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Stress, Peer Affiliation, and Transforming Growth Factor-β1 in Differentially Reared Primates

Published online by Cambridge University Press:  07 November 2014

Eric L.P. Smith,
Olcay A. Batuman,
Jeremy D. Coplan and
Leonard A. Rosenblum
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Abstract

A bidirectional regulatory interaction between the central nervous system and the immune system is largely provided by cytokines and their specific receptors, which are expressed by cells of both systems. Transforming growth factor-β1 (TGF-β1), produced by glial cells and lymphocytes and regulated by steroid hormones, is one such cytokine. In the current study, we examined the relationship between TGF-β1 and peer affiliation in bonnet macaques (Macaca radiata) either reared normally or exposed as infants to conditions in which their mothers faced fluctuating requirements for food procurement (variable foraging demand [VFD]). Rearing under VFD conditions has been previously shown to produce dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis in these animals. Serum levels of TGF-β1 after exposure to a moderate stressor had no correlation with peer affiliation under baseline conditions (r=.07), but were highly correlated with affiliation after subsequent challenge with a fear stimulus (r=.62). Affiliation after the fear stimulus also was inversely correlated with baseline levels of affiliation (r=−.71). These data suggest that changes in peripheral TGF-β1 may be reflective of latent behavioral and biochemical propensities possibly related to affect. Further examination of the effects of early adversity will improve our understanding of the relationship between the HPA axis and immune function.

Information

Type
Original Research
Information
CNS Spectrums , Volume 6 , Issue 7: Novel Perspectives of Central CRF/HPA Axis Dysfunction , July 2001, pp. 573 - 578
Copyright
Copyright © Cambridge University Press 2001

