Effects of dominance status and environmental enrichment on cell-mediated immunity in rhesus macaques

Applied Animal Behaviour Science

Volumn 56, Issue 2-4, 1998, Pages 319-332

  Schapiro, Steven J ^a   Nehete, Pramod N ^a   Perlman, Jaine E ^a   Bloomsmith, Mollie A ^a   Sastry, K Jagannadha ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cytokines; Environmental enrichment; Lymphocytes; Macaca mulatta; Natural killer cells; Social dominance

Indexed keywords

EID: 0031960801     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-1591(97)00087-7     Document Type: Article

References (50)

1. Bayne K., Mainzer H., Dexter S., Campbell G., Yamada F., Suomi S. The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. Am. J. Primatol. 23:1991;23-35.
2. Benveniste O., Vaslin B., Le Grand R., Cheret A., Matheux F., Theodoro F., Cranage M.P., Dormont D. Comparative interleukin (IL)-2/interferon (IFN)-γ and IL-4/IL-10 responses during acute infection of macaques inoculated with attenuated nef-truncated or pathogenic SIVmac251 virus. Proc. Natl. Acad. Sci. USA. 93:1996;3658-3663.
3. Bloomsmith M.A., Alford P.L., Maple T.L. Successful feeding enrichment for captive chimpanzees. Am. J. Primatol. 16:1988;155-164.
4. Boccia M.L., Laudenslager M.L., Reite M.L. Spatial distribution of food and dominance related behavior in bonnet macaques. Am. J. Primatol. 16:1988;123-130.
5. Boccia M.L., Laudenslager M.L., Broussard C.L., Hijazi A.S. Immune responses following competitive water tests in two species of macaques. Brain Behav. Immunity. 6:1992;201-213.
6. Boccia M.L., Scanlan J.M., Laudenslager M.L., Berger C.L., Hijazi A.S., Reite M.L. Juvenile friends, behavior, and immune responses to separation in bonnet macaque infants. Physiol. Behav. 61:1997;191-198.
7. Capitanio J.P., Mendoza S.P., McChesney M. Influences of blood sampling procedures on basal hypothalamic-pituitary-adrenal hormone levels and leukocyte values in rhesus macaques (Macaca mulatta). J. Med. Primatol. 25:1996;26-33.
8. Champoux M., Coe C.L., Schanberg S.M., Kuhn C.M., Suomi S.J. Hormonal effects of early rearing conditions in the infant rhesus monkey. Am. J. Primatol. 19:1989;111-117.
9. Clarke M.R., Koritnik D.R., Martin L.N., Baskin G.B. Cage enrichment, physiology, and behavior in nursery-reared rhesus monkeys. Am. J. Primatol. Suppl. 1:1989;53-57.
10. Clarke M.R., Harrison R.M., Didier E.S. Behavioral, immunological, and hormonal responses associated with social change in rhesus monkeys (Macaca mulatta). Am. J. Primatol. 39:1996;223-233.
11. Clerici M., Shearer G.H. A TH1 to TH2 switch is a critical step in the etiology of HIV infection. Immunol. Today. 14:1993;107-111.
12. Coe C.L. Psychosocial factors and immunity in nonhuman primates: A review. Psychosom. Med. 55:1993;298-308.
13. Coe C.L., Rosenberg L.T., Levine S. Effect of maternal separation on the complement system and antibody responses in infant primates. Int. J. Neurosci. 40:1988;289-302.
14. Coe C.L., Lubach G.R., Ershler W.B., Klopp R.G. Influence of early rearing on lymphocyte proliferation responses in juvenile rhesus monkeys. Brain Behav. Immunity. 3:1989;47-60.
15. Coe C.L., Ershler W.B., Champoux M., Olson J. Psychosocial factors and immune senescence in the aged primate. Ann. NY Acad. Sci. 650:1992;276-282.
