AJP - Regu Fuel your research with LabChart
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Am J Physiol Regul Integr Comp Physiol 290: R1714-R1719, 2006. First published January 12, 2006; doi:10.1152/ajpregu.00869.2005
0363-6119/06 $8.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
290/6/R1714    most recent
00869.2005v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (10)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Weil, Z. M.
Right arrow Articles by Nelson, R. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Weil, Z. M.
Right arrow Articles by Nelson, R. J.

COMPARATIVE AND EVOLUTIONARY PHYSIOLOGY

Perinatal photoperiod organizes adult immune responses in Siberian hamsters (Phodopus sungorus)

Zachary M. Weil, Leah M. Pyter, Lynn B. Martin, II, and Randy J. Nelson

Departments of Neuroscience and Psychology, and Institute for Behavioral Medicine Research, The Ohio State University, Columbus, Ohio

Submitted 12 December 2005 ; accepted in final form 6 January 2006


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Individuals of many nontropical rodent species display reproductive, immunological, and somatic responses to day length. In general, short day (SD) lengths inhibit reproduction and enhance immune function in the laboratory when all other conditions are held constant. Most studies to date have focused on seasonal variation in immune function in adulthood. However, perinatal photoperiods also communicate critical day length information and serve to establish a developmental trajectory appropriate for the time of year. Nontropical rodents born early in the breeding season undergo rapid reproductive development, presumably to promote mating success during their first reproductive season. Rodents born late in the breeding season suspend somatic growth and puberty until the following vernal breeding season. We tested the hypothesis that perinatal day lengths have similar enduring effects on the immune system of rodents. Siberian hamsters (Phodopus sungorus) were maintained prenatally and until weaning (21 days) in either SDs (8 h light:16 h dark) or long days (LD) (16 h light:8 h dark), then they were weaned into either the opposite photoperiod or maintained in their natal photoperiod, forming four groups (LD-LD, LD-SD, SD-LD, and SD-SD). After 8-wk in these conditions, cell-mediated immune activity was compared among groups. SD-SD hamsters of both sexes enhanced immune function relative to all other groups. The reproductive effects of perinatal photoperiod were not evident by the end of the experiment; circulating testosterone and cortisol sampled at the end of the experiment reflected the postweaning, but not the perinatal photoperiod. This experiment demonstrates long-lasting organizational effects of perinatal photoperiod on the rodent immune system and indicates that photoperiod-induced changes in the immune system are dissociable from changes in the reproductive system.

photoperiodism; seasonality; melatonin; delayed-type hypersensitivity

MANY NONTROPICAL ANIMALS DISPLAY annual variation in reproductive and immune activity. Winter represents an energetic bottleneck, wherein increased thermoregulatory requirements coincide with reduced energy availability (7). Therefore, during the spring and summer, which encompasses much of the breeding season for small, nontropical vertebrates, investments are biased toward reproductive activities; however, during late autumn and winter, resources are diverted to traits promoting over-winter survival. In the laboratory, many seasonal physiological and behavioral responses can be induced by manipulating day length (photoperiod) (21). Photoperiod information is transduced into a physiological signal via nocturnal secretion of pineal melatonin (11). Short day (SD) lengths (<12.5 h light/day) inhibit reproductive function, but enhance several aspects of immune function (21).

Adult Siberian hamsters (Phodopus sungorus) housed in SD lengths enhance delayed-type hypersensitivity (DTH; an index of cell-mediated immune activity) responses (2). The majority of research on seasonality of immune function has focused on photoperiod-induced differences in adult animals born and raised in long days (LDs) (but see Refs. 23 and 27) that experience photoperiod manipulation in adulthood. Early-life photoperiods are also important sources of seasonal information and can establish an individual’s developmental trajectory by regulating somatic and reproductive development (6). Because the adaptations associated with investing in reproduction or survival mechanisms are generally mutually exclusive, it is useful for small animals to follow the appropriate seasonal developmental trajectory soon after birth. Siberian hamsters born late in the breeding season delay puberty until the following spring, whereas hamsters born early in the season undergo rapid reproductive development, presumably to have the opportunity to mate before autumn (12). Photoperiod information is communicated in utero to Siberian hamster pups (15) via the maternal melatonin rhythm. In addition to regulation of developmental processes, early-life photoperiod also affects reproductive (15) and affective (28) responses to day lengths later in life. Intermediate day lengths (e.g., 14 h) occur at both the beginning and the end of the breeding season; thus the same day lengths forecast very different environmental conditions. Photoperiodic rodents solve this problem by comparing ambient day length to a reference day length that is encoded prenatally via a mechanism termed photoperiod history (15, 25, 31). Thus for the reproductive system of seasonally breeding rodents, the direction of photoperiodic change is more important than the absolute day length (24).

