Social instability and immunity in rhesus monkeys: The role of the sympathetic nervous system

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1669, 2015, Pages

  Capitanio, John P ^a,b   Cole, Steven W ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Lymph; Nodes; Psychoneuroimmunology; Rhesus monkeys; Social stress; Stress hormones; Sympathetic nervous system

Indexed keywords

ENDOCRINE DISRUPTOR; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNITY; IMMUNOASSAY; NERVOUS SYSTEM; PRIMATE; PUBLIC HEALTH; SOCIAL STATUS; SUBLETHAL EFFECT;

ANIMALIA; MACACA MULATTA;

ADRENERGIC RECEPTOR STIMULATING AGENT; CATECHOLAMINE; CYTOKINE; MESSENGER RNA; METHAMPHETAMINE; VIRUS ANTIBODY;

ADRENERGIC SYSTEM; ANIMAL; ANIMAL BEHAVIOR; BIOSYNTHESIS; DRUG EFFECTS; GENETICS; IMMUNOLOGY; INNERVATION; LYMPH NODE; MALE; MENTAL STRESS; METABOLISM; NATURAL KILLER CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; SOCIAL BEHAVIOR;

ANIMALS; ANTIBODIES, VIRAL; BEHAVIOR, ANIMAL; CATECHOLAMINES; CYTOKINES; KILLER CELLS, NATURAL; LYMPH NODES; MACACA MULATTA; MALE; METHAMPHETAMINE; RNA, MESSENGER; SIMIAN IMMUNODEFICIENCY VIRUS; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; SYMPATHETIC NERVOUS SYSTEM; SYMPATHOMIMETICS;

EID: 84927723020     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0104     Document Type: Article

References (40)

