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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 May 7;270(1518):905–911. doi: 10.1098/rspb.2003.2341

Reductions in total body fat decrease humoral immunity.

Gregory E Demas 1, Deborah L Drazen 1, Randy J Nelson 1
PMCID: PMC1691330  PMID: 12803904

Abstract

Mounting an immune response requires substantial energy, and it is well known that marked reductions in energy availability (e.g. starvation) can suppress immune function, thus increasing disease susceptibility and compromising survival. We tested the hypothesis that moderate reductions in energy availability impair humoral immunity. Specifically, we examined the effects of partial lipectomy (LIPx) on humoral immunity in two seasonally breeding rodent species, prairie voles (Microtus ochrogaster) and Siberian hamsters (Phodopus sungorus). Animals received bilateral surgical removal of epididymal white adipose tissue (EWATx), inguinal white adipose tissue (IWATx) or sham surgeries and were injected with the antigen keyhole limpet haemocyanin (KLH) either four or 12 weeks after surgery. In prairie voles, serum anti-KLH immunoglobulin G (IgG) did not differ significantly at four weeks. At 12 weeks, serum IgG was significantly reduced in IWATx, but not EWATx animals, compared with sham-operated animals. In Siberian hamsters, both IWATx and EWATx animals reduced serum IgG at four weeks. At 12 weeks, EWATx hamsters displayed a significant compensatory increase in IWAT pad mass compared with sham-operated hamsters, and serum IgG no longer differed from sham-operated animals. There was no significant increase in EWAT in IWATx hamsters compared with sham animals and IgG remained significantly reduced in IWATx hamsters. These results suggest that reductions in energy availability can impair humoral immunity.

