Short Day Lengths Enhance Skin Immune Responses in Gonadectomised Siberian Hamsters

Prendergast, Brian J.; Bilbo, Staci D.; Nelson, Randy J.

doi:10.1111/j.1365-2826.2005.01273.x

Cited by 28 publications

(26 citation statements)

References 43 publications

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“…Increases in the number of cells expressing CD62 cell-surface markers-adhesion molecules that participate in the migration of lymphocytes through endothelium-could contribute to enhanced skin inflammatory responses in SD (7,12). Thus, earlier reports, suggesting gonadal hormone independence of skin inflammatory responses (39), are consistent with the persistence of photoperiodic differences in CD62ϩ cells following gonadectomy in the present study. Studies in other reproductively photoperiodic rodents have likewise indicated several gonadal hormone-independent effects of photoperiod on the immune system (16).…”

Section: Discussionsupporting

confidence: 81%

“…Data bearing on this issue have not yielded consistent results. In hamsters, photoperiodic changes in antibody production and skin inflammatory responses occur independent of changes in the reproductive system (18,39); in contrast, other indices of immunity more closely track gonadal condition (spontaneous blastogenesis, leukocyte concentrations) (41,45). Determining the extent to which seasonal changes in the immune system depend on concurrent changes in the reproductive system remains a key step toward understanding how photoperiod drives seasonal immunity, and more generally, may provide insight into how neuroendocrine activity impinges on the immune system.…”

mentioning

confidence: 99%

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Gonadal hormone-dependent and -independent regulation of immune function by photoperiod in Siberian hamsters

Prendergast¹,

Baillie²,

Dhabhar³

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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Siberian hamsters (Phodopus sungorus) exhibit changes in reproductive and immune function in response to seasonal variations in day length. Exposure to short days induces gonadal regression and inhibits testosterone secretion. In parallel, short days enhance immune function: increasing leukocyte numbers and attenuating cytokine and behavioral responses to infection. We examined whether photoperiodic changes in leukocyte phenotypes and sickness behaviors are dependent on concurrent photoperiodic changes in gonadal function. Male hamsters were gonadectomized or sham-gonadectomized and either exposed to short days (9 h light/day; SD) or kept in their natal long-day (15 h light/day; LD) photoperiod for 10 -13 wk. Blood samples were obtained for leukocyte enumeration, and hamsters were challenged with bacterial LPS, which induced behavioral (anorexia, reductions in nest building) and somatic (weight loss) sickness responses. Among gonad-intact hamsters, exposure to SD increased total and CD62Lϩ lymphocytes and CD3ϩ T lymphocytes in blood and significantly attenuated LPSinduced sickness responses. Independent of photoperiod, castration alone increased total and CD62Lϩ lymphocyte and CD3ϩ T lymphocyte numbers and attenuated somatic and anorexic sickness responses. Among castrated hamsters, SD exposure increased lymphocyte numbers and suppressed sickness behaviors. In castrated hamsters, the magnitude of most immunological effects of SD were diminished relative to those evident in gonad-intact hamsters. The SD phenotype in several measures of immunity can be instated via elimination of gonadal hormones alone; however, photoperiodic effects on immune function persist even in castrated hamsters. Thus, photoperiod affects the immune system and neural-immune interactions underlying sickness behaviors via gonadal hormone-dependent and -independent mechanisms. seasonality; sickness behaviors; infection; neural-immune interactions SEASONAL CHANGES IN PHYSIOLOGY and behavior are legion, most notably in reproductive function (8). Many mammals have evolved mechanisms that permit cessation of reproduction during intervals of the year when environmental conditions of food availability and ambient temperature are unfavorable for successful weaning of offspring (44,47). In nonequatorial regions, changes in day length (photoperiod) predict these environmental constraints (46) and function as proximate cues for triggering anticipatory changes in reproductive physiology and behavior. In long-day breeders, decreasing photoperiods of late-summer trigger gonadal atrophy, withdrawal of gonadal hormone secretion, and cessation of sex behaviors (8). The full complement of changes in the reproductive system can be elicited in the laboratory by exposing reproductively photoperiodic animals to winter-like day lengths (Ͻ12 h of light/day) (22).Seasonal changes in immune function also occur in wild and laboratory animals (34), and a growing body of research indicates photoperiod likewise drives these cycles. Among long-day breeding rodents, many a...

