Stress, immune function, and women's reproduction

Annals of the New York Academy of Sciences

Volumn 1113, Issue , 2007, Pages 350-364

  Nepomnaschy, Pablo A ^a,e   Sheiner, Eyal ^b   Mastorakos, George ^c   Arck, Petra C ^d  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c UNIVERSITY OF ATHENS   (Greece)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e MD A3 05 ^*  (United States)

Author keywords

Evolution; Immune function; Reproductive function; Stress

Indexed keywords

CORTICOTROPIN RELEASING FACTOR;

BIRTH; BLOOD LEVEL; CENTRAL NERVOUS SYSTEM; CLINICAL RESEARCH; CONFERENCE PAPER; FEMALE FERTILITY; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE SYSTEM; LIFESPAN; MATERNAL STRESS; METABOLIC STRESS; PREGNANT WOMAN; PUERPERIUM; REPRODUCTIVE HEALTH;

EID: 35548984471     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1196/annals.1391.028     Document Type: Conference Paper

References (79)

1. BAIRD, D. & B. STRASSMANN. 2000. Women's fecundability and factors affecting it [invited review]. In Women and Health. MB Goldman, H.M., Ed.: 126-137 Academic Press. San Diego, CA.
2. ARENA, B. et al. 1995. Reproductive hormones and menstrual changes with exercise in female athletes. Sports Med. 19: 278-287.
3. NEPOMNASCHY, P.A. et al. 2006. Cortisol levels and very early pregnancy loss in humans. Proc. Natl. Acad. Sci. USA 103: 3938-3942.
4. LAATIKAINEN, T.J. 1991. Corticotropin-releasing hormone and opioid peptides in reproduction and stress. Ann. Med. 23: 489-496.
5. WASSER, S.K. & D.P. BARASH. 1983. Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q. Rev. Biol. 58: 513-538.
6. SAPOLSKY, R.M., L.M. ROMERO & A.U. MUNCK. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21: 55-89.
7. TILBROOK, A.J., A.I. TURNER & I.J. CLARKE. 2000. Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev. Reprod. 5: 105-113.
8. NEPOMNASCHY, P.A. et al. 2004. Stress and female reproductive function: a study of daily variations in cortisol, gonadotrophins, and gonadal steroids in a rural Mayan population. Am. J. Hum. Biol. 16: 523-532.
9. ARCK, P.C. et al. 2001. Stress and immune mediators in miscarriage. Hum. Reprod. 16: 1505-1511.
10. BARZILAI-PESACH, V. et al. 2006. The effect of women's occupational psychologic stress on outcome of fertility treatments. J. Occup. Environ. Med. 48: 56-62.
11. HJOLLUND, N.H. et al. 1998. Job strain and time to pregnancy. Scand. J. Work Environ. Health 24: 344-350.
12. VARTIAINEN, H. et al. 1994. Psychosocial factors, female fertility and pregnancy: a prospective study - Part I: Fertility. J. Psychosom. Obstet. Gynaecol. 15: 67-75.
13. BONEN, A. 1994. Exercise-induced menstrual cycle changes. A functional, temporary adaptation to metabolic stress. Sports Med. 17: 373-392.
14. SCHENKER, M.B. et al. 1997. Self-reported stress and reproductive health of female lawyers. J. Occup. Environ. Med. 39: 556-568.
15. NEPOMNASCHY, P.A. 2005. Stress and Female Reproduction in a Rural Mayan Population, The University of Michigan. Ann Arbor, MI.
16. PIKE, I.L. & S.R. WILLIAMS. 2006. Incorporating psychosocial health into biocultural models: preliminary findings from Turkana women of Kenya. Am. J. Hum. Biol. 18: 729-740.
17. BAIRD, D.D. et al. 1999. Preimplantation urinary hormone profiles and the probability of conception in healthy women. Fertil. Steril. 71: 40-49.
18. FERIN, M. 1999. Clinical review 105: Stress and the reproductive cycle. J. Clin. Endocrinol. Metab. 84: 1768-1774.
19. FLESHNER, M. & M.L. LAUDENSLAGER. 2004. Psychoneuroimmunology: then and now. Behav. Cogn. Neurosci. Rev. 3: 114-130.
20. MCEWEN, B.S. 2004. Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann. N.Y. Acad. Sci. 1032: 1-7.
21. STEINMAN, L. 2004. Elaborate interactions between the immune and nervous systems. Nat. Immunol. 5: 575-581.
22. WEIGENT, D.A. & J.E. BLALOCK. 1987. Interactions between the neuroendocrine and immune systems: common hormones and receptors. Immunol. Rev. 100: 79-108.
23. BENSCHOP, R.J., M. RODRIGUEZ-FEUERHAHN & M. SCHEDLOWSKI. 1996. Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav. Immun. 10: 77-91.
24. WEBSTER, J.I., L. TONELLI & E.M. STERNBERG. 2002. Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 20: 125-163.