1. van Schaik CP, Kappeler PM. 1997 Infanticide risk and the evolution of male-female association in primates. Proc. R. Soc. Lond. B 264, 1687-1694. (doi:10.1098/rspb.1997.0234)
2. Di Fiore A, Rendall D. 1994 Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proc. Natl Acad. Sci. USA 91, 9941-9945. (doi:10.1073/pnas.91.21.9941)
3. Frith CD. 2007 The social brain? Phil. Trans. R. Soc. B 362, 671-678. (doi:10.1098/rstb.2006.2003)
4. Stroebe M, Schut H, Stroebe W. 2007 Health outcomes of bereavement. Lancet 370, 1960-1973. (doi:10.1016/S0140-6736(07)61816-9)
5. Cacioppo S, Capitanio JP, Cacioppo JT. 2015 Toward a neurology of loneliness. Psychol Bull. 140, 1464-1504. (doi:10.1037/a0037618)
6. Luo Y, Hawkley LC, Waite LJ, Cacioppo JT. 2012 Loneliness, health, and mortality in old age: a national longitudinal study. Soc. Sci. Med. 74, 907-914. (doi:10.1016/j.socscimed.2011.11.028)
7. Cacioppo JT, Cacioppo S, Cole SW, Capitanio JP, Goossens L, Boomsma DI. 2015 Loneliness across phylogeny and a call for comparative studies and animal models. Perspect. Psychol. Sci. (doi:10.1177/ 1745691614564876)
8. Hennessy MB, Kaiser S, Sachser N. 2009 Social buffering of the stress response: diversity, mechanisms, and functions. Front. Neuroendocrinol. 30, 470-482. (doi:10.1016/j.yfrne.2009.06.001)
9. Cavigelli SA, Caruso MJ. 2015 Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Phil. Trans. R. Soc. B 370, 20140103. (doi:10.1098/rstb.2014.0103)
10. Cacioppo JT, Cacioppo S, Capitanio JP, Cole SW. 2015 The neuroendcrinology of social isolation. Annu. Rev. Psychol. 66, 733-767. (doi:10.1146/annurevpsych-010814-015240)
11. Cole SW. 2008 Social regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity. Brain Behav. Immun. 22, 1049-1055. (doi:10.1016/ j.bbi.2008.02.006)
12. Cole SW, Mendoza SP, Capitanio JP. 2009 Social stress desensitizes lymphocytes to regulation by endogenous glucocorticoids: insights from in vivo cell trafficking dynamics in rhesus macaques. Psychosom. Med. 71, 591-597. (doi:10.1097/PSY. 0b013e3181aa95a9)
13. Cole SW, Hawkley LC, Arevalo JM, Sung CY, Rose RM, Cacioppo JT. 2007 Social regulation of gene expression in human leukocytes. Genome Biol. 8, R189. (doi:10.1186/gb-2007-8-9-r189)
14. Miller GE, Cohen S, Ritchey AK. 2002 Chronic psychological stress and the regulation of proinflammatory cytokines: a glucocorticoid-resistance model. Health Psychol. 21, 531-541. (doi:10.1037/ 0278-6133.21.6.531)
15. Irwin MR, Cole SW. 2011 Reciprocal regulation of the neural and innate immune systems. Nat. Rev. Immunol. 11, 625-632. (doi:10.1038/nri3042)
16. Padro CJ, Sanders VM. 2014 Neuroendocrine regulation of inflammation. Semin. Immunol. pii, S1044-S5323. (doi:10.1016/j.smim.2014.01.003)
17. Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF. 2012 Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Br. Behav. Immun. 26, 1150-1159. (doi:10.1016/j.bbi.2012.07.011)
18. Powell ND et al. 2013 Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via b-adrenergic induction of myelopoiesis. Proc. Natl Acad. Sci. USA 110, 16 574-16 579. (doi:10.1073/pnas.1310655110)
19. Capitanio JP, Mendoza SP, Lerche NW, Mason WA. 1998 Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proc. Natl Acad. Sci. USA 95, 4714-4719. (doi:10.1073/pnas.95.8.4714)
20. Sloan EK, Capitanio JP, Tarara RP, Mendoza SP, Mason WA, Cole SW. 2007 Social stress enhances sympathetic innervation of primate lymph nodes: mechanisms and implications for viral pathogenesis. J. Neurosci. 27, 8857-8865. (doi:10.1523/ JNEUROSCI.1247-07.2007)
21. Collado-Hidalgo A, Sung C, Cole SW. 2006 Adrenergic inhibition of innate antiviral response: PKA blockade of Type I interferon gene transcription mediates catecholamine support for HIV-1 replication. Brain Behav. Immun. 20, 552-563. (doi:10.1016/j.bbi.2006.01.005)
22. Sloan EK, Tarara RP, Capitanio JP, Cole SW. 2006 Enhanced SIV replication adjacent to catecholaminergic varicosities in primate lymph nodes. J. Virol. 80, 4326-4335. (doi:10.1128/JVI. 80.9.4326-4335.2006)
23. Cole SW, Korin YD, Fahey JL, Zack JA. 1998 Norepinephrine accelerates HIV replication via protein kinase A-dependent effects on cytokine production. J. Immunol. 161, 610-616.