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Section: Discussionsupporting

confidence: 81%

mentioning

confidence: 99%

Gonadal hormone-dependent and -independent regulation of immune function by photoperiod in Siberian hamsters

Prendergast¹,

Baillie²,

Dhabhar³

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Indeed, gonadal androgens influence immune function-often in an immunosuppressive fashion (Klein, 2000;Obendorf and Patchev, 2004;Mueh-lenbein and Bribiescas, 2005). However, in Siberian hamsters, several experiments have indicated that photoperiodic changes in immune function can occur independent of changes in reproductive system (blastogenesis: Prendergast et al, 2002b;leukocyte counts: Prendergast et al, 2004a; skin inflammatory responses: Prendergast et al, 2005). Studies in other reproductively photoperiodic species have indicated similar gonadal hormone-independent effects of photoperiod on the immune system (Demas and Nelson, 1998).…”

Section: Discussionmentioning

confidence: 99%

Pineal-dependent and -independent effects of photoperiod on immune function in Siberian hamsters (Phodopus sungorus)

Wen

Dhabhar

Prendergast

2007

Hormones and Behavior

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Siberian hamsters (Phodopus sungorus) exhibit reproductive and immunological responses to photoperiod. Short (<10-h light/day) days induce gonadal atrophy, increase leukocyte concentrations, and attenuate thermoregulatory and behavioral responses to infection. Whereas hamster reproductive responses to photoperiod are dependent on pineal melatonin secretion, the role of the pineal in short-day induced changes in immune function is not fully understood. To examine this, adult hamsters were pinealectomized (PINx) or sham-PINx, and transferred to short days (9-h light/day; SD) or kept in their natal long-day (15-h light/day; LD) photoperiod. Intact and PINx hamsters housed in LD maintained large testes over the next 12 weeks; sham-PINx hamsters exhibited gonadal regression in SD, and PINx abolished this effect. Among pineal-intact hamsters, blood samples revealed increases in leukocyte, lymphocyte, CD62L+ lymphocyte, and T cell counts in SD relative to LD; PINx did not affect leukocyte numbers in LD hamsters, but abolished the SD increase in these measures. Hamsters were then treated with bacterial lipopolysaccharide (LPS), which induced thermoregulatory (fever), behavioral (anorexia, reductions in nest building), and somatic (weight loss) sickness responses in all groups. Among pineal-intact hamsters, febrile and behavioral responses to LPS were attenuated in SD relative to LD. PINx did not affect sickness responses to LPS in LD hamsters, but abolished the ameliorating effects of SD on behavioral responses to LPS. Surprisingly, PINx failed to abolish the effect of SD on fever. In common with the reproductive system, PINx induces the LD phenotype in most aspects of the immune system. The pineal gland is required for photoperiodic regulation of circulating leukocytes and neural-immune interactions that mediate select aspects of sickness behaviors.

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“…Further, because oestrogens tend to enhance immune activity, if photoperiodic changes in immune function are mainly due to fluctuations in sex steroid hormones, then females in short days that have low oestrogen concentrations should show reduced immune function when compared with long-day animals (or at least not exhibit male-like increases). Because these predictions were not substantiated in male and female deer mice ) and gonadectomy and exogenous testosterone administration did not alter short-day enhancement of the DTH response in Siberian hamsters (Prendergast et al 2005), this hypothesis has fallen out of favour.…”

Section: Proximate Mechanisms Mediating Trade-offsmentioning

confidence: 96%

Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs

Martin

Weil

Nelson

2007

Phil. Trans. R. Soc. B

470

496

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Animals living in temporally dynamic environments experience variation in resource availability, climate and threat of infection over the course of the year. Thus, to survive and reproduce successfully, these organisms must allocate resources among competing physiological systems in such a way as to maximize fitness in changing environments. Here, we review evidence supporting the hypothesis that physiological trade-offs, particularly those between the reproductive and immune systems, mediate part of the seasonal changes detected in the immune defences of many vertebrates. Abundant recent work has detected significant energetic and nutritional costs of immune defence. Sometimes these physiological costs are sufficiently large to affect fitness (e.g. reproductive output, growth or survival), indicating that selection for appropriate allocation strategies probably occurred in the past. Because hormones often orchestrate allocations among physiological systems, the endocrine mediators of seasonal changes in immune activity are discussed. Many hormones, including melatonin, glucocorticoids and androgens have extensive and consistent effects on the immune system, and they change in systematic fashions over the year. Finally, a modified framework within which to conduct future studies in ecological immunology is proposed, viz. a heightened appreciation of the complex but intelligible nature of the vertebrate immune system. Although other factors besides tradeoffs undoubtedly influence seasonal variation in immune defence in animals, a growing literature supports a role for physiological trade-offs and the fitness consequences they sometimes produce.

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Short Day Lengths Enhance Skin Immune Responses in Gonadectomised Siberian Hamsters

Cited by 28 publications

References 43 publications

Gonadal hormone-dependent and -independent regulation of immune function by photoperiod in Siberian hamsters

Gonadal hormone-dependent and -independent regulation of immune function by photoperiod in Siberian hamsters

Pineal-dependent and -independent effects of photoperiod on immune function in Siberian hamsters (Phodopus sungorus)

Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs

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