecule grabbing non-integrin (DC-SIGN, CD209)[54,55] as a dengue virus non-Fc-receptor protein. DC-SIGN is a multifunctional protein involved in the establishment of the immunological synapse between the dendritic cells and T cells through binding to the ICAM3 protein[81], in the migration of DCs based on its ability to bind the ICAM-2 protein[82] as well as in the binding and/or internalization of a variety of viruses [83-89] , bacteria [90-94] , parasites [90,95,96] , yeast [97] and fungus [98] . Interestingly, it was the ability of DC-SIGN to bind the HIV-1 envelope glycoprotein gp120 that originally led Curtis and colleagues[99] to isolate, clone, sequence and study this C-type lectin protein in 1992. Using DC-SIGN-specific monoclonal antibodies, its expression has been detected in blood, particularly in one small subset of myeloid DC CD14+ cells [100], whereas in peripheral tissues its expression has been found in immature myeloid DCs in skin, intestine, lung, liver, placenta and lymph nodes[81,101,102]. Additionally, its presence has been reported in alveolar macrophages[98,103] but neither Langerhans cells nor plasmacytoid DCs express DC-SIGN[81,104]. The participation of DC-SIGN in dengue virus infections was shown by competition assays employing either monoclonal antibodies against DC-SIGN or soluble DC-SIGN to inhibit DENV infection, as well by the acquisition of susceptibility to dengue infection by a dengue virus-resistant cell line (THP-1) after DC-SIGN transfection [54,55]. However, mutations in the DC -SIGN internalization motifs as well as in its intracellular domain permit infection at levels similar to the wild type protein, suggesting that DC-SIGN may participate in the early events of virus attachment but function as a 125

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co-receptor during the internalization process[64]. Based on immunohistochemical analysis, alveolar macrophages have been reported to be susceptible to infection by the dengue virus[105,106] and to express DC-SIGN, but the involvement of DC-SIGN in the infection process remains to be demonstrated. Attention has also focused on a homolog of DC-SIGN, called L-SIGN[107]. While L-SIGN is a homolog of DC-SIGN, there are differences in the extracellular domain as well as differences in its ability to bind some ligands [108,109] and L-SIGN expression is apparently restricted to liver sinusoidal endothelial cells as well as a subset of endothelial cells in the paracortex zone of lymph nodes[101,110]. While L-SIGN has the ability to bind dengue viruses and its expression in THP-1 cells induces susceptibility to dengue virus infection, and specific antibodies against L-SIGN can subsequently block the acquired susceptibility[54], an in vivo role for this protein remains to be established. The L-SIGN-dependent DENV infection of THP-1 cells offers an intriguing possibility for the participation of L-SIGN in dengue virus infection in the liver, where the physical location of liver sinusoidal endothelial cells confers a strategic advantage for interacting with DENV in the early period of infection[111]. Although an in vivo role for L-SIGN in dengue virus internalization has not been demonstrated, histochemical and in situ hybridization analysis of post-mortem samples have shown the presence of DENV antigen in the vascular endothelial liver cells, although the presence of dengue virus was reported to be negative[105,106]. However, it is possible that, as has been demonstrated for other viruses, the participation of L-SIGN could be limited to the binding, concentration and infection in trans- of neighbouring cells as has been shown to occur with the human immunodeficiency virus, hepatitis C virus and Ebola virus[84,110,112]. 126

Dengue Virus Receptors Expressed in the Liver Several lines of evidence show the involvement of the liver during dengue virus infections. Analyses of liver sections from fatal cases of dengue virus infection by immunohistochemistry consistently demonstrate the presence of dengue virus antigens in hepatocytes, Kupffer cells and/or liver endothelial cells[86, 105, 113], and the presence of the dengue virus RNA in hepatocytes and/or Kupffer cells has been demonstrated by RTPCR and in situ hybridization.[106,114-116] Increases in alanine transaminase (ALT) and aspartate transaminase (AST) levels during the development of the disease[117-121] as well as liver enlargement are common features of the disease. Although damage to the liver in the most severe forms of the disease has been well documented, it is not clear what the initial target cells are and what mediates the initial contact between the virus and the liver target cell[122]. In the absence of a valid animal model system, and given the difficulties associated with working with primary human cells, studies of dengue virus infection of the human liver in vitro have primarily centred around the use of human hepatoma cell lines[25,29,31,39,48-50,120,123]. While it needs to be borne in mind that these cells possess considerable variation from primary human cells in that they have undergone neoplastic transformation[124,125,126], they evince many of the properties seen in patients during dengue virus infection such as increases in the level of ALT/AST[120], a rise in the production of the chemokine RANTES[127] as well as virusinduced apoptosis[128-130]. However, at some point the use of human primary hepatoma cells will be required to validate the results generated with transformed cell lines. In 2000, Hilgard and Stockert[25], employing the human hepatoma cell line HuH-7, reported the participation of two 33 and 37-kDa trypsinDengue Bulletin – Vol 29, 2005