25. CHROUSOS, G.P. 1992. Regulation and dysregulation of the hypothalamic-pituitary-adrenal axis. The corticotropin-releasing hormone perspective. Endocrinol. Metab. Clin. North Am. 21: 833-858.
26. MASTORAKOS, G., M.G. PAVLATOU & M. MIZAMTSIDI. 2006. The hypothalamic-pituitary-adrenal and the hypothalamic- pituitary-gonadal axes interplay. Pediatr. Endocrinol. Rev. 3(Suppl 1): 172-181.
27. HABIB, K.E., P.W. GOLD & G.P. CHROUSOS. 2001. Neuroendocrinology of stress. Endocrinol. Metab. Clin. North Am. 30: 695-728; vii-viii.
28. RIVIER, C. & S. RIVEST. 1991. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol. Reprod. 45: 523-532.
29. MAGIAKOU, M.A. et al. 1997. The hypothalamic-pituitary- adrenal axis and the female reproductive system. Ann. N.Y. Acad. Sci. 816: 42-56.
30. TSIGOS, C. & G.P. CHROUSOS. 1994. Physiology of the hypothalamic-pituitary-adrenal axis in health and dysregulation in psychiatric and autoimmune disorders. Endocrinol. Metab. Clin. North Am. 23: 451-466.
31. EVANS, J.J. 1999. Modulation of gonadotropin levels by peptides acting at the anterior pituitary gland. Endocr. Rev. 20: 46-67.
32. CHROUSOS, G.P., D.J. TORPY & P.W. GOLD. 1998. Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann. Intern. Med. 129: 229-240.
33. FINKELSTEIN, M. & J.M. SHAEFER. 1979. Inborn errors of steroid biosynthesis. Physiol. Rev. 59: 353-406.
34. MASTORAKOS, G. et al. 1993. Immunoreactive corticotropin-releasing hormone and its binding sites in the rat ovary. J. Clin. Invest. 92: 961-968.
35. GHIZZONI, L. et al. 1997. Corticotropin-releasing hormone (CRH) inhibits steroid biosynthesis by cultured human granulosa-lutein cells in a CRH and interleukin-1 receptor-mediated fashion. Endocrinology 138: 4806-4811.
36. MASTORAKOS, G. et al. 1996. Presence of immunoreactive corticotropin-releasing hormone in human endometrium. J. Clin. Endocrinol. Metab. 81: 1046-1050.
37. GOLAND, R.S. et al. 1988. Biologically active corticotropin-releasing hormone in maternal and fetal plasma during pregnancy. Am. J. Obstet. Gynecol. 159: 884-890.
38. ORTH, D.N. & C.D. MOUNT. 1987. Specific high-affinity binding protein for human corticotropin-releasing hormone in normal human plasma. Biochem. Biophys. Res. Commun. 143: 411-417.
39. LAATIKAINEN, T. et al. 1987. Immunoreactive corticotropin-releasing factor and corticotropin during pregnancy, labor and puerperium. Neuropeptides 10: 343-353.
40. MAGIAKOU, M.A. et al. 1996. The maternal hypothalamic-pituitary-adrenal axis in the third trimester of human pregnancy. Clin. Endocrinol. (Oxf.) 44: 419-428.
41. WINTOUR, E.M. et al. 1986. Effect of long-term infusion of ovine corticotrophin-releasing factor in the immature ovine fetus. J. Endocrinol. 111: 469-475.
42. MCLEAN, M. et al. 1995. A placental clock controlling the length of human pregnancy. Nat. Med. 1: 460-463.
43. FLORES, D.L. & V.C. HENDRICK. 2002. Etiology and treatment of postpartum depression. Curr. Psychiatry Rep. 4: 461-466.
44. VAMVAKOPOULOS, N.C. & G.P. CHROUSOS. 1993. Structural organization of the 5′ flanking region of the human corticotropin releasing hormone gene. DNA Seq. 4: 197-206.
45. GREGOIRE, A.J. et al. 1996. Transdermal oestrogen for treatment of severe postnatal depression. Lancet 347: 930-933.
46. NORWITZ, E.R., D.J. SCHUST & S.J. FISHER. 2001. Implantation and the survival of early pregnancy. N. Engl. J. Med. 345: 1400-1408.
47. LIN, H. et al. 1993. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J. Immunol. 151: 4562-4573.
48. PICCINNI, M.P. et al. 1998. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med. 4: 1020-1024.
49. MUNN, D.H. et al. 1998. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 1191-1193.
50. TERNESS, P. et al. 2002. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J. Exp. Med. 196: 447-457.
51. SASAKI, Y. et al. 2004. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 10: 347-353.
52. ALUVIHARE, V.R., M. KALLIKOURDIS & A.G. BETZ. 2004. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5: 266-271.
53. GULERIA, I. et al. 2005. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 202: 231-237.