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Selected References

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  1. Ardawi M. S., Newsholme E. A. Metabolism in lymphocytes and its importance in the immune response. Essays Biochem. 1985;21:1–44. [PubMed] [Google Scholar]
  2. Bartness T. J., Wade G. N. Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev. 1985 Winter;9(4):599–612. doi: 10.1016/0149-7634(85)90006-5. [DOI] [PubMed] [Google Scholar]
  3. Chandra R. K. Nutrition and the immune system from birth to old age. Eur J Clin Nutr. 2002 Aug;56 (Suppl 3):S73–S76. doi: 10.1038/sj.ejcn.1601492. [DOI] [PubMed] [Google Scholar]
  4. Dark J., Forger N. G., Stern J. S., Zucker I. Recovery of lipid mass after removal of adipose tissue in ground squirrels. Am J Physiol. 1985 Jul;249(1 Pt 2):R73–R78. doi: 10.1152/ajpregu.1985.249.1.R73. [DOI] [PubMed] [Google Scholar]
  5. Demas G. E., Chefer V., Talan M. I., Nelson R. J. Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am J Physiol. 1997 Nov;273(5 Pt 2):R1631–R1637. doi: 10.1152/ajpregu.1997.273.5.R1631. [DOI] [PubMed] [Google Scholar]
  6. Demas G. E., Drazen D. L., Jasnow A. M., Bartness T. J., Nelson R. J. Sympathoadrenal system differentially affects photoperiodic changes in humoral immunity of Siberian hamsters (Phodopus sungorus). J Neuroendocrinol. 2002 Jan;14(1):29–35. doi: 10.1046/j.0007-1331.2001.00736.x. [DOI] [PubMed] [Google Scholar]
  7. Drazen D. L., Demas G. E., Nelson R. J. Leptin effects on immune function and energy balance are photoperiod dependent in Siberian hamsters (Phodopus sungorus). Endocrinology. 2001 Jul;142(7):2768–2775. doi: 10.1210/endo.142.7.8271. [DOI] [PubMed] [Google Scholar]
  8. Drazen D. L., Kriegsfeld L. J., Schneider J. E., Nelson R. J. Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. Am J Physiol Regul Integr Comp Physiol. 2000 Jun;278(6):R1401–R1407. doi: 10.1152/ajpregu.2000.278.6.R1401. [DOI] [PubMed] [Google Scholar]
  9. Faggioni R., Feingold K. R., Grunfeld C. Leptin regulation of the immune response and the immunodeficiency of malnutrition. FASEB J. 2001 Dec;15(14):2565–2571. doi: 10.1096/fj.01-0431rev. [DOI] [PubMed] [Google Scholar]
  10. Faust I. M., Johnson P. R., Hirsch J. Noncompensation of adipose mass in partially lipectomized mice and rats. Am J Physiol. 1976 Aug;231(2):539–544. doi: 10.1152/ajplegacy.1976.231.2.538. [DOI] [PubMed] [Google Scholar]
  11. Hamilton J. M., Wade G. N. Lipectomy does not impair fattening induced by short photoperiods or high-fat diets in female Syrian hamsters. Physiol Behav. 1988;43(1):85–92. doi: 10.1016/0031-9384(88)90102-3. [DOI] [PubMed] [Google Scholar]
  12. Harris Ruth B. S., Hausman Dorothy B., Bartness Timothy J. Compensation for partial lipectomy in mice with genetic alterations of leptin and its receptor subtypes. Am J Physiol Regul Integr Comp Physiol. 2002 Nov;283(5):R1094–R1103. doi: 10.1152/ajpregu.00339.2002. [DOI] [PubMed] [Google Scholar]
  13. Klingenspor M., Niggemann H., Heldmaier G. Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J Comp Physiol B. 2000 Feb;170(1):37–43. doi: 10.1007/s003600050005. [DOI] [PubMed] [Google Scholar]
  14. Kral J. G. Surgical reduction of adipose tissue in the male Sprague-Dawley rat. Am J Physiol. 1976 Oct;231(4):1090–1096. doi: 10.1152/ajplegacy.1976.231.4.1090. [DOI] [PubMed] [Google Scholar]
  15. Kriegsfeld L. J., Nelson R. J. Gonadal and photoperiodic influences on body mass regulation in adult male and female prairie voles. Am J Physiol. 1996 May;270(5 Pt 2):R1013–R1018. doi: 10.1152/ajpregu.1996.270.5.R1013. [DOI] [PubMed] [Google Scholar]
  16. Lord G. M., Matarese G., Howard J. K., Baker R. J., Bloom S. R., Lechler R. I. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998 Aug 27;394(6696):897–901. doi: 10.1038/29795. [DOI] [PubMed] [Google Scholar]
  17. Martí A., Marcos A., Martínez J. A. Obesity and immune function relationships. Obes Rev. 2001 May;2(2):131–140. doi: 10.1046/j.1467-789x.2001.00025.x. [DOI] [PubMed] [Google Scholar]
  18. Mauer M. M., Bartness T. J. Body fat regulation after partial lipectomy in Siberian hamsters is photoperiod dependent and fat pad specific. Am J Physiol. 1994 Mar;266(3 Pt 2):R870–R878. doi: 10.1152/ajpregu.1994.266.3.R870. [DOI] [PubMed] [Google Scholar]
  19. Mauer M. M., Bartness T. J. Fat pad-specific compensatory mass increases after varying degrees of lipectomy in Siberian hamsters. Am J Physiol. 1997 Dec;273(6 Pt 2):R2117–R2123. doi: 10.1152/ajpregu.1997.273.6.R2117. [DOI] [PubMed] [Google Scholar]
  20. Mauer M. M., Harris R. B., Bartness T. J. The regulation of total body fat: lessons learned from lipectomy studies. Neurosci Biobehav Rev. 2001 Jan;25(1):15–28. doi: 10.1016/s0149-7634(00)00047-6. [DOI] [PubMed] [Google Scholar]
  21. Moret Y., Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science. 2000 Nov 10;290(5494):1166–1168. doi: 10.1126/science.290.5494.1166. [DOI] [PubMed] [Google Scholar]
  22. Nelson R. J., Demas G. E. Seasonal changes in immune function. Q Rev Biol. 1996 Dec;71(4):511–548. doi: 10.1086/419555. [DOI] [PubMed] [Google Scholar]
  23. Nelson R. J., Fine J. B., Demas G. E., Moffatt C. A. Photoperiod and population density interact to affect reproductive and immune function in male prairie voles. Am J Physiol. 1996 Mar;270(3 Pt 2):R571–R577. doi: 10.1152/ajpregu.1996.270.3.R571. [DOI] [PubMed] [Google Scholar]
  24. Nova E., Samartín S., Gómez S., Morandé G., Marcos A. The adaptive response of the immune system to the particular malnutrition of eating disorders. Eur J Clin Nutr. 2002 Aug;56 (Suppl 3):S34–S37. doi: 10.1038/sj.ejcn.1601482. [DOI] [PubMed] [Google Scholar]
  25. Pond C. M. Interactions between adipose tissue and the immune system. Proc Nutr Soc. 1996 Mar;55(1B):111–126. doi: 10.1079/pns19960014. [DOI] [PubMed] [Google Scholar]
  26. Woods S. C., Seeley R. J. Adiposity signals and the control of energy homeostasis. Nutrition. 2000 Oct;16(10):894–902. doi: 10.1016/s0899-9007(00)00454-8. [DOI] [PubMed] [Google Scholar]
  27. Yaqoob P., Newsholme E. A., Calder P. C. The effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation. Immunology. 1994 Aug;82(4):603–610. [PMC free article] [PubMed] [Google Scholar]
  28. Yellon S. M., Teasley L. A., Fagoaga O. R., Nguyen H. C., Truong H. N., Nehlsen-Cannarella L. Role of photoperiod and the pineal gland in T cell-dependent humoral immune reactivity in the Siberian hamster. J Pineal Res. 1999 Nov;27(4):243–248. doi: 10.1111/j.1600-079x.1999.tb00622.x. [DOI] [PubMed] [Google Scholar]

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