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sensitive heparan sulfate proteoglycans in the virus binding, attachment and internalization, but presented no further characterization of the molecules identified. However, in 2004, Thepparit and Smith[50], using a combination of virus overlay protein binding assay and mass spectroscopy, identified the 37/67-kDa highaffinity laminin receptor as a DENV-1 receptor expressed by HepG2 liver cells. Using a combination of the natural ligand for this receptor (soluble laminin) and antibodies directed against the 37/67kDa high-affinity laminin receptor, the authors further restricted the participation of this receptor to DENV-1. More recently, Tio et al.[53], using a twodimensional VOPBA analysis of proteins expressed by Porcine kidney cell line PS Clone D, confirmed the ability of the 37/67-kDa highaffinity laminin receptor to bind DENV-1, and suggested that, in addition, the 37/67-kDa highaffinity laminin receptor under certain conditions may also be able to bind DENV-2 and DENV-3 (but not DENV-4). While Tio et al.[53] suggest a broader role for the 37/67-kDa high-affinity laminin receptor as a dengue virus receptor, their use of porcine kidney cells as well as their observations relying solely on binding studies without validation of receptor function makes the results of questionable significance. The 37/67 kDa high-affinity laminin receptor is a nonintegrin cell surface receptor that mediates high-affinity interactions between cells and laminin[131]. The 37kDa molecule is believed to be a precursor protein generating the mature 67kDa laminin receptor, with the maturation process involving dimerization and acylation of the precursor[132], although the relationship between the two forms is not fully understood. The 37/67kDa high-affinity laminin receptor is expressed in a number of normal tissues including liver cells, as well as being up-regulated in hepatocyte carcinoma cells[133]. While the natural ligand for this receptor is the laminin protein in the extracellular matrix, some Dengue Bulletin – Vol 29, 2005

alphaviruses[134,135], the cellular prion protein[136] and the cytotoxic necrotizing factor 1[137], a bacterial ligand, all use the 37/67 kDa highaffinity laminin receptor protein as receptor with pathological consequences for the host. Evidence also suggests that there is an association between the 37/67kDa high-affinity laminin receptor protein and other glycoproteins at the cell surface, including the dengue virus low-affinity binding molecule heparan sulfate. Thepparit and Smith [50] reported an additive effect on dengue virus internalization between heparan sulfate and the 37/67kDa high-affinity laminin receptor, suggesting a parallel with the mechanism of the cellular prion protein where binding has been shown to consist of a complex between heparan sulfate, the 37/67kDa high-affinity laminin receptor and the prion protein[138]. However, given that the 37/67kDa high-affinity laminin receptor protein is expressed in a number of cell types while only a few of them are documented to be able to be infected by the dengue virus, it is likely that additional elements of this receptor system remain to be determined. Additionally in 2004, Jindadamrongwech and Smith[49], employing VOPBA on membrane extracts of the human hepatoma cell line HepG2, identified dengue-binding proteins with approximate molecular masses of 78-80, 90, 98 and 102kDa for DENV-2, 90, 130 and 182kDa for DENV-3 and 90 and 130kDa for DENV-4[48]. Further coupling VOPBA and mass spectroscopy, they subsequently identified the 78kDa band for DENV-2 as the glucose-related protein, GRP78 (BiP)[49]. Pre-treatment with anti-GRP78 antibodies resulted in either a partial inhibition of DENV-2 infection or a dosedependent virus production enhancement[49] dependent upon the specific antibody used, suggesting that additional receptor elements are almost certainly required. GRP78 is a homolog of the HSP proteins and is located principally in the endoplasmic reticulum (ER) 127

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where it may function to assist correct protein folding[139]. The presence of GRP78 at the cell surface has been demonstrated, where it can function as co-receptor for CAV-9 binding[140] and as the activated and receptor recognized form of α2-macroglobulin signalling receptor[141]. Given that GRP78 is a homolog of HSPs, it is possible that other members of this stress-induced family may play a role in dengue virus binding and internalization in different cell types.

Future Directions While the last few years have shown significant progress being made in determining the nature and mechanism of the actions of the dengue virus receptor proteins, many questions still remain to be answered. Future research will need to define more closely which specific cell types are susceptible to both productive and non-productive infection as well as defining what receptors are expressed by those cells. The issue of serotype-specific usage of receptors as noted with some of the liver cell lines remains

References

controversial, and studies with human primary cells are urgently needed. The question of the biological significance of receptor usage is one that will become particularly prominent. In this regard, the recent work by Sakuntabhai and co-authors[142], who reported a promoter polymorphism in CD209 (DC-SIGN) that provides significant protection against dengue fever but not against dengue haemorrhagic fever, is particularly important. The identification of this and other receptors may open the way to the development of specific, receptor-based prophylaxis and therapy as well as, potentially, the early genetic identification of individuals at increased risk of developing dengue fever or, more importantly, dengue haemorrhagic fever or dengue shock syndrome.

Acknowledgements Arturo Cabrera-Hernandez is supported by the Consejo Nacional de Ciencia y Tecnología, México, and Duncan R. Smith is supported by the Thailand Research Fund and Mahidol University, Thailand.

[6]

Esko JD and Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest. 2001; 108(2): 169173.

[1]

Guzman MG and Kouri G. Dengue: an update. Lancet Infect Dis. 2002; 2(1): 33-42.

[7]

[2]

Halstead SB. Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenic cascade. Rev Infect Dis. 1989; 11(Suppl 4): S830S839.

