Different Photoperiods Affect Proliferation of Lymphocytes but Not Expression of Cellular,Humoral,or Innate Immunity in Hamsters

Abstract

In seasonal mammals, photoperiod change is associated with a suite of alterations in physiology. It has recently been proposed that the immune response is one of the systems regulated by changes in photoperiod, although this hypothesis has not been rigorously challenged by assays of functional immune responses. The aim of this study was to test the hypothesis that photoperiod modulates immune responsiveness in Syrian (Mesocricetus auratus) and Siberian (Phodopus sungorus) hamsters. Consistent with previously reported data, short-day-housed (SD) animals exhibited a significant increase in lymph node cell (LNC) numbers and increased cellular proliferation in response to the polyclonal mitogen concanavalin Acompared to long-day-housed (LD) animals. In contrast, LNC numbers from intact or gonadectomized SD animals that had been sensitized with the antigen dinitrofluorobenzene (DNFB) exhibited a reduced ex vivo proliferative response and reduced production of interleukin-6 (IL-6) compared to LD animals. In vivo studies of the contact hypersensitivity response of animals that had previously been sensitized, and subsequently challenged, with DNFB were similar in SD and LD animals, as was the proliferative activity of LNC recovered from these animals. There were also no photoperiodic differences in the antidinitrophenyl antibody response of animals sensitized with DNFB, or the anti–sheep red blood cell (srbc) response of animals immunized with srbc. Furthermore, no differences could be detected in the activity of natural killer cells from spleens of LD and SD Siberian hamsters, or in lipopolysaccharide-induced IL-6 production by LD and SD Syrian hamsters in vivo. Thus, although photoperiod is able to influence factors regulating the gross number and non-antigen-specific proliferation of lymphocytes in seasonally breeding mammals, day length does not directly influence activation of an effective immune response. The authors conclude, therefore, that expression of the immune response is not directly modified or compromised by photoperiod in these seasonally breeding hamster species.

Keywords

seasonal immunity antibody cell-mediated immunity cytotoxicity inflammation cytokines

References

Atcha Z , Cagampang FRA , Stirland JA , Morris ID , Brooks AN , Ebling FJP , Klingenspor M , and Loudon ASI (2000) Leptin acts on metabolism in a photoperiod-dependent manner, but has no effect on reproductive function in the seasonally breeding Siberian hamster (Phodopus sungorus). Endocrinology 141:4128-4135.

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

Bartness TJ and Wade GN (1984) Photoperiodic control of body weight and energy metabolism in Syrian hamsters (Mesocricetus auratus): Role of the pineal gland, melatonin, gonads, and diet. Endocrinology 114:492-498.

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

Blom JMC , Gerber JM , and Nelson RJ (1994) Day length affects immune cell numbers in deer mice: Interactions with age, sex, and prenatal photoperiod. Am J Physiol 36:R596-R601.

Bouchard B , Ormandy CJ , DiSanto JP , and Kelly PA (1999) Immune system development and function in prolactin receptor-deficient mice. J Immunol 163:576-582.

Brainard GC , Knobler RL , Podolin PL , Lasava M , and Lubin FD (1987) Neuroimmunology: Modulation of hamster immune system by photoperiod. Life Sci 40:1319-1326.

Champney TH and McMurray DN (1991) Spleen morphology and lymphoproliferative activity in short photoperiod exposed hamsters. In Role of Melatonin and Pineal Peptides in Neuroimmunomodulation, F Fraschini and RJ Reiter , eds, pp 219-224, Plenum Press, New York.

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

10.

Demas GE and Nelson RJ (1996) Photoperiod and temperature interact to affect immune parameters in adult deer mice. J Biol Rhythms 11:94-103.

11.

Demas GE and Nelson RJ (1998a) Exogenous melatonin enhances cell-mediated, but not humoral, immune function in adult male deer mice (Peromyscus maniculatus). J Biol Rhythms 13:245-252.

12.

Demas GE and Nelson RJ (1998b) Photoperiod, ambient temperature, and food availability interact to affect reproductive and immune function in adult male deer mice (Peromyscus maniculatus). J Biol Rhythms 13:253-261.

13.