54. ZHU, X.Y. et al. 2005. Blockade of CD86 signaling facilitates a Th2 bias at the maternal-fetal interface and expands peripheral CD4+CD25+ regulatory T cells to rescue abortion-prone fetuses. Biol. Reprod. 72: 338-345.
55. POEHLMANN, T.G. et al. 2005. The possible role of the Jak/STAT pathway in lymphocytes at the fetomaternal interface. Chem. Immunol. Allergy 89: 26-35.
56. AYATOLLAHI, M., B. GERAMIZADEH & A. SAMSAMI. 2005. Transforming growth factor beta-1 influence on fetal allografts during pregnancy. Transplant Proc. 37: 4603-4604.
57. BLOIS, S. et al. 2005. Intercellular adhesion molecule-1/LFA-1 cross talk is a proximate mediator capable of disrupting immune integration and tolerance mechanism at the feto-maternal interface in murine pregnancies. J. Immunol. 174: 1820-1829.
58. CLARK, D.A., D. BANWATT & G. CHAOUAT. 1993. Stress-triggered abortion in mice prevented by alloimmunization. Am. J. Reprod. Immunol. 29: 141-147.
59. WONNACOTT, K.M. & R.H. BONNEAU. 2002. The effects of stress on memory cytotoxic T lymphocyte-mediated protection against herpes simplex virus infection at mucosal sites. Brain Behav. Immun. 16: 104-117.
60. ELENKOV, I.J. et al. 1999. Stress, corticotropin- releasing hormone, glucocorticoids, and the immune/inflammatory response: acute and chronic effects. Ann. N.Y. Acad. Sci. 876: 1-11; discussion 11-3.
61. VITORATOS, N. et al. 2006. Association between serum tumor necrosis factor-alpha and corticotropin-releasing hormone levels in women with preterm labor. J. Obstet. Gynaecol. Res. 32: 497-501.
62. DAHLSTROM, A. et al. 1965. Observations on adrenergic innervation of dog heart. Am. J. Physiol. 209: 689-692.
63. CACIOPPO, J.T. et al. 1998. Autonomic, neuroendocrine, and immune responses to psychological stress: the reactivity hypothesis. Ann. N.Y. Acad. Sci. 840: 664-673.
64. DHABHAR, F.S. 2000. Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann. N.Y. Acad. Sci. 917: 876-893.
65. SANDERS, V.M. et al. 1997. Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J. Immunol. 158: 4200-4210.
66. ALOE, L., E. ALLEVA & M. FIORE. 2002. Stress and nerve growth factor: findings in animal models and humans. Pharmacol. Biochem. Behav. 73: 159-166.
67. LEVI-MONTALCINI, R. et al. 1996. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci. 19: 514-520.
68. TOMETTEN, M. et al. 2006. Nerve growth factor translates stress response and subsequent murine abortion via adhesion molecule-dependent pathways. Biol. Reprod. 74: 674-683.
69. BLOIS, S.M. et al. 2004. Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J. Immunol. 172: 5893-5899.
70. JOACHIM, R. et al. 2003. The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune response. Steroids 68: 931-940.
71. CREEL, S. et al. 2007. Predation risk affects reproductive physiology and demography of elk. Science 315: 960.
72. XIAO, E., L. XIA-ZHANG & M. FERIN. 2000. Inhibitory effects of endotoxin on LH secretion in the ovariectomized monkey are prevented by naloxone but not by an interleukin-1 receptor antagonist. Neuroimmunomodulation 7: 6-15.
73. XIAO, E., L. XIA-ZHANG & M. FERIN. 2002. Inadequate luteal function is the initial clinical cyclic defect in a 12-day stress model that includes a psychogenic component in the Rhesus monkey. J. Clin. Endocrinol. Metab. 87: 2232-2237.
74. GARDNER, L. & A. MOFFETT. 2003. Dendritic cells in the human decidua. Biol. Reprod. 69: 1438-1446.
75. KAMMERER, U. et al. 2000. Human decidua contains potent immunostimulatory CD83(+) dendritic cells. Am. J. Pathol. 157: 159-169.
76. SPONG, C.Y. et al. 1999. Regulation of postimplantation mouse embryonic growth by maternal vasoactive intestinal peptide. Ann. N.Y. Acad. Sci. 897: 101-108.
77. SHEN, G.M. et al. 2006. Role of vasoactive intestinal peptide and nitric oxide in the modulation of electroacupuncture on gastric motility in stressed rats. World J. Gastroenterol. 12: 6156-6160.
78. CHORNY, A., E. GONZALEZ-REY & M. DELGADO. 2006. Regulation of dendritic cell differentiation by vasoactive intestinal peptide: therapeutic applications on autoimmunity and transplantation. Ann. N.Y. Acad. Sci. 1088: 187-194.
79. BLOIS, S.M. et al. 2004. Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biol. Reprod. 70: 1018-1023.