Coombe DR and Kett WC. Heparan sulfate-protein interactions: therapeutic potential through structure-function insights. Cell Mol Life Sci. 2005; 62(4): 410-424.

[8]

Compton T, Nowlin DM and Cooper NR. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology. 1993; 193(2): 834-841.

[9]

Zhu Z, Gershon MD, Gabel C, Sherman D, Ambron R and Gershon A. Entry and egress of varicella-zoster virus: role of mannose 6phosphate, heparan sulfate proteoglycan, and signal sequences in targeting virions and viral glycoproteins. Neurology. 1995; 45(12 Suppl 8): S15-S17.

[3]

Henchal EA and Putnak JR. The dengue viruses. Clin Microbiol Rev. 1990; 3(4): 376-396.

[4]

Mettenleiter TC. Brief overview on cellular virus receptors. Virus Res. 2002; 82(1-2): 3-8.

[5]

Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD, Linhardt RJ and Marks RM. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med. 1997; 3(8): 866-871.

128

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Mammalian Dengue Virus Receptors [10] Jackson T, Ellard FM, Ghazaleh RA, Brookes SM, Blakemore WE, Corteyn AH, Stuart DI, Newman JW and King AM. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J Virol. 1996; 70(8): 5282-5287. [11] Byrnes AP and Griffin DE. Binding of Sindbis virus to cell surface heparan sulfate. J Virol. 1998; 72(12): 7349-7356. [12] Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, Cohen GH, Eisenberg RJ, Rosenberg RD and Spear PG. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell. 1999; 99(1): 13-22. [13] Qiu J, Handa A, Kirby M and Brown KE. The interaction of heparin sulfate and adeno-associated virus 2. Virology. 2000; 269(1): 137-147. [14] Giroglou T, Florin L, Schafer F, Streeck RE and Sapp M. Human papillomavirus infection requires cell surface heparan sulfate. J Virol. 2001; 75(3): 1565-1570. [15] Hulst MM, van Gennip HGP, Vlot AC, Schooten E, de Smit AJ and Moormann RJM. Interaction of classical Swine fever Virus with membraneassociated heparan sulfate: Role for Virus Replication In Vivo and Virulence. J Virol. 2001; 75: 9585-9595. [16] Birkmann A, Mahr K, Ensser A, Yaguboglu S, Titgemeyer F, Fleckenstein B and Neipel F. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J Virol. 2001; 75(23): 1158311593. [17] Reddi HV and Lipton HL. Heparan sulfate mediates infection of high-neurovirulence Theiler’s viruses. J Virol. 2002; 76(16): 8400-8407. [18] Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, Kinoshita-Toyoda A, Toida T, Van Kuppevelt TH, Depla E, Von Weizsacker F, Blum HE and Baumert TF. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem. 2003; 278(42): 41003-41012. [19] Escribano-Romero E, Jimenez-Clavero MA, Gomes P, Garcia-Ranea JA and Ley V. Heparan sulphate mediates swine vesicular disease virus attachment to the host cell. J Gen Virol. 2004; 85(Pt 3): 653-663. [20] Zhang JP and Stephens RS. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell. 1992; 69(5): 861-869.

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[21] Alvarez-Dominguez C, Vazquez-Boland JA, Carrasco-Marin E, Lopez-Mato P and Leyva-Cobian F. Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun. 1997; 65(1): 78-88. [22] Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D and Wahlgren M. Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1. Blood. 2003; 101(6): 2405-2411. [23] Calvet CM, Toma L, De Souza FR, Meirelles M de N and Pereira MC. Heparan sulfate proteoglycans mediate the invasion of cardiomyocytes by Trypanosoma cruzi. J Eukaryot Microbiol. 2003; 50(2): 97-103. [24] Bishop JR and Esko JD. The elusive role of heparan sulfate in Toxoplasma gondii infection. Mol Biochem Parasitol. 2005; 139(2): 267-269. [25] Hilgard P and Stockert R. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology. 2000; 32(5): 1069-1077. [26] Thaisomboonsuk BK, Clayson ET, Pantuwatana S, Vaughn DW and Endy TP. Characterization of dengue-2 virus binding to surfaces of mammalian and insect cells. Am J Trop Med Hyg. 2005; 72(4): 375-383. [27] Martínez-Barragán JJ and del Angel RM. Identification of a putative coreceptor on vero cells that participates in dengue 4 virus infection. J Virol. 2001; 75(17): 7818-7827. [28] Germi R, Crance J-M, Garin D, Guimet J, LortatJacob H, Ruigrok RWH, Zarski JP and Drouet E. Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology. 2002; 292(1): 162-168. [29] Thepparit C, Phoolcharoen W, Suksanpaisan L and Smith DR. Internalization and propagation of the dengue virus in human hepatoma (HepG2) cells. Intervirology. 2004; 47(2): 78-86. [30] Bielefeldt-Ohmann H, Meyer M, Fitzpatrick DR and Mackenzie JS. Dengue virus binding to human leukocyte cell lines: receptor usage differs between cell types and virus strains. Virus Res. 2001; 73(1): 81-89. [31] Lin YL, Lei HY, Lin YS, Yeh TM, Chen SH and Liu HS. Heparin inhibits dengue-2 virus infection of five human liver cell lines. Antiviral Res. 2002; 56(1): 93-96.