16. Cohen S., Kaplan J.R., Cunnick J.E., Manuck S.B., Rabin B.S. Chronic social stress, affiliation, and cellular immune response in nonhuman primates. Psychol. Sci. 3:1992;301-304.
17. Crockett C.M., Bowers C.L., Bowden D.M., Sackett G.P. Sex differences in compatibility of pair-housed adult longtailed macaques. Am. J. Primatol. 32:1994;73-94.
18. Gordon T.P., Gust D.A., Wilson M.E., Ahmed-Ansari A., Brodie A.R., McClure H.M. Social separation and reunion affects immune system in juvenile rhesus monkeys. Physiol. Behav. 51:1992;467-472.
19. Gust D.A., Gordon T.P., Wilson M.E., Ahmed-Ansari A., Brodie A.R., McClure H.M. Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav. Immunity. 5:1991;296-307.
20. Gust D.A., Gordon T.P., Wilson M.E., Brodie A.R., Ahmed-Ansari A., McClure H.M. Removal from natal social group to peer housing affects cortisol levels and absolute numbers of T cell subsets in juvenile rhesus monkeys. Brain Behav. Immunity. 6:1992;189-199.
21. Gust D.A., Gordon T.P., Hambright M.K. Response to removal from and return to a social group in adult male rhesus monkeys. Physiol. Behav. 53:1993;599-602.
22. Gust D.A., Gordon T.P., Brodie A.R., McClure H.M. Effect of a preferred companion in modulating stress in adult female rhesus monkeys. Physiol. Behav. 55:1994;681-684.
23. Gust D.A., Gordon T.P., Brodie A.R., McClure H.M. Effect of companions in modulating stress associated with new group formation in juvenile rhesus macaques. Physiol. Behav. 59:1996;941-945.
24. Gust D.A., Gordon T.P., Wilson M.E., Brodie A.R., Ahmed-Ansari A., McClure H.M. Group formation of female pigtail macaques (Macaca nemestrina). Am. J. Primatol. 39:1996;263-273.
25. Kaplan J.R., Heise E.R., Manuck S.B., Shively C.A., Cohen S., Rabin B.S., Kasprowicz A.L. The relationship of agonistic and affiliative behavior patterns to cellular immune function among cynomolgus monkeys (Macaca fascicularis) living in unstable social groups. Am. J. Primatol. 25:1991;157-173.
26. Laudenslager M.L., Boccia M.L. Some observations on psychosocial stressors, immunity, and individual differences in nonhuman primates. Am. J. Primatol. 39:1996;205-221.
27. Laudenslager M.L., Capitanio J.P., Reite M.L. Possible effects of early separation experiences on subsequent immune function in adult macaque monkeys. Am. J. Psychiatry. 142:1985;862-865.
28. Laudenslager M.L., Held P.E., Boccia M.L., Reite M.L., Cohen J.J. Behavioral and immunological consequences of brief mother-infant separation: A species comparison. Dev. Psychobiol. 23:1990;247-264.
29. Laudenslager M.L., Berger C.L., Boccia M.L., Reite M.L. Natural cytotoxicity toward K562 cells by macaque lymphocytes from infancy through puberty: Effects of early social challenge. Brain Behav. Immunity. 10:1996;275-287.
30. Lemieux A.M., Coe C.L., Ershler W.B., Karaszewski J.W. Surgical and psychological stressors differentially affect cytolytic responses in the rhesus monkey. Brain Behav. Immunity. 10:1996;27-43.
31. Line S.W., Kaplan J.R., Heise E.R., Hilliard J.K., Cohen S., Rabin B.S., Manuck S.B. Effects of social reorganization on cellular immunity in male cynomolgus monkeys. Am. J. Primatol. 39:1996;235-249.
32. Lubach G.R., Coe C.L., Ershler W.B. Effects of early rearing environment on immune responses of infant rhesus monkeys. Brain Behav. Immunity. 9:1995;31-46.
33. Lubach G.R., Coe C.L., Karaszewski J.W., Ershler W.B. Effector and target cells in the assessment of natural cytotoxic activity of rhesus monkeys. Am. J. Primatol. 39:1996;275-287.