The present study was designed to examine the enduring effects of perinatal (the period from conception to weaning) photoperiod on cell-mediated immune function in adulthood. Animals were born in either SD or LD and maintained in their natal photoperiod until weaning, at which time they were either left in their birth photoperiod or they were transferred to the opposite lighting condition. The hamsters were housed in the adult photoperiod for 8 wk before immune challenge to allow the reproductive system to adjust to the adult photoperiod treatment. We hypothesized that perinatal exposure to photoperiods would alter the immunological responses to day length in adulthood. Specifically, we predicted that 1) perinatal SDs would enhance DTH responses in all groups, but to a greater extent in hamsters housed in SDs following weaning; and 2) exposure to LD lengths perinatally would attenuate adult SD-induced elevated immune function.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Animals

Hamsters (P. sungorus) in this study were bred in our colony at the Ohio State University from a wild-bred stock obtained from Dr. K. Wynne-Edwards, Queen’s University, Kingston, Ontario, Canada. Animals were housed in polypropylene cages (28 x 17 x 12 cm) in colony rooms with constant temperature (21 ± 4°C) and humidity (50 ± 10%) and had ad libitum access to food (Harlan Teklad 8640 Rodent Diet, Indianapolis, IN) and filtered tap water. All studies were conducted with approval of the Ohio State Institutional Laboratory Animal Care and Use Committee and were conducted in compliance with all U.S. federal animal welfare requirements.

Breeding pairs were established in rooms illuminated with either long (16 h light/day; LD) or short (8 h light/day; SD) photoperiods. Pairs were inspected daily for the presence of pups, and the day of birth was designated day 0. Pups were weaned at day 21 into either the opposite photoperiod (i.e., SD animals transferred to LD) or maintained in the perinatal photoperiod (i.e., SD animals remained in SD). Pups from each litter were distributed between the photoperiod groups in a pseudorandom fashion. No more than three pups of a single sex from any litters were used in any group. These photoperiodic manipulations produced four groups. Hamsters born in LD were either maintained in LD after weaning (LD-LD, n = 8 females, 11 males), or transferred to SD (LD-SD, n = 6 females, 11 males). Hamsters born in SD either remained in SD (SD-SD, n = 13 females, 14 males) or were moved into LD (SD-LD, n = 10 females, 9 males). The time of lights off was the same for both photoperiod treatments (1500 Eastern Standard Time). Experimental animals were individually housed at weaning and remained in their respective postweaning photoperiods for the remainder of the experiment. Seventeen litters were used to form the groups.

Experimental Procedures

Induction of DTH. DTH was induced by application of 2,4-dinitro-1-fluorobenzene (DNFB; Sigma) to the right pinna of each hamster after initial sensitization by application of DNFB to the dorsum. Sensitization was induced and DTH elicited as follows: following 8 wk of postweaning photoperiod treatment, all hamsters were anesthetized with isoflurane vapors, and an area ~2 x 3 cm was shaved on the dorsum. Twenty-five microliters of DNFB [0.5% (wt/vol) in 4:1 acetone-olive oil vehicle] was applied to the dorsal skin on 2 consecutive days. Seven days later, baseline thickness of both pinnae was measured in lightly anesthetized hamsters with a constant-loading dial micrometer (Long Island Indicator Service, Hauppauge, NY). Immediately after baseline pinnae thickness measurements were obtained, 20 µl of DNFB [0.2% (wt/vol) in 4:1 acetone-olive oil] were applied to the skin of the dorsal surface of the right pinna. Left pinnae were treated with vehicle. Pinnae thickness was measured every 24 h for the next 7 days. Pinnae thickness values obtained on each day following challenge were expressed as a percentage of baseline thickness. All DNFB treatments and pinna measurements were performed between 1300 and 1500, and all measurements were made on the same region of the pinna by the same person (Z. M. Weil). The DTH response in hamsters is extremely sensitive to stressors or increases in glucocorticoids; to minimize stress responses, hamsters were brought into the testing room one at a time.