129

Mammalian Dengue Virus Receptors [32] Hung JJ, Hsieh MT, Young MJ, Kao CL, King CC and Chang W. An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells. J Virol. 2004; 78(1): 378-388. [33] Anderson R, King AD and Innis BL. Correlation of E protein binding with cell susceptibility to dengue 4 virus infection. J Gen Virol. 1992; 73(Pt 8): 21552159. [34] Chen Y, Maguire T and Marks RM. Demonstration of binding of dengue virus envelope protein to target cells. J Virol. 1996; 70(12): 8765-8772. [35] Hung S-L, Lee P-L, Chen H-W, Chen L-K, Kao C-L and King C-C. Analysis of the steps involved in dengue virus entry into host cells. Virology. 1999; 257(1): 156-167. [36] Crill WD and Roehrig JT. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J Virol. 2001; 75(16): 7769-7773. [37] Thullier P, Demangel C, Bedouelle H, Mégret F, Jouan A, Deubel V, Mazie J-C and Lafaye P. Mapping of a dengue virus neutralizing epitope critical for the infectivity of all serotypes: insight into the neutralization mechanism. J Gen Virol. 2001; 82(Pt 8): 1885-1892. [38] Marks RM, Lu H, Sundaresan R, Toida T, Suzuki A, Imanari T, Hernaiz MJ and Linhardt RJ. Probing the interaction of dengue virus envelope protein with heparin: assessment of glycosaminoglycanderived inhibitors. J Med Chem. 2001; 44(13): 2178-2187.

[43] Ramos-Castaneda J, Imbert JL, Barron BL and Ramos C. A 65-kDa trypsin-sensible membrane cell protein as a possible receptor for dengue virus in cultured neuroblastoma cells. J Neurovirol. 1997; 3(6): 435-440. [44] Bielefeldt-Ohmann H. Analysis of antibodyindependent binding of dengue viruses and dengue virus envelope protein to human myelomonocytic cells and B lymphocytes. Virus Res. 1998; 57(1): 63-79. [45] Chen YC, Wang SY and King CC. Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism. J Virol. 1999; 73(4): 2650-2657. [46] Moreno-Altamirano MM, Sanchez-Garcia FJ and Munoz ML. Non Fc receptor-mediated infection of human macrophages by dengue virus serotype 2. J Gen Virol. 2002; 83(Pt 5): 1123-1130. [47] Wei HY, Jiang LF, Fang DY and Guo HY. Dengue virus type 2 infects human endothelial cells through binding of the viral envelope glycoprotein to cell surface polypeptides. J Gen Virol. 2003; 84(Pt 11): 3095-3098. [48] Jindadamrongwech S and Smith DR. Virus Overlay Protein Binding Assay (VOPBA) reveals serotype specific heterogeneity of dengue virus binding proteins on HepG2 human liver cells. Intervirology. 2004; 47(6): 370-373. [49] Jindadamrongwech S, Thepparit C and Smith DR. Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2. Arch Virol. 2004; 149(5): 915-927.

[39] Suksanpaisan L and Smith DR. Analysis of saturation binding and saturation infection for dengue serotypes 1 and 2 in liver cells. Intervirology. 2003; 46(1): 50-55.

[50] Thepparit C and Smith DR. Serotype-specific entry of dengue virus into liver cells: identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol. 2004; 78(22): 12647-12656.

[40] Vongchan P, Warda M, Toyoda H, Toida T, Marks RM and Linhardt RJ. Structural characterization of human liver heparan sulfate. Biochim Biophys Acta. 2005; 1721(1-3): 1-8.

[51] Littaua R, Kurane I and Ennis FA. Human IgG Fc receptor II mediates antibody-dependent enhancement of dengue virus infection. J Immunol. 1990; 144(8): 3183-3186.

[41] Belting M. Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem Sci. 2003; 28(3): 145-151.

[52] Schlesinger JJ and Chapman SE. Influence of the human high-affinity IgG receptor FcgRI (CD64) on residual infectivity of neutralized dengue virus. Virology. 1999; 260(1): 84-88.

[42] Rothwell SW, Putnak R and La Russa VF. Dengue2 virus infection of human bone marrow: characterization of dengue-2 antigen-positive stromal cells. Am J Trop Med Hyg. 1996; 54(5): 503-510. 130

[53] Tio PH, Jong WW and Cardosa MJ. Two dimensional VOPBA reveals laminin receptor (LAMR1) interaction with dengue virus serotypes 1, 2 and 3. Virol J. 2005; 2(1): 25. Dengue Bulletin – Vol 29, 2005

Mammalian Dengue Virus Receptors [54] Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, Sun W, Eller MA, Pattanapanyasat K, Sarasombath S, Birx DL, Steinman RM, Schlesinger S and Marovich MA. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med. 2003; 197(7): 823-829.

[64] Lozach PY, Burleigh L, Staropoli I, Navarro-Sanchez E, Harriague J, Virelizier JL, Rey FA, Despres P, Arenzana-Seisdedos F and Amara A. DC-SIGNmediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J Biol Chem. 2005; 280(25):23698-23708.

