Pineal Melatonin Rhythms in Female Turkish Hamsters: Effects of ...

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Syrian hamster. (Mesocricetus auratus) results in continuous mainte- nance ... 2#{176}C.All hamsters were supplied with food. (Wayne. Lab. Blox or Purina.
BIOLOGY

OF

35, 74-83

REPRODUCTION

Pineal

(1986)

Melatonin

Rhythms

Effects

of Photoperiod

JANET

in Female

M. DARROW,2

J.

MARILYN Worcester

and

Turkish Hibernation’

LAWRENCE

DUNCAN,4

and

Foundation

for

Shrewsbury,

Hamsters:

TAMARKIN,3

BRUCE

D. GOLDMAN4

Experimental

Biology24

Massachusetts

01545

and Clinical National

Psychobiology Branch3 Institute of Mental Health

Bethesda,

Maryland

20205

ABSTRACT Daily rhythms of pineal and serum melatonin content were characterized for adult female Turkish hamsters (Mesocricetus brandti) exposed to long days (16L:8D, 22#{176}C)or after transfer to short days (IOL:14D, 22#{176}C). The nocturnal peak of pineal melatonin content was found to be approximately 3 h greater in duration on short than on long days. Changes in levels of serum melatonin closely paralleled those of pineal melatonin. Thus, an effect of photoperiod on synthesis and secretion of pineal melatonin was demonstrated. In a separate experiment, female hamsters were induced to hibernate by exposure to a short-day, cold environment (1OL: 14D, 6#{176}C).During the 4 to por (body temperature

5-mo

37#{176}C). Little during torpor.

of

tonin

evidence However,

rhythms

absence

=

no

of pineal

appropriately

hibernation season, Turkish hamsters are 7-9#{176}C) alternating with 1 to 3-day intervals

nocturnal animals

different

in phase

melatonin

phased,

synthesis or secretion sampled during the first

output

rhythmic

or amplitude during

melato

from

torpor,

nm

the

signal

during

those pineal

number of seasonally breeding Goldman and Darrow, 1983; son and Watson-Whitmyre, cek,

1985;

sters

and

tion

of

critical veys

Tamarkinet in sheep, the

feature daylength

al., it has

nocturnal

1985).

pineal

of a pineal information

In Djungarian

proposed

that

melatonin

endocrine (Bittman

hamthe

peak

signal

durais the

which et

al.,

1983; 1984). unlike results

assay HD

15912

held

in females sampled bout displayed mela-

at 22#{176} C. Thus, Turkish

hamsters

despite

the

produces

an

of euthermia.

to pinealectomy, it was of interest daily rhythm of pineal melatonin con-

tent in this species on long vs. short days, for comparison with melatonin patterns already characterized in other species. Furthermore, since it has been suggested that pineal melatonin in mammals is secreted predominantly 1978),

Accepted November 12, 1985. Received August 12, 1985. ‘This research was supported by NIH Research Grant BDG. 2 Reprint requests: Janet M. Darrow, Ph.D., Worcester for Experimental Biology, 222 Maple Avenue, Shrewsbury,

in females of hibernating

Turkish hamsters to examine the

con-

Carter and Goldman, 1983a,b; Goldman et al., In the Turkish hamster (Mesocricetus brandti), other mammals tested to date, pinealectomy

melatonin was detected arousal from a torpor

of tor= 35-

in gonadal regression on long days, indicating that the pineal is required for maintenance of gonadal function (Carter et al., 1982). In contrast, removal of the pineal gland in the closely related Syrian hamster (Mesocricetus auratus) results in continuous maintenance of the reproductive system on long days and prevents short-day-induced reproductive regression (Reiter, 1978). Because of the unusual response of

to in a

mammals (Reiter, 1980; Karsch et al., 1984; Stet1984; lllnerova and Vane-

been

seen gland

intervals

INTRODUCTION The daily rhythm of pineal melatonin is known be a component of the photoperiodic mechanism

of pineal day after

known to display 4 to 8-day bouts of euthermia (body temperature

into the peripheral we utilized a recently for serum

melatonin

circulation developed to measure

(Rollag et al., radioimmunocirculating

of the hormone. Turkish hamsters hibernate when exposed short-day, cold environment in the laboratory and Goldman, 1980). The hibernation season

to

Foundation MA 01545.

74

levels to a (Hall is 4-5

MELATONIN

mo in bouts

duration of torpor

and is characterized (lasting 4-8 days)

ly

IN

TURKISH

Uteri

alternating and arousal

were

removed

Radioimmunoassay

(lasting 1-3 days). During torpor, core body temperature drops to as low as 7-9#{176} C, representing a substan-

formed

as

1979),

using

tial decline from body temperatures

generously

arousal. pineal tion, sured

To

the

35-37#{176}C range observed during

investigate

the

of euthermic intervals

of

of torpor

on

consequences

biosynthetic/secretory activity during hibernalevels of pineal and serum melatonin were meain hibernating hamsters during torpor and during

intervals

of arousal.

served those

The

in hibernating measured in

daily

melatonin

hamsters nonhibernating

were

profiles compared animals

obwith housed

at 22#{176}C.

the

adult

brandti) animals

were were

period 22 ± (Wayne

Turkish

hamsters

man

(Mesocricetus

obtained from our breeding colony. The raised from birth on a long-day photo-

(16L:8D, 2#{176}C.All Lab

water

lights hamsters

Blox

on

or

from were

Purina

0200 to supplied Chow

No.