Reproductive and somatic responses to photoperiod. Following the conclusion of DTH measurements, animals were weighed, and pelages were scored on a scale from 1 to 5 (1 = dark, summer coat color; 5 = white, winter coat color) in whole integers for each group (10, 28). Hamsters were then deeply anesthetized with isoflurane vapors and killed by rapid decapitation, and trunk blood was collected. Reproductive tissues (testes and epididymal fat pads in males and uteri and ovaries in females) were removed, cleaned of connective tissue, and weighed to the nearest 0.1 mg. All animals housed in short photoperiods as adults having testes or uterine masses falling 2 standard deviations below the LD mean were considered reproductively responsive to short photoperiods. Any animals housed in a short photoperiod as adults whose testes or uterine mass fell within the range of the mean minus 2 standard deviations of the long photoperiod group were considered reproductive nonresponders and were excluded from further analyses. One male (LD-SD) and one female (SD-SD) were reproductively nonresponsive and were excluded.

An additional group of hamsters was used to verify that perinatal photoperiod treatment alone had an effect on reproductive morphology. To confirm this, a separate group of hamsters born in SD or LD was killed at weaning by cervical dislocation at 21 days of age, and their reproductive tissues were removed and weighed.

RIA procedures. Trunk blood samples were allowed to clot for 30 min; then they were centrifuged for 30 min at 2,500 rpm, and supernatants were stored in polypropylene microcentrifuge tubes at –70°C. Serum testosterone concentrations (from males) were determined in a single assay using a Diagnostic Systems Laboratories (Webster, TX) 125I double-antibody kit. The intra-assay coefficient of variation was <5%. Serum cortisol concentrations were determined in a single assay using a Diagnostic Systems Laboratories 125I double-antibody kit. The intra-assay coefficient of variation was <5%. Both kits have been validated previously for use in this species (29).

Data Analyses and Statistics

Reproductive tissue weights and testosterone concentrations were analyzed with a two-way (perinatal photoperiod x postweaning photoperiod) ANOVA separately for each sex. Spleen mass, final body mass, pelage score, and serum cortisol concentrations were analyzed with three-factor ANOVAs (sex x perinatal photoperiod x postweaning photoperiod). All tissue weights were corrected for final body mass before statistical comparisons. Testis length was analyzed with repeated-measures ANOVA for perinatal and adult photoperiod manipulation. DTH reactions were compared between sex and group with repeated-measures ANOVA using litter as a covariate. However, litter had no effect on any measure and was removed from subsequent analyses. Following a significant F score, repeated-measures data were analyzed with sequential Bonferroni multiple-comparison tests; differences were not considered statistically significant unless P < 0.0083. Within days and between groups, multiple comparisons that were planned a priori were conducted with Tukey’s honestly significant difference tests. All comparisons other than the Bonferroni test results were considered significant if P ≤ 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 GRANTS
 REFERENCES
 
Reproductive Responses

After 10 wk of housing in their respective postweaning photoperiods, females were significantly lighter than males [F(1,81) = 60.143, P < 0.0001 data not shown]. Hamsters housed in SD as adults were lighter than those in LD, regardless of perinatal photoperiod [F(1,81) = 106.235, P < 0.0001; data not shown].

Perinatal exposure to SDs reduced both testis [F(1,12) = 859.938, P < 0.0001; Fig. 1A] and uterine mass [F(1,14) = 32.637, P < 0.0001; Fig. 1B] in animals killed at weaning. However, by the end of the experiment (10 wk postweaning), only adult photoperiod affected paired testis weight, such that animals housed in LD as adults had larger testes than those housed in SD as adults, regardless of the perinatal photoperiod [F(1,44) = 578.64, P < 0.0001, Fig. 2]. Similarly, the size of the epididymal fat pads was affected by postweaning photoperiod [F(1,44) = 85.85, P < 0.0001, data not shown], but not perinatal photoperiod (P > 0.05). In females, uterine mass was also reduced by exposure to SD as adults, independent of perinatal photoperiod treatment [F(1,37) = 30.42, P < 0.0001, Fig. 2]. Ovarian mass was not affected by photoperiod treatment in any developmental periods (P > 0.05 for both perinatal and adult photoperiods). Pelage scores were significantly lower in all animals housed in SD as adults, irrespective of sex [F(1,79) = 438.675, P < 0.0001, data not shown], but no enduring effects of perinatal photoperiod were evident for pelage score. Only spleen mass was increased by perinatal exposure to SD [F(1,79) = 5.325, P = 0.025, Fig. 3], and this result was independent of both sex and adult photoperiod exposure.