[55] Navarro-Sanchez E, Altmeyer R, Amara A, Schwartz O, Fieschi F, Virelizier JL, Arenzana-Seisdedos F and Despres P. Dendritic-cell-specific ICAM3grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquitocell-derived dengue viruses. EMBO Rep. 2003; 4(7): 723-728.

[65] Marianneau P, Steffan AM, Royer C, Drouet MT, Jaeck D, Kirn A and Deubel V. Infection of primary cultures of human Kupffer cells by dengue virus: no viral progeny synthesis, but cytokine production is evident. J Virol. 1999; 73(6): 5201-5206.

[56] Reyes-Del Valle J, Chavez-Salinas S, Medina F and Del Angel RM. Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol. 2005; 79(8): 4557-4567. [57] Yazi Mendoza M, Salas-Benito JS, Lanz-Mendoza H, Hernandez-Martinez S and del Angel RM. A putative receptor for dengue virus in mosquito tissues: localization of a 45-kDa glycoprotein. Am J Trop Med Hyg. 2002; 67(1): 76-84. [58] Salas-Benito JS and del Angel RM. Identification of two surface proteins from C6/36 cells that bind dengue type 4 virus. J Virol. 1997; 71: 7246-7252. [59] Munoz ML, Cisneros A, Cruz J, Das P, Tovar R and Ortega A. Putative dengue virus receptors from mosquito cells. FEMS Microbiol Lett. 1998; 168(2): 251-258. [60] Chee HY and AbuBakar S. Identification of a 48kDa tubulin or tubulin-like C6/36 mosquito cells protein that binds dengue virus 2 using mass spectrometry. Biochem Biophys Res Commun. 2004; 320(1): 11-17. [61] Halstead SB, O’Rourke EJ and Allison AC. Dengue viruses and mononuclear phagocytes. II. Identity of blood and tissue leukocytes supporting in vitro infection. J Exp Med. 1977; 146(1): 218-229. [62] Sasmono RT and Hume DA. The biology of macrophages. In: Kaufmann SHE, Sher A, Ahmed R (Ed.), The innate immune response to infection. ASM Press, American Society for Microbiology, Washington, DC, 2002: pp 71-93. [63] Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, Putvatana R, Louder MK, Filgueira L, Marovich MA, Wong HK, Blauvelt A, Murphy GS, Robb ML, Innes BL, Birx DL, Hayes CG and Frankel SS. Human skin Langerhans cells are targets of dengue virus infection. Nat Med. 2000; 6(7): 816820. Dengue Bulletin – Vol 29, 2005

[66] Halstead SB and O’Rourke EJ. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med. 1977; 146(1): 201-217. [67] Halstead SB, Porterfield JS and O’Rourke EJ. Enhancement of dengue virus infection in monocytes by flavivirus antisera. Am J Trop Med Hyg. 1980; 29(4): 638-642. [68] Daughaday CC, Brandt WE, McCown JM and Russell PK. Evidence for two mechanisms of dengue virus infection of adherent human monocytes: trypsin-sensitive virus receptors and trypsin-resistant immune complex receptors. Infect Immun. 1981; 32(2): 469-473. [69] O’Sullivan MA and Killen HM. The differentiation state of monocytic cells affects their susceptibility to infection and the effects of infection by dengue virus. J Gen Virol. 1994; 75(Pt 9): 2387-2392. [70] Walter S and Buchner J. Molecular chaperonescellular machines for protein folding. Angew Chem Int Ed Engl. 2002; 41(7): 1098-1113. [71] Mayer MP. Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev Physiol Biochem Pharmacol. 2005; 153: 1-46. [72] Broquet AH, Thomas G, Masliah J, Trugnan G and Bachelet M. Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J Biol Chem. 2003; 278(24): 21601-21606. [73] Triantafilou M and Triantafilou K. The dynamics of LPS recognition: complex orchestration of multiple receptors. J Endotoxin Res. 2005; 11(1): 5-11. [74] Lopez S and Arias CF. Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol. 2004; 12(6): 271-278. [75] Triantafilou K and Triantafilou M. Lipid raft microdomains: key sites for Coxsackievirus A9 infectious cycle. Virology. 2003; 317(1): 128-135. 131

Mammalian Dengue Virus Receptors [76] Triantafilou K, Triantafilou M and Dedrick RL. A CD14-independent LPS receptor cluster. Nat Immunol. 2001; 2(4): 338-345. [77] Ostberg JR, Kaplan KC and Repasky EA. Induction of stress proteins in a panel of mouse tissues by fever-range whole body hyperthermia. Int J Hyperthermia. 2002; 18(6): 552-562. [78] Ho LJ, Wang JJ, Shaio MF, Kao CL, Chang DM, Han SW and Lai JH. Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production. J Immunol. 2001; 166(3): 1499-1506. [79] Libraty DH, Pichyangkul S, Ajariyakhajorn C, Endy TP and Ennis FA. Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis. J Virol. 2001; 75(8): 3501-3508. [80] Marovich M, Grouard-Vogel G, Louder M, Eller M, Sun W, Wu SJ, Putvatana R, Murphy G, Tassaneetrithep B, Burgess T, Birx D, Hayes C, Schlesinger-Frankel S and Mascola J. Human dendritic cells as targets of dengue virus infection. J Investig Dermatol Symp Proc. 2001; 6(3): 219224. [81] Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, van Kooyk Y and Figdor CG. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000; 100(5): 575-585. [82] Geijtenbeek TB, Krooshoop DJ, Bleijs DA, van Vliet SJ, van Duijnhoven GC, Grabovsky V, Alon R, Figdor CG and van Kooyk Y. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol. 2000; 1(4): 353-357. [83] Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, Kewal Ramani VN, Littman DR, Figdor CG and van Kooyk Y. DC-SIGN, a dendritic cellspecific HIV-1-binding protein that enhances transinfection of T cells. Cell. 2000; 100(5): 587-597.

