Time course and role of the pineal gland in photoperiod control of innate immune cell functions in male Siberian hamsters

Yellon, Steven M.; Kim, Kiam; Hadley, Allison R; Tran, Long T.

doi:10.1016/j.jneuroim.2004.12.008

Cited by 16 publications

(10 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In one previous experiment, pharmacological injections of melatonin delivered daily 4 h before the onset of darkness (so as to lengthen the endogenous melatonin profile) mimicked the effects of short-days on febrile responses to a simulated infection, suggesting that the duration of melatonin is sufficient in this regard (Bilbo and Nelson, 2002); a similar paradigm yielded comparable results on circulating leukocyte concentrations (Prendergast et al, 2003b). Pineal dependence of innate immunity has been inferred from a study which maintained hamsters in constant light, suppressing endogenous melatonin secretion (Yellon et al, 2005); pineal dependence of adaptive immunity has been inferred from an experiment which exposed pinealectomized hamsters to short days for 1 week prior to antigenic challenge (Yellon et al, 1999b). The interpretation of these studies is not straightforward, given that: (1) daily melatonin injections also render the circadian system in a SD-typical state (Puchalski and Lynch, 1988;Margraf and Lynch, 1993), (2) little is known regarding the significance of the amplitude of melatonin signals on immune function, and (3) constant light renders circadian rhythms in a free-running state, functions as a stressor, and can be immunosuppressive (Morimoto et al, 1975;Ramaley, 1977;Larsen et al, 1994;Liebmann et al, 1996).…”

Section: Introductionmentioning

confidence: 93%

“…In Siberian hamsters, short days enhance natural killer cell cytolytic capacity and spontaneous blastogenesis in both whole blood lymphocytes and isolated lymphocytes (Yellon et al, 1999a). Circulating lymphocyte concentrations (e.g., T cells, B cells) are greater in short days relative to long days (Bilbo et al, 2002a;Prendergast et al, 2004a;Yellon et al, 2005). In addition, more integrative measures of immune function such as T-cell-dependent skin inflammatory responses, which depend in part on specific leukocyte subtypes (i.e., CD44+ and CD62+ leukocytes), are greater in short days relative to long days (Dhabhar et al, 2000;Bilbo et al, 2002a;Prendergast et al, 2004a).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Wen

Dhabhar

Prendergast

2007

Hormones and Behavior

View full text Add to dashboard Cite

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.

show abstract

Section: Introductionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

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

Wen

Dhabhar

Prendergast

2007

Hormones and Behavior

View full text Add to dashboard Cite

show abstract

“…In common with reproductive responses, photoperiodic changes in immunity are dependent on pineal melatonin secretion (49). Temporally, photoperiodic changes in immune function appear to parallel changes in reproductive function (41,44,56). In light of the immunomodulatory role of gonadal hormones (5,29,40), photoperiodic changes in the immune system may arise exclusively as a consequence of photoperiod-driven changes in the reproductive system.…”

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

View full text Add to dashboard Cite

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...

show abstract

“…Short photoperiods (<13 h light/day) initiate gonadal regression and induce changes in numerous aspects of immune function, including increases in T and B lymphocytes (Bilbo et al, 2002a;Yellon et al, 2005), enhanced lymphocyte function (Yellon et al, 1999), and attenuated antibody responses (Demas and Sakaria, 2005). Species differences in immune responses to photoperiod exist, but a general trend toward improved immune function under short days is evident among long-day-breeding rodents (Nelson, 2004).…”

mentioning

confidence: 99%

Photoperiodic Regulation of Behavioral Responses to Bacterial and Viral Mimetics: A Test of the Winter Immunoenhancement Hypothesis

Baillie

Prendergast

2008

J Biol Rhythms

View full text Add to dashboard Cite

Siberian hamsters (Phodopus sungorus) exhibit changes in immune function following adaptation to short photoperiods, including a marked attenuation of energetically expensive thermoregulatory and behavioral responses to gram-negative bacterial infections. Whether this seasonal attenuation of the immune response is idiosyncratic to gram-negative infections or is representative of innate immune responses in general is not known. If seasonal attenuation of responsiveness to infection is indeed driven primarily by anticipation of energetic constraints, then one would predict that responsiveness to all pathogens would be diminished during short days. If, on the other hand, seasonal changes in responsiveness to infection reflect anticipation of specific pathogens that are common at different phases of the annual cycle, then one would expect short photoperiods to attenuate responsiveness to some pathogens and long photoperiods to attenuate responsiveness to others. To resolve this issue, we exposed male Siberian hamsters to either long or short photoperiods for 11 weeks, then examined their behavioral sickness responses to compounds that represent the minimally immunogenic components of gram-negative bacterial (lipopolysaccharide), gram-positive bacterial (muramyl dipeptide), and viral (polyinosinepolycytidylic acid) organisms. Hamsters exhibited anorexic, anhedonic, ponderal, and/or thermoregulatory sickness behaviors to all 3 pathogen mimetics, but in all cases in which sickness responses were evident, they were attenuated in short days. Energetically costly behavioral responses to several distinct classes of infectious organisms are attenuated in anticipation of winter. The data are not consistent with a pathogen-specific seasonal modulation of innate immune responses.

show abstract

Time course and role of the pineal gland in photoperiod control of innate immune cell functions in male Siberian hamsters

Cited by 16 publications

References 41 publications

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

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

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

Photoperiodic Regulation of Behavioral Responses to Bacterial and Viral Mimetics: A Test of the Winter Immunoenhancement Hypothesis

Contact Info

Product

Resources

About