Figure 1
View larger version (13K):
[in this window]
[in a new window]
  		Fig. 1. Perinatal exposure to short days (SDs) reduced tissue masses at weaning. Means (±SE) are shown of paired testes mass (mg) of male (A) and uterine mass (mg) of female (B) P. sungorus at 21 days of age. ***Significantly different from hamsters housed in long days (LDs) perinatally: P < 0.0001.

 

Figure 2
View larger version (17K):
[in this window]
[in a new window]
  		Fig. 2. Postweaning but not perinatal photoperiod affects means (±SE) uterine mass (mg) of female (A) and testes mass (mg) of male (B) P. sungorus. *Significantly different from hamsters housed in LD as adults (LD-LD and SD-LD): P < 0.05.

 

Figure 3
View larger version (18K):
[in this window]
[in a new window]
  		Fig. 3. Perinatal but not postweaning photoperiod affects spleen mass (mg; means ± SE) of male and female P. sungorus. SD-SD and SD-LD groups significantly different from LD-LD and LD-SD: P < 0.05.

 
Hormones

Testosterone concentrations were reduced in animals housed in SD, regardless of perinatal photoperiod treatment [F(1,40) = 39.165, P < 0.0001; Fig. 4]. However, perinatal exposure to SD reduced circulating testosterone in animals housed in LD as adults, as indicated by a main effect of perinatal photoperiod [F(1,40) = 6.128, P = 0.018] and an interaction between perinatal and adult photoperiods [F(1,40) = 6.213, P = 0.017] on testosterone. Basal cortisol concentrations were higher in hamsters housed in SD as adults relative to those in LD during that period [F(1,62) = 9.812, P = 0.003; Fig. 5]. Perinatal photoperiod treatment and sex did not significantly alter cortisol concentrations (P > 0.05).


Figure 4
View larger version (11K):
[in this window]
[in a new window]
  		Fig. 4. Perinatal and postweaning photoperiods interact to affect serum testosterone concentrations. Means (±SE) are shown of serum testosterone of male P. sungorus (ng/ml). *Significantly different from LD-LD, #significantly different from LD-LD and SD-LD groups: P < 0.05.

 

Figure 5
View larger version (20K):
[in this window]
[in a new window]
  		Fig. 5. Hamsters housed in SDs after weaning had significantly higher serum cortisol (means ± SE) concentrations than the hamsters housed in LDs after weaning. This effect was not modulated by perinatal photoperiod. Shaded bars indicate females, and hatched bars indicate hamsters transferred from their perinatal photoperiod into the opposite day length at weaning. *Hamsters in SD perinatally have significantly higher cortisol concentrations than animals in LD perinatally: P < 0.05.

 
Immune Activity

Both perinatal [F(1,79) = 8.976, P < 0.0001; Fig. 6] and adult photoperiod [F(1,79) = 7.588, P < 0.0001] and the interaction between perinatal and adult photoperiods [F(3,79) = 2.503; P < 0.05] affected DTH responses. The effect of perinatal photoperiod was mediated by an enhanced swelling response in the SD-SD groups of both sexes relative to all other groups. Swelling responses from animals in all other groups did not differ statistically from each other.


Figure 6
View larger version (17K):
[in this window]
[in a new window]
  		Fig. 6. Exposure to SDs both perinatally and postweaning enhances delayed-type hypersensitivity responses (means ± SE expressed as a percentage increase in pinna thickness) for male (A) and female (B) P. sungorus. aSD-SD significantly greater than all other groups, bSD-SD group significantly greater than LD-LD group, cSD-SD significantly different from LD-LD and LD-SD: P < 0.05.

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
Perinatal photoperiod treatment altered immunological responses to day length in adulthood, but these immunological effects were dissociated from photoperiod-induced changes in the reproductive system. Hamsters of both sexes held in SDs throughout the experiment (SD-SD) displayed stronger cell-mediated immune responses relative to all other groups. Adult photoperiod evoked more modest changes in DTH responses. Reproductive tissue masses, on the other hand, were affected exclusively by adult photoperiod. No persistent effects of perinatal photoperiod were detected on reproductive tissues, even though testosterone was markedly decreased and reproductive development was inhibited (as indicated by smaller testis length at weaning) in male hamsters housed in SDs perinatally.