34. Maggio-Price L., Pollack S.B., Shiota F., Thouless M., Moazed T., Grossmann A. Characterization of natural killer cell activity in Macaca nemestrina. Am. J. Primatol. 39:1996;252-261.
35. Nehete, P.N., Arlinghaus, R.B., Sastry, K.J., Satterfield, W.C., Matherne, C.M., 1993. HIV-specific T-cell responses in rhesus monkeys immunized with synthetic peptides from gp160. In: Lerner, R.A., Brown, F., Ginsberg, H.S. (Eds.), Vaccines 93. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 91-94.
36. Nehete P.N., Murthy K.K., Satterfield W.C., Arlinghaus R.B., Sastry K.J. Studies on V3-specific cross-reactive T-cell responses in chimpanzees chronically infected with HIV-1 IIIB. AIDS. 9:1995;567-572.
37. Parks K.A., Novak M.A. Observations of increased activity and tool use in captive rhesus monkeys exposed to troughs of water. Am. J. Primatol. 29:1993;13-25.
38. Reinhardt V. Pair-housing rather than single-housing for laboratory rhesus macaques. J. Med. Primatol. 23:1994;426-431.
39. Sapolsky R. Testicular function, social rank, and personality among wild baboons. Psychoneuroendocrinology. 16:1991;281-295.
40. Schapiro S.J., Bloomsmith M.A. Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys. Am. J. Primatol. 32:1994;159-170.
41. Schapiro S.J., Bloomsmith M.A. Behavioral effects of enrichment on singly-housed, yearling rhesus monkeys: An analysis including three enrichment conditions and a control group. Am. J. Primatol. 35:1995;89-101.
42. Schapiro S.J., Bushong D. Effects of enrichment on veterinary treatment of laboratory rhesus macaques (Macaca mulatta). Anim. Welfare. 3:1994;25-36.
43. Schapiro S.J., Bloomsmith M.A., Kessel A.L., Shively C.A. Effects of enrichment and housing on cortisol response in juvenile rhesus monkeys. Appl. Anim. Behav. Sci. 37:1993;251-263.
44. Schapiro S.J., Lee-Parritz D.E., Taylor L.L., Watson L., Bloomsmith M.A., Petto A. Behavioral management of specific pathogen-free (SPF) rhesus macaques: Group formation, reproduction, and parental competence. Lab. Anim. Sci. 44:1994;229-234.
45. Schapiro S.J., Bloomsmith M.A., Porter L.M., Suarez S.A. Enrichment effects on rhesus monkeys successively housed singly, in pairs, and in groups. Appl. Anim. Behav. Sci. 48:1996;159-171.
46. Schapiro S.J., Bloomsmith M.A., Suarez S.A., Porter L.M. Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys. Am. J. Primatol. 40:1996;247-260.
47. Schapiro S.J., Bloomsmith M.A., Suarez S.A., Porter L.M. A comparison of the effects of simple versus complex environmental enrichment on the behaviour of group-housed, subadult rhesus macaques. Anim. Welfare. 6:1997;17-28.
48. Schmitt D.A., Sonnenfeld G., Husson D., Tkaczuk J., Andre E., Schaffar L. In vitro interleukin-1 and 2 production and interleukin 2 receptor expression in the rhesus monkey. Life Sci. 59:1996;931-937.
49. Terao K., Hamano M., Koyama T. The repeated procedure of weaning and peer group formation causes accumulation of stress and changes of plasma cortisol level and natural killer cell activity in squirrel monkeys (Saimiri sciureus). Primates. 36:1995;121-127.
50. Villinger F., Hunt D., Mayne A., Vuchetich M., Findley H., Ansari A.A. Qualitative and quantitative studies of cytokines synthesized and secreted by non-human primate peripheral blood mononuclear cells. Cytokine. 5:1993;469-479.