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References

REFERENCES

1. Dunn, AJ. Interactions between the nervous system and the immune system: implications for psychopharmacology. In: Bloom, FE, Kupfer, DJ, eds. Psychopharmacology: The Fourth Generation of Progress. New York, NY: Raven Press; 1995:719–731.Google Scholar
2. Elenkov, IJ, Wilder, RL, Chrousos, GP, Vizi, ES. The sympathetic nervean integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev. 2000;52:595–638.Google ScholarPubMed
3. Sternberg, EM. Interactions between the immune and neuroendocrine systems. Prog Brain Res. 2000;122:35–42.CrossRefGoogle ScholarPubMed
4. Chrousos, GP. Stress, chronic inflammation, and emotional and physical well-being: concurrent effects and chronic sequelae. J Allergy Clin Immunol. 2000;106(Suppl):S275–S291.CrossRefGoogle ScholarPubMed
5. Lubach, GR, Coe, CL, Ershler, WB. Effects of early rearing environment on immune responses of infant rhesus monkeys. Brain Behav Immun. 1995;9:31–46.CrossRefGoogle ScholarPubMed
6. Glaser, R, Kiecolt-Glaser, JK, Bonneau, R, et al. Stress-induced modulation of the immune response to recombinant hepatitis B vaccine. Psychosom Med. 1992;54:22–29.CrossRefGoogle ScholarPubMed
7. Perez, L, Lysle, DT. Corticotropin-releasing hormone is involved in conditioned stimulus-induced reduction of natural killer cell activity but not in conditioned alterations in cytokine production or proliferation responses. J Neuroimmunol. 1995;63:1–8.CrossRefGoogle ScholarPubMed
8. Chrousos, GP. The stress response and immune function: clinical implications. The 1999 Novera H. Spector Lecture. Ann N Y Acad Sci. 2000;917:38–67.Google Scholar
9. Maier, SF, Watkins, LR. Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychol Rev. 1998;105:83–107.CrossRefGoogle ScholarPubMed
10. De Bosscher, K, Vanden Berghe, W, Haegeman, G. Mechanisms of antiinflammatory action and oi immunosuppression by glucocorticoids: negative interference of activated glucocorticoid receptor with transcription factors. J Neuroimmunol. 2000;109:16–22.CrossRefGoogle Scholar
11.Gaillard, RC. Interaction between the hypothalamo-pituitary-adrenal axis and the immunological system. Ann Endocrinol (Paris). 2001;62:155–163.Google ScholarPubMed
12. Abe, K, Saito, H. Effects of basic fibroblast growth factor on central nervous system functions. Pharmacol Res. 2001;43:307–312.CrossRefGoogle ScholarPubMed
13. Freidin, MM. Antibody to the extracellular domain of the low affinity NGF receptor stimulates p75(NGFR)-mediated apoptosis in cultured sympathetic neurons. J Neurosci Res. 2001;64:331–340.CrossRefGoogle Scholar
14. Steinberg, EM. Neural-immune interactions in health and disease. J Clin Invest. 1997;100:2641–2647.CrossRefGoogle Scholar
15. Turnbull, AV, Rivier, CL. Regulation of the hypothalamic-pituitaryadrenal axis by cytokines: actions and mechanisms of action. Physiol Rev. 1999;79:1–71.CrossRefGoogle Scholar
16. Esposito, P, Gheorghe, D, Kandere, K, et al. Acute stress increases permeability of the blood-brain-barrier through activation of brain mast cells. Brain Res. 2001;888:117–127.Google Scholar
17. Gaykema, RPA, Goehler, LE, Hansen, MK, Maier, SF, Watkins, LR. Subdiaphragmatic vagotomy blocks interleukin-1β-induced fever but does not reduce IL-1β levels in the circulation. Auton Neurosci. 2000;85:72–77.CrossRefGoogle Scholar
18. Brand, C, Cherradi, N, Defaye, G, et al. Transforming growth factor β1 decreases cholesterol supply to mitochondria via repression of steroidogenic acute regulatory protein expression. J Biol Chem. 1998;273:6410–6416.CrossRefGoogle ScholarPubMed
19. Blobe, GC, Schiemann, WP, Lodish, HF. Role of transforming growth factor β in human disease. N Engl J Med. 2000;342:1350–1358.CrossRefGoogle ScholarPubMed
20. Raber, J, Koob, GF, Bloom, FE. Interferon-α and transforming growth factor-β1 regulate corticotropin-releasing factor release from the amygdala: comparison with the hypothalamic response. Neurochem Int. 1997;30:455–463.CrossRefGoogle Scholar
21.Munger, JS, Harpel, JG, Gleizes, PE, et al. Latent transforming growth factor-β: structural features and mechanisms of activation. Kidney Int. 1997;51:1376–1382.CrossRefGoogle ScholarPubMed
22. Roberts, AB, Sporn, MB. The transforming growth factor-βs. In: Sporn, MB, Roberts, AB, eds. Peptide Growth Factors and Their Receptors. Berlin, Germany: Springer-Verlag; 1990:419–472.CrossRefGoogle ScholarPubMed