This experiment was designed to determine whether or not the immune system was attending to perinatal photoperiod cues, even after extended housing in a different photoperiod after weaning. Enhanced DTH responses alone are not necessarily indicative of some global increase in "immunocompetence." Assays of other aspects of the immune system would be necessary to determine whether this effect is generalizable. However, it is clear from the data here that the specific immunological processes involved in producing the DTH response are permanently altered by perinatal day lengths. However, the DTH response is not without meaning, as it incorporates immunological memory, cell proliferation, antigen presentation, leukocyte trafficking, and inflammatory processes into an integrative measure. DTH responses are associated with resistance to bacteria, fungi, and viruses (9).

Photoperiodic conditions early in life and in adulthood can be conceptualized as having organizational and activational effects on the immune system, respectively (23). In the present study, SDs early in life were necessary for the expression of SD-induced enhancement of immune function. However, perinatal SD lengths were not sufficient to elevate DTH responses in LD hamsters. These results are reminiscent of the effects of testosterone on male mating behavior in rats. That is, testosterone early in life is necessary to organize the neural substrate on which testosterone in adulthood can activate the neural circuits associated with mating (13).

The critical photoperiod information encoded by hamsters in this study was likely communicated during prenatal development. Transfer of photoperiod information occurs prenatally via the maternal melatonin rhythm. Pinealectomy abolishes prenatal photoperiodic effects on reproductive development (16), and cross-fostering experiments have revealed that pups respond to the photoperiod of birth, rather than the photoperiod experienced by the foster dam (14). Siberian hamster pups are responsive to maternal melatonin infusions in utero during the period between ~6 and 2 days before birth (34). Following birth, pups are unable to produce melatonin in response to photoperiod information until ~15 days of age (36). Gonadal responses to postnatal photoperiods first occur at ~20 days (35). Taken together, these results suggest that maternal melatonin rhythm in utero is responsible for programming the immunological differences detected in adulthood. Early exposure to long-duration melatonin signal may be the proximate mediator of the effect of early day lengths on adult immune function. In support of this interpretation, melatonin treatment of turkeys (Meleagris gallopavo) in ovo enhanced both cell-mediated and humoral immune function in juveniles (20). Furthermore, pinealectomy of neonatal rats reduced adult expression of antibody-dependent cellular cytotoxicity (33) and slowed cutaneous wound healing; these effects were reversed by melatonin administration (1).

At an ultimate level of explanation, energetic trade-offs between reproductive development and immune function are likely to underlie the photoperiod-induced differences in immune function in this study. Day length is an important proximate cue that hamsters use to prioritize these physiological processes. SD lengths early in life can delay the onset of puberty until the subsequent breeding season. Hamsters born in SDs become refractory to day length and undergo reproductive development after ~25 wk. This interval is well within the treatment duration used in this study. Taken together, this would suggest that animals held in SDs perinatally delayed reproductive development. Subsequently, this interpretation means that SD-LD animals were stimulated to develop, whereas SD-SD animals remained inhibited by SD lengths throughout the experiment. Animals in LD lengths, on the other hand, underwent rapid reproductive development, as indicated by testes size at weaning. This gonadal growth was then arrested in the LD-SD group by transfer to SDs. These data suggest that the SD-SD hamsters had not experienced any stimulatory effects of day length on their reproductive systems. This delay in sexual maturation may serve as a possible proximate cause of the enhanced immune function in the SD-SD group. Growth and maintenance of tissue is expensive and often incompatible with maximum investment in immune function (18). Furthermore, induction of fever at 20 days of age attenuated pubertal development in Siberian hamsters in LD (26).

One of the major downstream targets of photoperiod (via the effects of melatonin) is the HPG axis. SDs reduce circulating gonadotrophins and arrest both spermatogenesis and steroidogenesis in the testes (22, 32). Although testosterone was elevated in hamsters maintained in LD lengths and is often considered immunosuppressive (17), sex steroid hormones are unlikely to account for group differences in immune function in this study, at least in an activational sense. Previous studies indicate that testosterone did not inhibit DTH responses in SD hamsters (24); indeed, sex steroid administration enhanced antibody production and lymphocyte proliferation in gonadectomized hamsters (5). However, the possibility that photoperiod-induced alterations in androgen exposure may have contributed to the differences in adult immune function cannot be ruled out.

