Skip to main content

Advertisement

Log in

Metabolic stress suppresses humoral immune function in long-day, but not short-day, Siberian hamsters (Phodopus sungorus)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Individuals of many species experience marked seasonal variation in environmental conditions and must adapt to potentially large fluctuations in energy availability and expenditure. Seasonal changes in immunity have likely evolved as an adaptive mechanism to cope with seasonal stressors. In addition, these changes may be constrained by seasonal fluctuations in energy availability. The goal of this study was to assess the role of energetic trade-offs associated with seasonal variation in immunity. In addition to body fat stores, metabolic fuels (e.g., glucose) may affect immune function in seasonally breeding rodents. In this study we experimentally reduced energy availability via injections of the metabolic inhibitor 2-deoxy-d-glucose (2-DG) in long- and short-day housed Siberian hamsters (Phodopus sungorus) and then examined antigen-specific antibody production. Metabolic stress decreased antibody response compared with control animals in long days. In contrast, no difference was observed between treatment groups in short days. These data suggest that reductions in energy availability suppress immunity and short days buffer organisms against glucoprivation-induced immunosuppression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

2-DG:

2-Deoxy-d-glucose

IgM:

Immunoglobulin M

IgG:

Immunoglobulin G

KLH:

Keyhole limpet hemocyanin

PWAT:

Parametrial white adipose tissue

IWAT:

Inguinal white adipose tissue

RWAT:

Retroperitoneal white adipose tissue

ELISA:

Enzyme-linked immunosorbent assay

EIA:

Enzyme immunoassay

PBS-T:

Phosphate buffered saline with Tween-20

OD:

Optical density

ANOVA:

Analysis of variance

PVN:

Paraventricular nucleus

AVP:

Arginine vasopressin

CRH:

Corticotropin-releasing hormone

References

  • Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious disease. Ecol Lett 9:467–484

    Article  PubMed  Google Scholar 

  • Bartness TJ, Goldman BD (1989) Mammalian pineal melatonin: a clock for all seasons. Experientia 45:939–945

    Article  PubMed  CAS  Google Scholar 

  • Bartness TJ, Wade GN (1985) Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev 9:599–612

    Article  PubMed  CAS  Google Scholar 

  • Bartness TJ, Powers JB, Hastings MH, Bittman EL, Goldman BD (1993) The timed infusion paradigm for melatonin delivery: what it has taught us about the melatonin signal, its reception, the photoperiodic control of seasonal responses. J Pineal Res 15:161–190

    Article  PubMed  CAS  Google Scholar 

  • Bilbo SD, Nelson RJ (2003) Sex differences in photoperiodic and stress-induced enhancement of immune function in Siberian hamsters. Brain Behav Immun 17:462–472

    Article  PubMed  CAS  Google Scholar 

  • Bilbo SD, Drazen DL, Quan N, He L, Nelson RJ (2002) Short day lengths attenuate the symptoms of infection in Siberian hamsters. Proc R Soc Lond B Biol Sci 269:447–454

    Article  Google Scholar 

  • Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago

    Google Scholar 

  • Bronson FH, Heideman PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The physiology of reproduction, 2nd edn. Raven, New York, pp 541–584

    Google Scholar 

  • Caroleo MC, Frasca D, Nistico G, Doria G (1992) Melatonin as an immunomodulator in immunodeficient mice. Immunopharmacology 23:81–89

    Article  PubMed  CAS  Google Scholar 

  • Cassone VM (1990) Melatonin: time in a bottle. Oxf Rev Reprod Biol 12:319–367

    PubMed  CAS  Google Scholar 

  • Dark J, Zucker I (1983) Short photoperiods reduce winter energy requirements of the Meadow vole (Microtus pennsylvanicus). Physiol Behav 31:699–702

    PubMed  CAS  Google Scholar 

  • Dark J, Miller DR, Zucker I (1994) Reduced glucose availability induces torpor in Siberian hamster. Am J Physiol 267:R496–R501

    PubMed  CAS  Google Scholar 

  • Demas GE (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45:173–180

    Article  PubMed  CAS  Google Scholar 

  • Demas GE, Nelson RJ (1996) The effects of photoperiod and temperature on immune function of adult male deer mice (Peromyscus maniculatus). J Biol Rhythms 11:94–102

    Article  PubMed  CAS  Google Scholar 

  • Demas GE, Nelson RJ (1998) Exogenous melatonin enhances cell-mediated, but not humoral, immune function in deer mice (Perimyscus maiculatus). J Comp Physiol A 179:819–825

    Google Scholar 

  • Demas GE, DeVries AC, Nelson RJ (1997) Effects of photoperiod and 2-deoxy-d-glucose-induced metabolic stress on immune function in female deer mice. Am J Physiol 272:610–616

    Google Scholar 

  • Demas GE, Drazen DL, Jasnow AM, Bartness TJ, Nelson RJ (2002) Sympathoadrenal system differentially affects photoperiodic changes in humoral immunity of Siberian hamsters (Phodopus sungorus). J Neuroendocrinol 14:29–35

