Seasonal immune function and sickness responses

doi:10.1016/j.it.2004.02.001

Trends in Immunology

Volume 25, Issue 4, April 2004, Pages 187-192

https://doi.org/10.1016/j.it.2004.02.001 Get rights and content

Abstract

Winter is a particularly difficult time to breed and survive. Animals monitor day length (photoperiod) to engage seasonally appropriate adaptations in anticipation of harsh winter conditions. I propose that photoperiodic information, mediated by melatonin, might also influence immune responses. Individuals could improve survival if seasonally recurring stressors were anticipated and countered. Recent studies suggest that short day lengths reroute energy from reproduction and growth to bolster immune function during winter. Short days can either enhance or suppress components of immune function, as well as reduce fever and the expression of sickness behaviors. The net result of these photoperiod-mediated adjustments is enhanced immune function and increased survival. Melatonin appears to be part of an integrated system that coordinates reproductive, immunological and other processes to cope successfully with energetic stressors during winter and to balance trade-offs between reproductive success and survival.

Section snippets

Energy and seasonal immune function

Species-specific strategies for optimal partitioning of resources among growth, reproduction and survival mechanisms are called life-history strategies [6]. Because long-lived individuals generally produce more offspring than short-lived conspecifics, whereas breeding often compromises health and survival, natural selection operates on the mechanisms mediating both survival and reproductive success to maximize Darwinian fitness. Adaptive functional studies generally consider immune function as

Photoperiod effects on the immune system

Exposure to short day lengths affects several parameters of the immune system. Short days correlate closely with the seasonal peak in invasive pneumococcal disease among humans [34]. Earlier reports indicated that spleen mass is elevated in deer mice and Syrian hamsters kept in a short photoperiod 35, 36. Photoperiod affects the immune system of several rodent species (Table 2). Short days increase the number of circulating blood leukocytes, lymphocytes, T cells and NK cells, as well as

Melatonin: endocrine photoperiod signal

Melatonin, an indole amine, is secreted by the pineal gland. This hormone functions as the biological signal for day length or, more precisely, night length. Melatonin synthesis and secretion occurs exclusively at night and is inhibited directly by light. The duration of its release is proportional to night length; consequently, short-day animals experience longer durations of melatonin secretion, than do long-day animals, and use this temporal information to determine the time of the year.

Melatonin: influences on the immune system

The role of melatonin as an immunomodulator is well established for many species, including humans [16]. Melatonin receptors have been localized on lymphocytes, and in vitro melatonin treatment enhances splenocyte proliferation (the division of immune cells) in rodents [47]. Enhancement of immune function in mice is mediated directly through type 2 melatonin receptors (mt-2) on lymphocytes [48]. Melatonin also stimulates the production of endogenous opioids directly from T cells, which might

Concluding remarks

Both the incidence and responses to stressors varies on a seasonal basis. Furthermore, stress can impair immune function and increase disease susceptibility. Consequently, seasonal changes in immune responses have evolved as adaptive mechanisms to counter seasonal stress-induced immune suppression [16]; these changes appear to be defined by seasonal fluctuations in energy availability. Experimental manipulations of energy availability alter immune function in the expected direction; that is,

Acknowledgements

This work was supported by NSF grant IBN 00–08454 and NIH grants MH H057535 and MH066144. I thank A.K. Hotchkiss, A.C. DeVries, I. Zucker, L.M. Pyter and G.N. Neigh for helpful comments on the manuscript. I am also grateful to G.N. Neigh for assistance with the figures.

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Trends in Immunology

Seasonal immune function and sickness responses

Abstract

Section snippets

Energy and seasonal immune function

Photoperiod effects on the immune system

Melatonin: endocrine photoperiod signal

Melatonin: influences on the immune system

Concluding remarks

Acknowledgements

Trends Ecol. Evol.

Poult. Sci.

Parasitol. Today

Life Sci.

Cell. Immunol.

Neurosci. Biobehav. Rev.

Brain Behav. Immun.

Gen. Comp. Endocrinol.

Free Radic. Biol. Med.

Poult. Sci.

Cell. Immunol.

Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement

J. Biol. Rhythms

Seasonal changes in immune function

Q. Rev. Biol.

Food supplements modulate changes in leucocyte numbers in breeding male ground squirrels

J. Exp. Biol.

Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels

Am. J. Physiol. Regul. Integr. Comp. Physiol.

The Evolution of Life Histories

Seasonal changes in immune response and parasite impact on hosts

Am. Nat.

Trade-offs in evolutionary immunology: just what is the cost of immunity?

Oikos

Ecological immunology: life history trade-offs and immune defenses in birds

Behav. Ecol.

Assessing the cost of mounting an immune response

Am. Nat.

Cost of resistance: relationship between reduced fertility and increased resistance in a snail–schistosome host–parasite system

Proc. R. Soc. Lond. B. Biol. Sci.

Costs of immune response in cold-stressed laboratory mice selected for high and low basal metabolism rates

Proc. R. Soc. Lond. B. Biol. Sci.

Reductions in total body fat decrease humoral immunity

Proc. R. Soc. Lond. B. Biol. Sci.

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Science

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Am. J. Physiol. Regul. Integr. Comp. Physiol.

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Am. J. Physiol.

Lethal weight loss: the focus shifts to signal transduction

Sci. STKE

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Nature

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Horizontal prion transmission in mule deer

Nature

SARS, wildlife, and human health

Science