1800 with

h) at food

5008)

and

on Long

I. Pineal and Short

Female monitored following

for

ranging this

in age

study.

by daily examination the method of Orsini

of the experiment, ted for the study days. This proportion

39% were

from

Estrous

1.5

to

further killed

43

was

of vaginal discharges (1961). At the onset

(60/15 3) of the females selecfound to be acyclic on long of anovulatory females is typi-

cyclic females were left All animals were checked

period of 5-6 by decapitation

which

al., was

hamsters

(2-4

mo

of

age)

wk, animals the night,

days

decapitated dim red

and pineals. and February.

at

were

were

using

using

melatonin

analog

by

antiserum

Brown

the

(Gold(Meloy

NJ) and R1055 Serum melatonin R1056,

by Dr. Rollag. Serum samples with 2.5 ml dichioromethane described

at

previously

1-melatonin

125

sampled

performed

as described

1984),

After

various times for collection

light,

Inc., Springfield, supplied by M. D. Rollag.

measured

(16L:8D).

Animals

assays

Foundation

et al.,

supplied extracted

on long

were under

melatonin

Laboratories, antiserum was

left

et

also

(300 p1) were according to a al.

(1983),

and

was determined by double antibody procedures (Darrow and Goldman,

3 mo

cyclicity

cal for our colony of Turkish hamsters. Thirty-one acyclic and 50 cycling females were transferred to a short-day light schedule (1OL:14D, lights from 0500-1500 h, 22#{176}C), and the remaining acyclic and day schedule.

et

R1055,

1986).

Days

hamsters

selected

per-

by Dr. M. D. Rollag.

melatonin content radioimmunoassay

Melatonin

weighed. was

(Tamarkin

antiserum

were

procedure

ad libitum.

Experiment

were

female

and

melatonin

previously

female

remainder

Worcester

Young

females

were selected for this study. Estrous cyclicity was not monitored in these females. Thirty-eight females were transferred to short days (1OL:14D, as above), and

Pineal Animals

pineal

II. Pineal and Serum on Long and Short Days

of trunk blood during January

METHODS

most

for melatonin

Seventy-three

during AND

from

described supplied

Experiment Melatonin

4-5

MATERIALS

75

HAMSTERS

on the daily

on 29

longfor a

wk, at which time they were at various times of day. At

Experiment III.Melatonin Rhythms During Hibernation Ninety selected

females for study.

ranging After

in age from 2-4 mo a 6-wk prior exposure

were to

short days transferred short-day

(1OL:14D, 22#{176}C),groups of females were to a cold room (6 ± 1#{176}C) with an identical photoschedule. Hamsters were housed

separately

in 48

containing

X

25

X

Absorb-Dri

21

cm

bedding

polycarbonate and

cages,

cotton

nesting

material. Individuals were checked for torpor each day at 2-4 hours before lights-off. Torpid hamsters were readily identified by their reduced respiration rate and lack of response to a puff of air detected at the

animal’s

back

(Hall

and

Goldman,

1980).

This

each time point, 2-8 females of each reproductive state were sampled on both long and short days. During the dark portion of the light/dark cycle, hamsters were killed under dim red illumination.

method of detecting torpor has been corroborated by telemetric recording of body temperature (Hall, 1981). Those individuals exhibiting torpor for at least

Pineals were vials on dry

tated at 4-h intervals, of torpor, or during

rapidly ice, then

excised stored

and frozen in at -20#{176}C until

separate assayed.

10

days

in

a preceding

20-day

interval

were

decapi-

either on Day 2 or 3 of a bout the first day after spontaneous

76

DARROW

arousal

from

collected

torpor.

as

in

Pineals

and

previous

trunk

studies.

blood

Some

(16/90) showed less than 10 days of torpor days of cold exposure. These females were nonhibernators, The

and

cold

March

room

were

portion

sampled

at

the

experiment

of

were

hamsters during 60 designated

3 times

of day. ran

from

6-week study. of “spontaneous”

Thus,

on

that

to short

long

days,

it appears

Statistical tests employed were chi square, linear gression analysis and one-way analysis of variance by the

Duncan

posteriori

test

for

exposure

despite acyclicity days

inhibited of female

reproductive activity in a significant Turkish hamsters (p< 0.01). Uterine

number weights

for

of the

sampled

most

females

in Table

whose 1. On each

weights of acyclic females were as compared to those of cycling

Analysis

lowed

came acyclic during the the rather high incidence

are presented

to July.

Data

ET AL.

pineals

were

photoperiod

uterine

significantly reduced hamsters (p