Immune function and HPA axis activity in free-ranging rhesus macaques

Physiology and Behavior

Volumn 104, Issue 3, 2011, Pages 507-514

  Hoffman, Christy L ^a,b   Higham, James P ^b   Heistermann, Michael ^c   Coe, Christopher L ^d   Prendergast, Brian J ^b,e   Maestripieri, Dario ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c GERMAN PRIMATE CENTER   (Germany)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

Aging; Allostatic load; Cortisol; Cytokines; Reproduction; Rhesus macaque

Indexed keywords

GLUCOCORTICOID; INTERLEUKIN 1 ANTIBODY; INTERLEUKIN 6; INTERLEUKIN 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; BODY CONSTITUTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES ANALYSIS; FEMALE; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE SYSTEM; INTERMETHOD COMPARISON; LACTATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; REPRODUCTION; RHESUS MONKEY; SOCIAL STATUS;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; CYTOKINES; FEMALE; GLUCOCORTICOIDS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LACTATION; LONGITUDINAL STUDIES; MACACA MULATTA; PITUITARY-ADRENAL SYSTEM; PREGNANCY; REGRESSION ANALYSIS; SOCIAL ENVIRONMENT;

EID: 79959836698     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.05.021     Document Type: Article

References (71)

1. Romero L.M., Wikelski M. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci USA 2001, 98:7366-7370.
2. Romero L.M., Wikelski M. Stress physiology as a predictor of survival in Galapagos marine iguanas. Proc R Soc B Biol Sci 2010, 277:3157-3162.
3. Hansel A., Hong S.Z., Camara R.J.A., von Kanel R. Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci Biobehav Rev 2010, 35:115-121.
4. Pride R.E. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta). Biol Lett 2005, 1:60-63.
5. McEwen B.S., Stellar E. Stress and the individual - mechanisms leading to disease. Arch Intern Med 1993, 153:2093-2101.
6. McEwen B.S., Seeman T. Protective and damaging effects of mediators of stress - elaborating and testing the concepts of allostasis and allostatic load. Ann N Y Acad Sci 1999, 896:30-47.
7. Goshen I., Yirmiya R. Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol 2009, 30:30-45.
8. Reyes T.M., Coe C.L. The proinflammatory cytokine network: interactions in the CNS and blood of rhesus monkeys. Am J Physiol Regul Integr Comp Physiol 1998, 274:R139-R144.
9. Chrousos G.P., Gold P.W. The concepts of stress and stress system disorders - overview of physical and behavioral homeostasis. J Am Med Assoc 1992, 267:1244-1252.
10. Avitsur R., Padgett D.A., Sheridan J.F. Social interactions, stress, and immunity. Neurol Clin 2006, 24:483-491.
11. Christian L.M., Graham J.E., Padgett D.A., Glaser R., Kiecolt-Glaser J.K. Stress and wound healing. Neuroimmunomodulation 2006, 13:337-346.
12. Altemus M., Rao B., Dhabhar F.S., Ding W.H., Granstein R. Stress-induced changes in skin barrier function in healthy women. J Invest Dermatol 2001, 117:309-317.
13. Ferrucci L., Corsi A., Lauretani F., Bandinelli S., Bartali B., Taub D.D., et al. The origins of age-related proinflammatory state. Blood 2005, 105:2294-2299.
14. Forsey R.J., Thompson J.M., Ernerudh J., Hurst T.L., Strindhall J., Johansson B., et al. Plasma cytokine profiles in elderly humans. Mech Ageing Dev 2003, 124:487-493.
15. Cava F., Gonzalez C., Pascual M.J., Navajo J.A., Gonzalez-Buitrago J.M. Biological variation of interleukin 6 (IL-6) and soluble interleukin 2 receptor (sIL2r) in serum of healthy individuals. Cytokine 2000, 12:1423-1425.
16. Rao K.M.K., Pieper C.S., Currie M.S., Cohen H.J. Variability of plasma Il-6 and cross-linked fibrin dimers over time in community-dwelling elderly subjects. Am J Clin Pathol 1994, 102:802-805.
17. Epel E.S., Lin J., Wilhelm F.H., Wolkowitz O.M., Cawthon R., Adler N.E., et al. Cell aging in relation to stress arousal and cardiovascular disease risk factors. Psychoneuroendocrinology 2006, 31:277-287.
18. Rozlog L.A., Kiecolt-Glaser J.K., Marucha P.T., Sheridan J.F., Glaser R. Stress and immunity: implications for viral disease and wound healing. J Periodontol 1999, 70:786-792.
19. Brunner E.J., Hemingway H., Walker B.R., Page M., Clarke P., Juneja M., et al. Adrenocortical, autonomic, and inflammatory causes of the metabolic syndrome - nested case-control study. Circulation 2002, 106:2659-2665.
20. Kulstad J.J., McMillan P.J., Leverenz J.B., Cook D.G., Green P.S., Peskind E.R., et al. Effects of chronic glucocorticoid administration on insulin-degrading enzyme and amyloid-beta peptide in the aged macaque. J Neuropathol Exp Neurol 2005, 64:139-146.