Another possible effector system that is modulated by melatonin is the hypothalamic-pituitary-adrenal (HPA) axis. HPA reactivity alters immune responses (19), and adult Siberian hamsters have elevated basal and stress-induced cortisol concentrations in SDs relative to LDs. Stress immediately before challenge enhances DTH responses in mice (8), and SD lengths augment the enhancement of the DTH responses in hamsters (2). In the present study, basal cortisol concentrations were higher in hamsters housed in SDs as adults, regardless of perinatal photoperiod treatment or sex. Therefore, adult cortisol concentrations cannot directly explain differences in DTH responses between LD-SD and SD-SD groups. However, differences in HPA activity cannot be completely ruled out; cortisol concentrations may have differed during other developmental periods. Also, it is possible that circadian regulation or HPA reactivity to stressors was altered by perinatal photoperiod treatment (30). The regulation of the HPA axis and its effects on immune function in this paradigm deserve future attention.

This study is the first to our knowledge to demonstrate SD enhancements of immune function in female Siberian hamsters. Previous studies reported that DTH responses in restrained female hamsters were higher in SD compared with LD, but no differences between unstressed groups were detected (4). However, SD-SD hamsters significantly enhanced DTH responses in the present study relative to all other groups, providing further evidence that the age of photoperiod treatment is critical to determining immunological outcomes.

Hamsters housed in SDs perinatally and then transferred to LDs at weaning had significantly higher circulating testosterone concentrations compared with hamsters in LDs, both perinatally and postweaning. This occurred without detectable differences in testes mass. This suggests that perinatal exposure to SDs alters the set point for androgen concentrations. This effect is likely mediated via alterations in either hypothalamic gonadotropin-releasing hormone signaling, steroid negative feedback, or the Leydig cells themselves. Future studies will address both the proximate mediators of this phenomenon, as well as the behavioral and physiological sequelae of alterations in androgen exposure. In addition, the possible effects of perinatal exposure to SDs on female estrous cycles and fertility will also be addressed.

Immune responses in the other three photoperiodic groups (not including SD-SD) did not differ statistically from one another. Hamsters in SDs, either perinatally or as adults, exhibited numerically larger responses compared with hamsters in LDs throughout their lives (LD-LD). However, several previous studies have shown enhanced DTH responses in SDs relative to LDs when the animals were born in LDs and only transferred after reaching adulthood (e.g., Refs. 2–4). Hamsters in SDs as adults in this study exhibited DTH responses comparable to those of the SD-SD hamsters in other studies. Although it is possible that variations in experimental procedures are responsible for this discrepancy, it is more likely that the age of animals at which time the photoperiod transfer was made [~55 days previously (2, 24), 21 days in this experiment] affected subsequent immunological responsiveness to day length. These data suggest that exposure to LD through puberty enhances SD-induced augmentation of immune function.

This study demonstrated enhanced immune function in animals kept in SD throughout their lives relative to all other groups. This effect was not complementary of reproductive changes induced by photoperiod, as the perinatal effects on the reproductive system had, for the most part, been resolved by the end of the experiment. Photoperiod early in life regulates both reproductive and immunological responses to day length in adulthood. SD exposure both perinatally and in adulthood was necessary but not sufficient to induce increases in DTH responses. Taken together, these data suggest that early-life photoperiod can have important organizational effects on subsequent immunological responses to day length.


   GRANTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
REFERENCES
 
This work was supported by National Institute of Mental Health Grants MH-57535 and MH-66144 and by National Science Foundation Grant IBN 04–16897. Additional support was received from National Institutes of Health Grant P30NS045758.


   ACKNOWLEDGMENTS
 
We thank Stephanie Bowers and Joanna Workman for technical assistance, Brian Trainor for help with statistical analyses, and Nik Ristev for guidance and support.