Demas GE and Nelson RJ (1998c) Short-day enhancement of immune function is independent of steroid hormones in deer mice (Peromyscus maniculatus). J Comp Physiol B 168:419-426.

14.

Dorshkind K and Horseman ND (2000) The roles of prolactin, growth hormone, insulin-like growth factor-I, and thyroid hormones in lymphocyte development and function: Insights from genetic models of hormone and hormone receptor deficiency. Endocr Rev 21:292-312.

15.

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

16.

Drazen DL , Kriegsfeld LJ , Schneider JE , and Nelson RJ (2000) Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. Am J Physiol 278:R1401-R1407.

17.

Guerrero JM and Reiter RJ (1992) A brief review of pineal gland-immune interrelationships. Endocr Res 18:91-113.

18.

Hope JC , Campbell F , and Hopkins SJ (2000) Deficiency of interleukin-2 or interleukin-6 reduces lymphocyte proliferation, but only interleukin-6 deficiency decreases the CH response. Eur J Immunol 30:197-203.

19.

Hope JC , Dearman RJ , Debicki RJ , Kimber I , and Hopkins SJ (1994) Interleukin-6 production by draining lymph node cells following primary contact sensitisation of mice: Relationship to the proliferative response. Int Arch Allergy Appl Immunol 103:378-383.

20.

Hope JC , Dearman RJ , Kimber I , and Hopkins SJ (1994) The kinetics of cytokine production by draining lymph node cells following primary exposure of mice to chemical allergens. Immunology 83:250-255.

21.

Horton TH , Buxton OM , Losee-Olson S , and Turek FW (2000) Twenty-four-hour profiles of serum leptin in Siberian and golden hamsters: Photoperiodic and diurnal variations. Horm Behav 37:388-398.

22.

Klingenspor M , Dickopp A , Heldmaier G , and Klaus S (1996) Short photoperiod reduces leptin gene expression in brown and white adipose tissue of Djungarian hamsters. FEBS Lett 399:290-294.

23.

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

24.

Lord GM , Matarese G , Howard JK , Baker RJ , Bloom SR , and Lechler RI (1998) Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394:897-901.

25.

Loudon ASI (1994) Photoperiod and the regulation of annual and circannual cycles of food intake. Proc Nutr Soc 53:495-507.

26.

Loudon ASI , Curlewiss JD , Milne JA , and McNeilly AS (1989) A comparison of the seasonal hormone changes and pattern of growth, voluntary food intake and reproduction in juvenile and adult red deer (Cervus elaphus) and Pere David's deer (Elaphurus davidianus) hinds. J Endocrinol 122:733-745.

27.

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

28.

Miller AJ , Luheshi G , Rothwell NJ , and Hopkins SJ (1997) Local cytokine induction by lipopolysaccharide in the rat air pouch and its relationship to the febrile response. Am J Physiol 272:R857-R861.

29.

Nelson RJ and Blom JMC (1994) Photoperiodic effects on tumor development and immune function. J Biol Rhythms 9:233-249.

30.

Nelson RJ and Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511-548.

31.

Soares MJ , Colosi P , and Talamantes F (1983) Development of a homologous radioimmunoassay for secreted hamster prolactin. Proc Soc Exp Biol Med 172:379-381.

32.

Vaughan MK , Hubbard GB , and Champney TH (1987) Splenic hypertrophy and extramedullary hematopoiesis induced in male Syrian hamsters by short photoperiod or melatonin injection and reversed by melatonin pellets or pinealectomy. Am J Anat 179:131-136.

33.

Vriend J and Lauber J (1973) Effects of light intensity, wavelength and quanta on gonads and spleen of the deer mouse. Nature 244:37-38.

34.

Yellon SM , Fagoaga OR , and Nehlsen-Cannarella SL (1999) Influence of photoperiod on immune cell functions in the male Siberian hamster. Am J Physiol 45:R97-R102.

35.

Yellon SM , Teasley LA , Fagoaga OR , Nguyen HC , Truong HN , and Nehlsen-Cannarella SL (1999) Role of photoperiod and the pineal gland in Tcell-dependent humoral immune reactivity in the Siberian hamster. J Pineal Res 27:243-248.

36.

Yu-Lee LY (1997) Molecular actions of prolactin in the immune system. Proc Soc Exp Biol Med 215:35-52.