[86] Lozach PY, Lortat-Jacob H, de Lacroix de Lavalette A, Staropoli I, Foung S, Amara A, Houles C, Fieschi F, Schwartz O, Virelizier JL, Arenzana-Seisdedos F and Altmeyer R. DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J Biol Chem. 2003; 278(22): 20358-20366. [87] Halary F, Amara A, Lortat-Jacob H, Messerle M, Delaunay T, Houles C, Fieschi F, ArenzanaSeisdedos F, Moreau JF and Dechanet-Merville J. Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity. 2002; 17(5): 653664. [88] Klimstra WB, Nangle EM, Smith MS, Yurochko AD and Ryman KD. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell derived viruses. J Virol. 2003; 77(22): 12022-12032. [89] de Parseval A, Su SV, Elder JH and Lee B. Specific interaction of feline immunodeficiency virus surface glycoprotein with human DC-SIGN. J Virol. 2004; 78(5): 2597-2600. [90] Appelmelk BJ, van Die I, van Vliet SJ, Vandenbroucke-Grauls CM, Geijtenbeek TB and van Kooyk Y. Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells. J Immunol. 2003; 170(4): 1635-1639. [91] Bergman MP, Engering A, Smits HH, van Vliet SJ, van Bodegraven AA, Wirth HP, Kapsenberg ML, Vandenbroucke-Grauls CM, van Kooyk Y and Appelmelk BJ. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med. 2004; 200(8): 979-990.

[84] Alvarez CP, Lasala F, Carrillo J, Muniz O, Corbi AL and Delgado R. C-type lectins DC-SIGN and LSIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol. 2002; 76(13): 6841-6844.

[92] Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B and Neyrolles O. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med. 2003; 197(1): 121127.

[85] Pohlmann S, Zhang J, Baribaud F, Chen Z, Leslie GJ, Lin G, Granelli-Piperno A, Doms RW, Rice CM and McKeating JA. Hepatitis C virus glycoproteins interact with DC-SIGN and DCSIGNR. J Virol. 2003; 77(7): 4070-4080.

[93] Geijtenbeek TB, Van Vliet SJ, Koppel EA, SanchezHernandez M, Vandenbroucke- Grauls CM, Appelmelk B and Van Kooyk Y. Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med. 2003; 197(1): 7-17.

132

Dengue Bulletin – Vol 29, 2005

Mammalian Dengue Virus Receptors [94]

Kaufmann SH and Schaible UE. A dangerous liaison between two major killers: Mycobacterium tuberculosis and HIV target dendritic cells through DC-SIGN. J Exp Med. 2003; 197(1): 1-5.

[95]

van Die I, van Vliet SJ, Nyame AK, Cummings RD, Bank CM, Appelmelk B, Geijtenbeek TB and van Kooyk Y. The dendritic cell-specific Ctype lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology. 2003; 13(6): 471478.

[96]

Colmenares M, Puig-Kroger A, Pello OM, Corbi AL and Rivas L. Dendritic cell (DC)-specific intercellular adhesion molecule 3 (ICAM-3)grabbing nonintegrin (DC-SIGN, CD209), a Ctype surface lectin in human DCs, is a receptor for Leishmania amastigotes. J Biol Chem. 2002; 277(39): 36766-36769.

[97]

[98]

[99]

Cambi A, Gijzen K, de Vries JM, Torensma R, Joosten B, Adema GJ, Netea MG, Kullberg BJ, Romani L and Figdor CG. The C-type lectin DCSIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J Immunol. 2003; 33(2): 532-538. Serrano-Gomez D, Dominguez-Soto A, Ancochea J, Jimenez-Heffernan JA, Leal JA and Corbi AL. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol. 2004; 173(9): 5635-5643. Curtis BM, Scharnowske S and Watson AJ. Sequence and expression of a membraneassociated C-type lectin that exhibits CD4independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc Natl Acad Sci USA. 1992; 89(17): 83568360.