   FOOTNOTES
 

Address for reprint requests and other correspondence: Z. M. Weil, Dept. of Psychology, The Ohio State Univ., Columbus, OH 43210 (e-mail: Weil.20{at}osu.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 

  1. Beskonakli E, Palaoglu S, Renda N, Kulacoglu S, Turhan T, and Taskin Y. The effect of pinealectomy on immune parameters in different age groups in rats: results of the weekly alteration of the zinc level and the effect of melatonin administration on wound healing. J Clin Neurosci 7: 320–324, 2000.[CrossRef][ISI][Medline]
  2. Bilbo SD, Dhabhar FS, Viswanathan K, Saul A, Yellon SM, and Nelson RJ. Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function. Proc Natl Acad Sci USA 99: 4067–4072, 2002.[Abstract/Free Full Text]
  3. Bilbo SD and Nelson RJ. Photoperiod influences the effects of exercise and food restriction on an antigen-specific immune response in Siberian hamsters. Endocrinology 145: 556–564, 2004.[Abstract/Free Full Text]
  4. Bilbo SD and Nelson RJ. Sex differences in photoperiodic and stress-induced enhancement of immune function in Siberian hamsters. Brain Behav Immun 17: 462–472, 2003.[CrossRef][ISI][Medline]
  5. Bilbo SD and Nelson RJ. Sex steroid hormones enhance immune function in male and female Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 280: R207–R213, 2001.[Abstract/Free Full Text]
  6. Bronson FH. Mammalian reproduction: an ecological perspective. Biol Reprod 32: 1–26, 1985.[Abstract]
  7. Bronson FH. Mammalian Reproductive Biology. Chicago, IL: University of Chicago Press, 1989.
  8. Dhabhar FS and McEwen BS. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11: 286–306, 1997.[CrossRef][ISI][Medline]
  9. Dhabhar FS and McEwen BS. Enhancing versus suppressive effects of stress hormones on skin immune function. Proc Natl Acad Sci USA 96: 1059–1064, 1999.[Abstract/Free Full Text]
  10. Duncan MJ and Goldman BD. Physiological doses of prolactin stimulate pelage pigmentation in Djungarian hamster. Am J Physiol Regul Integr Comp Physiol 248: R664–R667, 1985.[Abstract/Free Full Text]
  11. Goldman BD. Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 16: 283–301, 2001.[Abstract]
  12. Gorman MR. A plastic interval timer synchronizes pubertal development of summer- and fall-born hamsters. Am J Physiol Regul Integr Comp Physiol 281: R1613–R1623, 2001.[Abstract/Free Full Text]
  13. Grady KL, Phoenix CH, and Young WC. Role of the developing rat testis in differentiation of the neural tissues mediating mating behavior. J Comp Physiol Psychol 59: 176–182, 1965.[CrossRef][ISI][Medline]
  14. Horton TH. Cross-fostering of voles demonstrates in utero effect of photoperiod. Biol Reprod 33: 934–939, 1985.[Abstract]
  15. Horton TH. Growth and reproductive development of male Microtus montanus is affected by the prenatal photoperiod. Biol Reprod 31: 499–504, 1984.[Abstract]
  16. Horton TH, Stachecki SA, and Stetson MH. Maternal transfer of photoperiodic information in Siberian hamsters. IV. Peripubertal reproductive development in the absence of maternal photoperiodic signals during gestation. Biol Reprod 42: 441–449, 1990.[Abstract]
  17. Klein SL. The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev 24: 627–638, 2000.[CrossRef][ISI][Medline]
  18. Martin LB. Trade-offs between molt and immune activity in two populations of house sparrows (Passer domesticus). Can J Zool 83: 780–787, 2005.
  19. McEwen BS, Biron CA, Brunson KW, Bulloch K, Chambers WH, Dhabhar FS, Goldfarb RH, Kitson RP, Miller AH, Spencer RL, and Weiss JM. The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res Brain Res Rev 23: 79–133, 1997.[CrossRef][Medline]
  20. Moore CB and Siopes TD. Effect of melatonin supplementation on the ontogeny of immunity in the Large White turkey poult. Poult Sci 81: 1898–1903, 2002.[Abstract/Free Full Text]
  21. Nelson RJ and Demas GE. Seasonal changes in immune function. Q Rev Biol 71: 511–548, 1996.[CrossRef][Medline]
  22. Niklowitz P, Khan S, Bergmann M, Hoffmann K, and Nieschlag E. Differential effects of follicle-stimulating hormone and luteinizing hormone on Leydig cell function and restoration of spermatogenesis in hypophysectomized and photoinhibited Djungarian hamsters (Phodopus sungorus). Biol Reprod 41: 871–880, 1989.[Abstract]
  23. Prendergast BJ, Bilbo SD, Dhabhar FS, and Nelson RJ. Effects of photoperiod history on immune responses to intermediate day lengths in Siberian hamsters (Phodopus sungorus). J Neuroimmunol 149: 31–39, 2004.[CrossRef][ISI][Medline]
  24. Prendergast BJ, Bilbo SD, and Nelson RJ. Short day lengths enhance skin immune responses in gonadectomised Siberian hamsters. J Neuroendocrinol 17: 18–21, 2005.[CrossRef][ISI][Medline]
  25. Prendergast BJ, Gorman MR, and Zucker I. Establishment and persistence of photoperiodic memory in hamsters. Proc Natl Acad Sci USA 97: 5586–5591, 2000.[Abstract/Free Full Text]
  26. Prendergast BJ, Hotchkiss AK, Bilbo SD, and Nelson RJ. Peripubertal immune challenges attenuate reproductive development in male Siberian hamsters (Phodopus sungorus). Biol Reprod 70: 813–820, 2004.[Abstract/Free Full Text]
  27. Prendergast BJ, Hotchkiss AK, and Nelson RJ. Photoperiodic regulation of circulating leukocytes in juvenile Siberian hamsters: mediation by melatonin and testosterone. J Biol Rhythms 18: 473–480, 2003.[Abstract]
  28. Pyter LM and Nelson RJ. Enduring effects of photoperiod on affective behaviors in Siberian hamsters (Phodopus sungorus). Behav Neurosci 120: 125–134, 2006.[CrossRef][ISI][Medline]
  29. Reburn CJ and Wynne-Edwards KE. Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav 35: 163–176, 1999.[CrossRef][Medline]
  30. Ronchi E, Spencer RL, Krey LC, and McEwen BS. Effects of photoperiod on brain corticosteroid receptors and the stress response in the golden hamster (Mesocricetus auratus). Brain Res 780: 348–351, 1998.[CrossRef][ISI][Medline]
  31. Shaw D and Goldman BD. Influence of prenatal and postnatal photoperiods on postnatal testis development in the Siberian hamster (Phodopus sungorus). Biol Reprod 52: 833–838, 1995.[Abstract]
  32. Turek FW, Elliott JA, Alvis JD, and Menaker M. The interaction of castration and photoperiod in the regulation of hypophyseal and serum gonadotropin levels in male golden hamsters. Endocrinology 96: 854–860, 1975.[Abstract]
  33. Vermeulen M, Palermo M, and Giordano M. Neonatal pinealectomy impairs murine antibody-dependent cellular cytotoxicity. J Neuroimmunol 43: 97–101, 1993.[CrossRef][ISI][Medline]
  34. Weaver DR, Keohan JT, and Reppert SM. Definition of a prenatal sensitive period for maternal-fetal communication of day length. Am J Physiol Endocrinol Metab 253: E701–E704, 1987.[Abstract/Free Full Text]
  35. Yellon SM and Goldman BD. Photoperiod control of reproductive development in the male Djungarian hamster (Phodopus sungorus). Endocrinology 114: 664–670, 1984.[Abstract]
  36. Yellon SM, Tamarkin L, and Goldman BD. Maturation of the pineal melatonin rhythm in long- and short-day reared Djungarian hamsters. Experientia 41: 651–652, 1985.[CrossRef][ISI][Medline]