21. Soderholm J.D., Yang P.C., Ceponis P., Vohra A., Riddell R., Sherman P.M., et al. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology 2002, 123:1099-1108.
22. Cavigelli S.A., Ragan C.M., Michael K.C., Kovacsics C.E., Brliscke A.P. Stable behavioral inhibition and glucocorticoid production as predictors of longevity. Physiol Behav 2009, 98:205-214.
23. Blas J., Bortolotti G.R., Tella J.L., Baos R., Marchant T.A. Stress response during development predicts fitness in a wild, long lived vertebrate. Proc Natl Acad Sci USA 2007, 104:8880-8884.
24. Chung H.Y., Cesari M., Anton S., Marzetti E., Giovannini S., Seo A.Y., et al. Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 2009, 8:18-30.
25. Harris T.B., Ferrucci L., Tracy R.P., Corti M.C., Wacholder S., Ettinger W.H., et al. Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am J Med 1999, 106:506-512.
26. Lindmark E., Diderholm E., Wallentin L., Siegbahn A. Relationship between interleukin 6 and mortality in patients with unstable coronary artery disease - effects of an early invasive or noninvasive strategy. J Am Med Assoc 2001, 286:2107-2113.
27. Drost A.C., Burleson D.G., Cioffi W.G., Jordan B.S., Mason A.D., Pruitt B.A. Plasma cytokines following thermal-injury and their relationship with patient mortality, burn size, and time postburn. J Trauma Inj Infect & Crit Care 1993, 35:335-339.
28. Ridker P.M., Rifai N., Stampfer M.J., Hennekens C.H. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 2000, 101:1767-1772.
29. Jensen G.L. Inflammation: roles in aging and sarcopenia. JPEN J Parenter Enteral Nutr 2008, 32:656-659.
30. Bruunsgaard H. Effects of tumor necrosis factor-alpha and interleukin-6 in elderly populations. Eur Cytokine Netw 2002, 13:389-391.
31. Baune B.T., Ponath G., Rothermundt M., Roesler A., Berger K. Association between cytokines and cerebral MRI changes in the aging brain. J Geriatr Psychiatry Neurol 2009, 22:23-34.
32. Boekholdt S.M., Peters R.J.G., Hack C.E., Day N.E., Luben R., Bingham S.A., et al. IL-8 plasma concentrations and the risk of future coronary artery disease in apparently healthy men and women - the EPIC-Norfolk prospective population study. Arterioscler Thromb Vasc Biol 2004, 24:1503-1508.
33. Fukuda H., Ichinose T., Kusama T., Sakurai R., Anndow K., Akiyoshi N. Stress assessment in acute care department nurses by measuring interleukin-8. Int Nurs Rev 2008, 55:407-411.
34. Marsland A.L., Sathanoori R., Muldoon M.F., Manuck S.B. Stimulated production of interleukin-8 covaries with psychosocial risk factors for inflammatory disease among middle-aged community volunteers. Brain Behav Immun 2007, 21:218-228.
35. Weik U., Herforth A., Kola-Bachofen V., Deinzer R. Acute stress induces proinflammatory signaling at chronic inflammation sites. Psychosom Med 2008, 70:906-912.
36. Morozink J.A., Friedman E.M., Coe C.L., Ryff C.D. Socioeconomic and psychosocial predictors of interleukin-6 in the MIDUS national sample. Health Psychol 2010, 29:626-635.
37. Baune B.T., Ponath G., Golledge J., Varga G., Arolt V., Rothermundt M., et al. Association between IL-8 cytokine and cognitive performance in an elderly general population - the MEMO-Study. Neurobiol Aging 2008, 29:937-944.
38. Roubenoff R., Harris T.B., Abad L.W., Wilson P.W.F., Dallal G.E., Dinarello C.A. Monocyte cytokine production in an elderly population: effect of age and inflammation. J Gerontol A Biol Sci Med Sci 1998, 53:M20-M26.
39. Wei J., Xu H.M., Davies J.L., Hemmings G.P. Increase of plasma IL-6 concentration with age in healthy-subjects. Life Sci 1992, 51:1953-1956.
40. Wang Y.C., Colditz G.A., Kuntz K.M. Forecasting the obesity epidemic in the aging US population. Obesity 2007, 15:2855-2865.
41. Fain J.N. Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Interleukins 2006, 443-477.
42. Sempere L., Martinez J., de Madaria E., Lozano B., Sanchez-Paya J., Jover R., et al. Obesity and fat distribution imply a greater systemic inflammatory response and a worse prognosis in acute pancreatitis. Pancreatology 2008, 8:257-264.
43. Coe CL, Love GD, Karasawa M, Kawakami N, Kitayama S, Markus HR, et al. Population differences in proinflammatory biology: Japanese have healthier profiles than Americans. Brain Behav Immun In Press, Corrected Proof.
44. Kim M.J., Aiken J.M., Havighurst T., Hollander J., Ripple M.O., Weindruch R. Adult-onset energy restriction of rhesus monkeys attenuates oxidative stress-induced cytokine expression by peripheral blood mononuclear cells. J Nutr 1997, 127:2293-2301.