23. Knuckey, NW, Finch, P, Palm, DE, et al. Differential neuronal and astrocytie expression of transforming growth factor beta isoforms in rat hippocampus following transient forebrain ischemia. Brain Res Mol Brain Res. 1996;40:1–14.Google ScholarPubMed
24. Plata-Salamán, CR, Ilyin, SE. Interleukin-1β (IL-1β)-induced modulation of the hypothalamic IL-1β system, tumor necrosis factor-α, and transforming growth factor-β1 mRNAs in obese (fa/fa) and lean (Fa/Fa) Zucker rats: implications to IL-1β feedback systems and eytokine-eytokine interactions. J Neurosci Res. 1997;49:541–550.3.0.CO;2-B>CrossRefGoogle Scholar
25. Ho, MM, Vinson, GP. Peptide growth factors and the adrenal cortex. Microsc Res Tech. 1997;36:558–568.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
26.Unsicker, K, Flanders, KC, Cissel, DS, Lafyatis, RJ, Sporn, MB. Transforming growth factor beta isoforms in the adult rat central and peripheral nervous system. Neuroscience. 1991;44:613–625.CrossRefGoogle ScholarPubMed
27. AyanlarBatuman, O, Ferrero, AP, Diaz, A, Berger, B, Pomerantz, RJ. Regulation of transforming growth factor-β1 gene expression by glucocorticoids in normal human T lymphocytes. J Clin Invest. 1991;88:1574–1580.CrossRefGoogle Scholar
28. Smith, ELP, Batuman, OA, Coplan, JD, et al. Transforming growth factor-β1 and cortisol in differentially reared primates. Brain Behav and Immun. In press.Google Scholar
29. Andrews, MW, Rosenblum, LA. Relationship between foraging and affiliative social referencing in primates. In: Fa, JE, Southwick, CH, eds. Ecology and Behavior of Food-enhanced Primate Groups. New York, NY: Alan Liss; 1988:247–268.Google Scholar
30. Andrews, MW, Rosenblum, LA. Attachment in monkey infants raised in variable- and low-demand environments. Child Dev. 1991;62:686–693.CrossRefGoogle ScholarPubMed
31. Andrews, MW, Rosenblum, LA. Assessment of attachment in differentially reared infant monkeys (Macaca radiata): response to separation and a novel environment. J Comp Psychol. 1993;107:84–90.CrossRefGoogle Scholar
32. Coplan, JD, Trost, RC, Owens, MJ, et al. Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Arch Gen Psychiatry. 1998;55:473–477.CrossRefGoogle ScholarPubMed
33. Coplan, JD, Andrews, MW, Rosenblum, LA, et al. Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc Natl Acad Sci U S A. 1996;93:1619–1623.CrossRefGoogle ScholarPubMed
34. Coplan, JD, Smith, ELP, Scharf, BA, et al. Variable foraging demand rearing in primates: biobehavioral sequelae. Paper presented at the annual meeting of the American Psychiatric Association, New Orleans, May 2001.Google Scholar
35. Sharpies, K, Plowman, GD, Rose, TM, Twardzik, DR, Purchio, AF. Cloning and sequence analysis of simian transforming growth factor-β cDNA. DNA. 1987;6:239–244.CrossRefGoogle Scholar
36. Rosenblum, LA, Forger, C, Noland, S, Trost, RC, Coplan, JD. Response of adolescent bonnet macaques to an acute fear stimulus as a function of early rearing conditions. Dev Psychobiol. In press.Google Scholar
37. Kelleher, RT, Morse, WH. Determinants of the specificity of behavioral effects of drugs. Ergeb Physiol. 1968;60:1–56.Google ScholarPubMed
38. Howell, LL, Byrd, LD, Marr, MJ. Similarities in the rate-altering effects of white noise and cocaine. J Exp Anal Behav. 1986;46:381–394.CrossRefGoogle ScholarPubMed
39. Francis, D, Diorio, J, Liu, D, Meaney, MJ. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science. 1999;286:1155–1158.CrossRefGoogle ScholarPubMed
40. Francis, DD, Caldji, C, Champagne, F, Plotsky, PM, Meaney, MJ. The role of corticotropin-releasing factor—norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biol Psychiatry. 1999;46:1153–1166.CrossRefGoogle ScholarPubMed
41. Higley, JD, Mehlman, PT, Poland, RE, et al. CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol Psychiatry. 1996;40:1067–1082.CrossRefGoogle ScholarPubMed
42. Westergaard, GC, Suomi, SJ, Higley, JD, Mehlman, PT. CSF 5-HIAA and aggression in female macaque monkeys: species and interindividual differences. Psychopharmacology (Berl). 1999;146:440–446.CrossRefGoogle ScholarPubMed
43. Suomi, SJ. Early stress and adult emotional reactivity in rhesus monkeys. Ciba Found Symp. 1991;156:171–183.Google ScholarPubMed