This article has been cited by other articles:


Home page
 J Biol RhythmsHome page
A. J. Gall, W. D. Todd, B. Ray, C. M. Coleman, and M. S. Blumberg
The Development of Day-Night Differences in Sleep and Wakefulness in Norway Rats and the Effect of Bilateral Enucleation
J Biol Rhythms, June 1, 2008; 23(3): 232 - 241.
[Abstract] [PDF]

Home page
 Integr. Comp. Biol.Home page
L. B. Martin II, Z. M. Weil, and R. J. Nelson
Refining approaches and diversifying directions in ecoimmunology
Integr. Comp. Biol., December 1, 2006; 46(6): 1030 - 1039.
[Abstract] [Full Text] [PDF]

Home page
 J Biol RhythmsHome page
Z. M. Weil, L. B. Martin II, and R. J. Nelson
Photoperiod Differentially Affects Immune Function and Reproduction in Collared Lemmings (Dicrostonyx groenlandicus).
J Biol Rhythms, October 1, 2006; 21(5): 384 - 393.
[Abstract] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
290/6/R1714    most recent
00869.2005v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (10)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Weil, Z. M.
Right arrow Articles by Nelson, R. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Weil, Z. M.
Right arrow Articles by Nelson, R. J.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online
Copyright © 2006 by the American Physiological Society.