zones of the paracortex of human lymph nodes. Am J Pathol. 2004; 164(5): 1587-1595. [102] van Kooyk Y and Geijtenbeek TB. DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol. 2003; 3(9): 697-709. [103] Soilleux EJ, Morris LS, Leslie G, Chehimi J, Luo Q, Levroney E, Trowsdale J, Montaner LJ, Doms RW, Weissman D, Coleman N and Lee B. Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J Leukoc Biol. 2002; 71(3): 445-457. [104] Soilleux EJ and Coleman N. Langerhans cells and the cells of Langerhans cell histiocytosis do not express DC-SIGN. Blood. 2001; 98(6): 19871988. [105] Miagostovich MP, Ramos RG, Nicol AF, Nogueira RM, Cuzzi-Maya T, Oliveira AV, Marchevsky RS, Mesquita RP and Schatzmayr HG. Retrospective study on dengue fatal cases. Clin Neuropathol. 1997; 16(4): 204-208. [106] Jessie K, Fong MY, Devi S, Lam SK and Wong KT. Localization of dengue virus in naturally infected human tissues, by immuno-histochemistry and in situ hybridization. J Infect Dis. 2004; 189(8): 1411-1418. [107] Soilleux EJ, Barten R and Trowsdale J. DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol. 2000; 165(6): 2937-2942. [108] Van Liempt E, Imberty A, Bank CM, Van Vliet SJ, Van Kooyk Y, Geijtenbeek TB and Van Die I. Molecular basis of the differences in binding properties of the highly related C-type lectins DC-SIGN and L-SIGN to Lewis X trisaccharide and Schistosoma mansoni egg antigens. J Biol Chem. 2004; 279(32): 33161-33167.

[100] Engering A, Van Vliet SJ, Geijtenbeek TB and Van Kooyk Y. Subset of DC-SIGN(+) dendritic cells in human blood transmits HIV-1 to T lymphocytes. Blood. 2002; 100(5): 1780-1786.

[109] Guo Y, Feinberg H, Conroy E, Mitchell DA, Alvarez R, Blixt O, Taylor ME, Weis WI and Drickamer K. Structural basis for distinct ligandbinding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat Struct Mol Biol. 2004; 11(7): 591-598.

[101] Engering A, van Vliet SJ, Hebeda K, Jackson DG, Prevo R, Singh SK, Geijtenbeek TB, van Krieken H and van Kooyk Y. Dynamic populations of dendritic cell-specific ICAM-3 grabbing nonintegrin-positive immature dendritic cells and liver/lymph node-specific ICAM-3 grabbing nonintegrin-positive endothelial cells in the outer

[110] Bashirova AA, Geijtenbeek TB, van Duijnhoven GC, van Vliet SJ, Eilering JB, Martin MP, Wu L, Martin TD, Viebig N, Knolle PA, KewalRamani VN, van Kooyk Y and Carrington M. A dendritic cell-specific intercellular adhesion molecule 3grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal

Dengue Bulletin – Vol 29, 2005

133

Mammalian Dengue Virus Receptors endothelial cells and promotes HIV-1 infection. J Exp Med. 2001; 193(6): 671-678.

patients with dengue fever: analysis of 1,585 cases. Braz J Infect Dis. 2004; 8(2): 156-163.

[111] Knolle PA and Limmer A. Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells. Trends Immunol. 2001; 22(8): 432-437.

[120] Lin YL, Liu CC, Lei HY, Yeh TM, Lin YS, Chen RM, Liu HS. Infection of five human liver cell lines by dengue-2 virus. J Med Virol. 2000; 60(4): 425-431.

[112] Cormier EG, Durso RJ, Tsamis F, Boussemart L, Manix C, Olson WC, Gardner JP and Dragic T. LSIGN (CD209L) and DC-SIGN (CD209) mediate transinfection of liver cells by hepatitis C virus. Proc Natl Acad Sci USA. 2004; 101(39): 1406714072. [113] Couvelard A, Marianneau P, Bedel C, Drouet MT, Vachon F, Henin D and Deubel V. Report of a fatal case of dengue infection with hepatitis: demonstration of dengue antigens in hepatocytes and liver apoptosis. Hum Pathol. 1999; 30(9): 1106-1110. [114] Rosen L, Drouet MT and Deubel V. Detection of dengue virus RNA by reverse transcriptionpolymerase chain reaction in the liver and lymphoid organs but not in the brain in fatal human infection. Am J Trop Med Hyg. 1999; 61: 720-724. [115] Kangwanpong D, Bhamarapravati N and Lucia HL. Diagnosing dengue virus infection in archived autopsy tissues by means of the in situ PCR method: a case report. Clin Diagn Virol. 1995; 3(2): 165-172. [116] Huerre MR, Lan NT, Marianneau P, Hue NB, Khun H, Hung NT, Khen NT, Drouet MT, Huong VT, Ha DQ, Buisson Y and Deubel V. Liver histopathology and biological correlates in five cases of fatal dengue fever in Vietnamese children. Virchows Arch. 2001; 438(2): 107-115. [117] Kalayanarooj S. and Nimmannitya S. Clinical and laboratory presentations of dengue patients with different serotypes. Dengue Bulletin. 2000; 24: 53-59. [118] Kalayanarooj S, Vaughn DW, Nimmannitya S, Green S, Suntayakorn S, Kunentrasai N, Viramitrachai W, Ratanachu-eke S, Kiatpolpoj S, Innis BL, Rothman AL, Nisalak A and Ennis FA. Early clinical and laboratory indicators of acute dengue illness. J Infect Dis. 1997; 176(2): 313321. [119] Souza LJ, Alves JG, Nogueira RM, Gicovate Neto C, Bastos DA, Siqueira EW, Souto Filho JT, Cezario Tde A, Soares CE and Carneiro Rda C. Aminotransferase changes and acute hepatitis in