45. Willette A.A., Bendlin B.B., McLaren D.G., Canu E., Kastman E.K., Kosmatka K.J., et al. Age-related changes in neural volume and microstructure associated with interleukin-6 are ameliorated by a calorie-restricted diet in old rhesus monkeys. Neuroimage 2010, 51:987-994.
46. Sapolsky R.M. The influence of social hierarchy on primate health. Science 2005, 308:648-652.
47. Roth G.S., Mattison J.A., Ottinger M.A., Chachich M.E., Lane M.A., Ingram D.K. Aging in rhesus monkeys: relevance to human health interventions. Science 2004, 305:1423-1426.
48. Hoffman C.L., Higham J.P., Mas-Rivera A., Ayala J.E., Maestripieri D. Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav Ecol 2010, 21:972-978.
49. Hoffman C.L., Ruiz-Lambides A.V., Davila E., Maldonado E., Gerald M.S., Maestripieri D. Sex differences in survival costs of reproduction in a promiscuous primate. Behav Ecol & Sociobiol 2008, 62:1711-1718.
50. Hoffman C.L., Ayala J.E., Mas-Rivera A., Maestripieri D. Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free-ranging female rhesus macaques. Am J Primatol 2010, 72:559-565.
51. Maestripieri D., Hoffman C.L., Fulks R., Gerald M.S. Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Horm Behav 2008, 53:170-176.
52. Melnick D.J., Pearl M.C. Cercopithecines in multimale groups: genetic diversity and population structure. Primate Societies 1987, 121-134. University of Chicago Press, Chicago. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, T.T. Struhsaker (Eds.).
53. Arend W.R. The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev 2002, 13:323-340.
54. Granowitz E.V., Santos A.A., Poutsiaka D.D., Cannon J.G., Wilmore D.W., Wolff S.M., et al. Production of interleukin-1-receptor antagonist during experimental endotoxemia. Lancet 1991, 338:1423-1424.
55. Rawlins R.G., Kessler M.J. The Cayo Santiago Macaques: history, behavior, and biology 1986, SUNY Press, Albany, NY.
56. Ardito G. Checklist of data on gestation length of primates. J Hum Evol 1976, 5:213-222.
57. Nelson E., Hoffman C.L., Gerald M.S., Shultz S. Digit ratio (2D:4D) and dominance rank in female rhesus macaques (Macaca mulatta). Behav Ecol & Sociobiol 2010, 64:1001-1009.
58. Laudenslager M.L., Rasmussen K.L., Berman C.M., Lilly A.A., Shelton S.E., Kalin N.H., et al. A preliminary description of responses of free-ranging rhesus monkeys to brief capture experiences: behavior, endocrine, immune, and health relationships. Brain Behav Immun 1999, 13:124-137.
59. Heistermann M., Ademmer C., Kaumanns W. Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus. Int J Primatol 2004, 25:689-708.
60. Heistermann M., Palme R., Ganswindt A. Comparison of different enzymeimmunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am J Primatol 2006, 68:257-273.
61. Shutt K., MacLarnon A., Heistermann M., Semple S. Grooming in Barbary macaques: better to give than to receive?. Biol Lett 2007, 3:231-233.
62. Ostner J., Heistermann M., Schulke O. Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm Behav 2008, 54:613-619.
63. Higham J.P., MacLarnon A.M., Heistermann M., Ross C., Semple S. Rates of self-directed behaviour and faecal glucocorticoid levels are not correlated in female wild olive baboons (Papio hamadryas anubis). Stress Int J Biol Stress 2009, 12:526-532.
64. Fichtel C., Kraus C., Ganswindt A., Heistermann M. Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Horm Behav 2007, 51:640-648.
65. Girard-Buttoz C., Heistermann M., Krummel S., Engelhardt A. Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiol Behav 2009, 98:168-175.
66. Whitten P.L., Stavisky R., Aureli F., Russell E. Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am J Primatol 1998, 44:57-69.
67. Johnson R.L., Malik I., Berman C.M. On the quantification of suckling intensity in primates. Am J Phys Anthropol 1998, 105:33-42.
68. Cavigelli S.A. Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed femurs, Lemur catta. Anim Behav 1999, 57:935-944.
69. Mateo J.M., Cavigelli S.A. A validation of extraction methods for noninvasive sampling of glucocorticoids in free-living ground squirrels. Physiol Biochem Zool 2005, 78:1069-1084.
70. Sheriff M.J., Krebs C.J., Boonstra R. Assessing stress in animal populations: do fecal and plasma glucocorticoids tell the same story?. Gen Comp Endocrinol 2010, 166:614-619.
71. Reyes T.M., Coe C.L. Interleukin-1 beta differentially affects interleukin-6 and soluble interleukin-6 receptor in the blood and central nervous system of the monkey. J Neuroimmunol 1996, 66:135-141.