    Article  PubMed  CAS  Google Scholar 

  • Demas GE, Drazen DL, Nelson RJ (2003a) Reductions in total body fat decrease humoral immunity. Proc R Soc Lond B Biol Sci 270:905–911

    Article  Google Scholar 

  • Demas GE, Bartness TJ, Nelson RJ, Drazen DL (2003b) Photoperiod modulates the effects of norepinephrine on lymphocyte proliferation in Siberian hamsters. Am J Physiol 285:R873–R879

    CAS  Google Scholar 

  • Demas GE, Johnson C, Polacek KM (2004) Social interactions differentially affect reproductive and immune responses of Siberian hamsters. Physiol Behav 83:73–79

    Article  PubMed  CAS  Google Scholar 

  • Dhabhar FS (2000) Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann N Y Acad Sci 917:876–893

    Article  PubMed  CAS  Google Scholar 

  • Dixon F, Jacot-Guillarmod H, McConahey PJ (1966) The antibody responses of rabbits and rats to hemocyanin. J Immunol 97:350–355

    PubMed  CAS  Google Scholar 

  • Dowell SF, Whitney CG, Rose CE, Schuchat A (2003) Seasonal patterns of invasive pneumococcal disease. Emerg Infect Dis 9:573–579

    PubMed  Google Scholar 

  • Drazen DL, Nelson RJ, Bartness TJ, Demas GE (2000) Sympathoadrenal regulation of photoperiodic changes in immune function in Siberian hamsters. Society for Neuroscience, New Orleans

    Google Scholar 

  • Drazen DL, Demas GE, Nelson RJ (2001) Leptin effects on immune function and energy balance are photoperiod-dependent in Siberian hamsters (Phodopus sungorus). Endocrinology 142:2768–2775

    Article  PubMed  CAS  Google Scholar 

  • Evans SB, Wilkinson CW, Bentson K, Gronbeck P, Zavosh A, Figlewicz DP (2001) PVN activation is suppressed by repeated hypoglycemia but not antecedent corticosterone in the rat. Am J Physiol Regul Integr Comp Physiol 281:R1426–R1436

    PubMed  CAS  Google Scholar 

  • Goldman BD, Elliot RJ (1988) Photoperiodism and seasonality in hamsters: role of the pineal gland. In: Stetson MH (ed) Processing of environmental information in vertebrates. Springer, Berlin Heidelberg New York, pp 203–218

    Google Scholar 

  • Goldman BD, Nelson RJ (1993) Melatonin and seasonality in mammals. In: Yu HS, Reiter RJ (eds) Melatonin: biosynthesis, physiological effects and clinical applications. CRC, New York

    Google Scholar 

  • Gorman MR, Zucker I (1997) Environmental induction of photoresponsiveness in the Siberian hamster (Photopus sungorus). Am J Physiol Reg I 41:R887–R895

    Google Scholar 

  • Heldmaier G, Steinlechner S, Ruf T, Wiesinger H, Klingenspor K (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythms 4:351–365

    Article  Google Scholar 

  • Henken AM, Brandsma HA (1982) The effects of environmental temperature on immune response and metabolism of the young chicken. Poult Sci 61:1667–1677

    PubMed  CAS  Google Scholar 

  • Hoffman K, Illnerova H, Vanecek J (1985) Comparison of pineal melatonin rhythms in young adult and old Djungarian hamsters (Phodopus sungorus) under long and short photoperiods. Neurosci Lett 56:39–43

    Article  Google Scholar 

  • Horton RW, Meldrum BS, Bachelard HS (1973) Enzymic and cerebral metabolic effects of 2-deoxy-d-glucose. J Neurochem 21:507–520

    Article  PubMed  CAS  Google Scholar 

  • Hosseini PR, Dhondt AA, Dobson A (2004) Seasonal and wildlife disease: how seasonal birth, aggregation, and variation in immunity effect the dynamics of Mycoplasma gallisepticum in house finches. Proc R Soc Lond B Biol Sci 271:2569–2577

    Article  Google Scholar 

  • Iverson SL, Turner BN (1974) Winter weight dynamics in Microtus pennsylvanicus. Ecology 55:1030–1040

    Article  Google Scholar 

  • John JL (1994) The avian spleen: a neglected organ. Q Rev Biol 69:327–351

    Article  PubMed  CAS  Google Scholar 

  • Kinsey SG, Prendergast BJ, Nelson RJ (2003) Photoperiod and stress affect wound healing in Siberian hamsters. Physiol Behav 78:205–211

    Article  PubMed  CAS  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Lochmiller RL, Vesty MR, McMurray ST (1994) Temporal variation in humoral and cell-mediated immune response in Sigmodon hispidus population. Ecology 75:236–245

    Article  Google Scholar 

  • Lynch GR, Lynch CB, Kliman RM (1989) Genetic analysis of photoresponsiveness in the Djungarian hamster, Phodopus sungorus. J Comp Physiol A 164:475–481

    Article  PubMed  CAS  Google Scholar 

  • Lysle DT, Cunnick JE, Wu R, Caggiula AR, Wood PG, Rabin BS (1988) 2-Deoxy-d-glucose modulation of T-lymphocyte reactivity: differential effects on lymphoid compartments. Brain Behav Immun 2:212–221