134

[121] Nguyen TL, Nguyen TH, Tieu NT. The impact of dengue haemorrhagic fever on liver function. Res Virol. 1997; 148(4): 273-277. [122] Marianneau P, Flamand M, Deubel V and Despres P. Apoptotic cell death in response to dengue virus infection: the pathogenesis of dengue haemorrhagic fever revisited. Clin Diagn Virol. 1998; 10(2-3): 113-119. [123] Marianneau P, Megret F, Olivier R, Morens DM and Deubel V. Dengue 1 virus binding to human hepatoma HepG2 and simian Vero cell surfaces differs. J Gen Virol. 1996; 77(Pt 10): 2547-2554. [124] Clayton RF, Rinaldi A, Kandyba EE, Edward M, Willberg C, Klenerman P and Patel AH. Liver cell lines for the study of hepatocyte functions and immunological response. Liver Int. 2005; 25(2): 389-402. [125] Shuda M, Kondoh N, Imazeki N, Tanaka K, Okada T, Mori K, Hada A, Arai M, Wakatsuki T, Matsubara O, Yamamoto N and Yamamoto M. Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: a possible involvement of the ER stress pathway in hepatocarcinogenesis. J Hepatol. 2003; 38(5): 605-614. [126] Ozaki I, Yamamoto K, Mizuta T, Kajihara S, Fukushima N, Setoguchi Y, Morito F and Sakai T. Differential expression of laminin receptors in human hepatocellular carcinoma. Gut. 1998; 43(6): 837-842. [127] Lin YL, Liu CC, Chuang JI, Lei HY, Yeh TM, Lin YS, Huang YH and Liu HS. Involvement of oxidative stress, NF-IL-6, and RANTES expression in dengue-2-virus-infected human liver cells. Virology. 2000; 276(1): 114-126. [128] Marianneau P, Cardona A, Edelman L, Deubel V and Despres P. Dengue virus replication in human hepatoma cells activates NF-kappaB which in turn induces apoptotic cell death. J Virol. 1997; 71(4): 3244-3249. [129] Marianneau P, Steffan AM, Royer C, Drouet MT, Kirn A and Deubel V. Differing infection patterns of dengue and yellow fever viruses in a human hepatoma cell line. J Infect Dis. 1998; 178(5): 1270-1278.

Dengue Bulletin – Vol 29, 2005

Mammalian Dengue Virus Receptors [130] Thongtan T, Panyim S and Smith DR. Apoptosis in dengue virus infected liver cell lines HepG2 and Hep3B. J Med Virol. 2004; 72(3): 436-444. [131] Ardini E, Pesole G, Tagliabue E, Magnifico A, Castronovo V, Sobel ME, Colnaghi MI and Menard S. The 67-kDa laminin receptor originated from a ribosomal protein that acquired a dual function during evolution. Mol Biol Evol. 1998; 15(8): 1017-1025. [132] Buto S, Tagliabue E, Ardini E, Magnifico A, Ghirelli C, van den Brule F, Castronovo V, Colnaghi MI, Sobel ME and Menard S. Formation of the 67kDa laminin receptor by acylation of the precursor. J Cell Biochem. 1998; 69(3): 244-251. [133] Ozaki I, Yamamoto K, Mizuta T, Kajihara S, Fukushima N, Setoguchi Y, Morito F and Sakai T. Differential expression of laminin receptors in human hepatocellular carcinoma. Gut. 1998; 43(6): 837-842. [134] Wang KS, Kuhn RJ, Strauss EG, Ou S and Strauss JH. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol. 1992; 66(8): 4992-5001. [135] Ludwig GV, Kondig JP and Smith JF. A putative receptor for Venezuelan equine encephalitis virus from mosquito cells. J Virol. 1996; 70(8): 5592-5599. [136] Gauczynski S, Peyrin JM, Haik S, Leucht C, Hundt C, Rieger R, Krasemann S, Deslys JP, Dormont D, Lasmezas CI and Weiss S. The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J. 2001; 20(21): 5863-5875.

Dengue Bulletin – Vol 29, 2005

[137] Kim KJ, Chung JW and Kim KS. 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J Biol Chem. 2005; 280(2): 1360-1368. [138] Hundt C, Peyrin JM, Haik S, Gauczynski S, Leucht C, Rieger R, Riley ML, Deslys JP, Dormont D, Lasmezas CI and Weiss S. Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor. EMBO J. 2001; 20(21): 5876-5886. [139] Lee AS. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods. 2005; 35(4): 373-381. [140] Triantafilou K, Fradelizi D, Wilson K and Triantafilou M. GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J Virol. 2002; 76(2): 633-643. [141] Misra UK, Chu CT, Gawdi G and Pizzo SV. Evidence for a second alpha 2-macroglobulin receptor. J Biol Chem. 1994; 269(17): 1254112547. [142] Sakuntabhai A, Turbpaiboon C, Casademont I, Chuansumrit A, Lowhnoo T, Kajaste-Rudnitski A, Kalayanarooj SM, Tangnararatchakit K, Tangthawornchaikul N, Vasanawathana S, Chaiyaratana W, Yenchitsomanus PT, Suriyaphol P, Avirutnan P, Chokephaibulkit K, Matsuda F, Yoksan S, Jacob Y, Lathrop GM, Malasit P, Despres P and Julier C. A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet. 2005; 37(5): 507-513.

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