24. Antoni MH. 2013 Psychosocial intervention effects on adaptation, disease course and biobehavioral processes in cancer. Br. Behav. Immun. 30, S88-S98. (doi:10.1016/j.bbi.2012.05.009)
25. Capitanio JP, Kyes RC, Fairbanks LA. 2006 Considerations in the selection and conditioning of Old World Monkeys for laboratory research: animals from domestic sources. ILAR J. 47, 294-306. (doi:10.1093/ilar.47.4.294)
26. Capitanio JP, Abel K, Mendoza SP, Blozis SA, McChesney MB, Cole SW, Mason WA. 2008 Personality and serotonin transporter genotype interact with social context to affect immunity and viral set-point in simian immunodeficiency virus disease. Brain Behav. Immun. 22, 676-689. (doi:10.1016/j.bbi.2007.05.006)
27. Pachl C et al. 1995 Rapid and precise quantification of HIV-1 RNA in plasma using a branched DNA signal amplification assay. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 8, 446-454. (doi:10.1097/ 00042560-199504120-00003)
28. Lu X et al. 1998 Targeted lymph-node immunization with whole inactivated simian immunodeficiency virus (SIV) or envelope and core subunit antigen vaccines does not reliably protect rhesus macaques from vaginal challenge with SIVmac251. AIDS 12, 1-10. (doi:10.1097/ 00002030-199801000-00001)
29. Leutenegger CM, Higgins J, Matthews TB, Tarantal AF, Luciw PA, Pedersen NC, North TW. 2011 Realtime TaqMan PCR as a specific and more sensitive alternative to the branched-chain DNA assay for quantitation of simian immunodeficiency virus RNA. AIDS Res. Hum. Retroviruses 17, 243-251. (doi:10. 1089/088922201750063160)
30. Maes M et al. 1998 The effects of psychological stress on humans: increased production of pro inflammatory cytokines and A Th1-like response in stress-induced anxiety. Cytokine 10, 313-318. (doi:10.1006/cyto.1997.0290)
31. Irwin M. 1994 Stress-induced immune suppression: role of brain corticotropin releasing hormone and autonomic nervous system mechanisms. Adv. Neuroimmunol. 4, 29-47. (doi:10.1016/S0960-5428(06)80188-9)
32. Noldus LPJJ. 1991 The Observer: a software system for collection and analysis of observational data. Behav. Res. Methods Instrum. Comput. 23, 415-429. (doi:10.3758/BF03203406)
33. Capitanio JP. 1985 Early experience and social processes in rhesus macaques (Macaca mulatta): II. Complex social interaction. J. Comp. Psychol. 99, 133-144. (doi:10.1037/0735-7036.99.2.133)
34. Altmann J. 1974 Observational study of behavior: sampling methods. Behaviour 49, 227-265. (doi:10.1163/156853974X00534)
35. Abel K, Alegria-Hartman MJ, Rothaeusler K, Marthas M, Miller CJ. 2002 The relationship between simian immunodeficiency virus RNA levels and the mRNA levels of alpha/beta interferons (IFN-a/b) and IFN-a/ b-inducible Mx in lymphoid tissues of rhesus macaques during acute and chronic infection. J. Virol. 76, 8433-8445. (doi:10.1128/JVI.76.16.8433-8445.2002)
36. Abel K et al. 2004 Gamma interferon-mediated inflammation is associated with lack of protection from intravaginal simian immunodeficiency virus SIVmac239 challenge in simian-human immunodeficiency virus 89.6-immunized rhesus macaques. J. Virol. 78, 841-854. (doi:10.1128/JVI. 78.2.841-854.2004)
37. Westermann J, Pabst R. 1990 Lymphocyte subsets in the blood: a diagnostic window on the lymphoid system? Immunol. Today 11, 406-410. (doi:10. 1016/0167-5699(90)90160-B)
38. Madden LJ, Flynn CT, Zandonatti MA, May M, Parsons LH, Katner SN, Henriksen SJ, Fox HS. 2005 Modeling human methamphetamine exposure in nonhuman primates: chronic dosing in the rhesus macaque leads to behavioral and physiological abnormalities. Neuropsychopharmacology 30, 350-359. (doi:10.1038/sj.npp.1300575)
39. Capitanio JP. 2011 Health and social relationships in nonhuman primates: toward a comparative health psychology. In Oxford handbook of health psychology (ed. HS Friedman), pp. 860-883. New York, NY: Oxford University Press.
40. Akinyi MY, Tung J, Jeneby M, Patel NB, Altmann J, Alberts SC. 2013 Role of grooming in reducing tick load in wild baboons (Papio cynocephalus). Anim. Behav. 85, 559-568. (doi:10.1016/j.anbehav. 2012.12.012)