    Article  PubMed  CAS  Google Scholar 

  • Maestroni GJ (1993) The immunoendocrine role of melatonin. J Pineal Res 14:1–10

    Article  PubMed  CAS  Google Scholar 

  • Margraff RR, Zlomanczuk P, Liskin LA, Lynch GR (1991) Circadian differences in neuronal activity of the suprachiasmatic nucleus in brain slices prepared from photo-responsive and photo-non-responsive Djungarian hamsters. Brain Res 544:42–48

    Article  Google Scholar 

  • Mann DR, Akinbami MA, Gould KG, Ansari AA (2000) Seasonal variations in cytokine expression and cell-mediated immunity in male rhesus monkeys. Cell Immunol 200:105–115

    Article  PubMed  CAS  Google Scholar 

  • Moffatt CA, DeVries AC, Nelson RJ (1993) Winter adaptations of male deer mice and prairie voles that vary in reproductive responsiveness to photoperiod. J Biol Rhythms 8:221–232

    Article  PubMed  CAS  Google Scholar 

  • Motawei K, Pyner S, Ranson RN, Kamel M, Coote JH (1999) Terminals of paraventricular spinal neurons are closely associated with adrenal medullary sympathetic preganglion neurons: immunocytochemical evidence for vasopressin as a possible neurotransmitter in this pathway. Exp Brain Res 126:68–76

    Article  PubMed  CAS  Google Scholar 

  • Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–48

    Article  PubMed  CAS  Google Scholar 

  • Nelson RJ, Badura LL, Goldman BD (1990) Mechanisms of seasonal cycles of behavior. Ann Rev Psychol 41:81–109

    Article  CAS  Google Scholar 

  • Prendergast BJ, Kreigsfeld LJ, Nelson RJ (2001) Photoperiodic polyphenisms in rodents: neuroendocrine mechanisms, costs, and functions. Q Rev Biol 76:293–325

    Article  PubMed  CAS  Google Scholar 

  • Prendergast BJ, Wynne-Edwards KE, Yellon SM, Nelson RJ (2002) Photorefractoriness of immune function in male Siberian hamsters (Phodopus sungorus). J Neuroendocrinol 14:318–329

    Article  PubMed  CAS  Google Scholar 

  • Puchalski W, Lynch RG (1986) Evidence for differences in the circadian organization of hamsters exposed to short day photoperiod. J Comp Physiol A 159:7–11

    Article  PubMed  CAS  Google Scholar 

  • Puchalski W, Lynch RG (1988) Daily melatonin injections affect the expression of circadian rhythmicity in Djungarian hamsters kept under a long-day photoperiod. Neuroendocrinology 48:280–286

    PubMed  CAS  Google Scholar 

  • Reburn CJ, Wynne-Edwards KE (1999) Cortisol and prolactin concentrations during repeated blood sample collection from freely moving, mouse-sized animals (Phodopus spp.). Comp Med 50:184–198

    Google Scholar 

  • Ribelayga C, Pevet P, Simonneaux V (2000) HIOMT drives photoperiodic changes in the amplitude of the melatonin peak of the Siberian hamster. Am J Physiol Reg I 278:R1339–R1345

    CAS  Google Scholar 

  • Ruby NF, Zucker I (1992) Daily torpor in the absence of the superchiasmatic nucleus in the Siberian hamster. Am J Physiol A 263:R353–R362

    CAS  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary psychology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Weindenfeld J, Corcos AP, Wohlman A, Feldman S (1994) Characterization of the 2-deoxyglucose effect on the adrenocortical axis. Endocrinology 134:1924–1931

    Article  Google Scholar 

  • Yates FE, Russell SM, Dallman MF, Hodge GA, McCann SM, Dhariwal AP (1971) Potentiation by vasopressin of corticotropin release induced by corticotropin-releasing factor. Endocrinology 88:3–15

    Article  PubMed  CAS  Google Scholar 

  • Yellon SM, Teasly LA, Fagoagal OR, Nguyen HC, Truong HN, Cannerella L (1999) Role of photoperiod and the pineal gland in T-cell dependent humoral immune reactivity in the Siberian hamster. J Pineal Res 29:86–93

    Google Scholar 

Download references

Acknowledgments

We thank Melissa-Ann L. Scotti, Timothy J. Greives, Andrew Garst, and Emily Chester for their assistance and two anonymous reviewers for helpful suggestions on this manuscript. This work was supported in part by NIH T32 Training Grant HD049336, a Faculty Research Support Program Grant, and the Center for the Integrative Study of Animal Behavior (CISAB). All procedures were approved by the Bloomington Institutional Animal Care and Use Committee.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Devin A. Zysling.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zysling, D.A., Demas, G.E. Metabolic stress suppresses humoral immune function in long-day, but not short-day, Siberian hamsters (Phodopus sungorus). J Comp Physiol B 177, 339–347 (2007). https://doi.org/10.1007/s00360-006-0133-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-006-0133-4

Keywords

Navigation