Journal of Reproductive Immunology
Volume 85, Issue 1 , Pages 86-92 , May 2010

Stress in early pregnancy: maternal neuro-endocrine-immune responses and effects

  • Victoria J. Parker
    • ,
  • Alison J. Douglas

      Affiliations

    • Corresponding Author InformationCorresponding author at: Centre for Integrative Physiology, School of Biomedical Sciences, University of Edinburgh, Hugh Robson Building, George Square, Edinburgh, EH8 9XD United Kingdom. Tel.: +44 131 650 3274; fax: +44 131 65 02872.

Received 31 August 2009 ,Revised 5 October 2009 ,Accepted 8 October 2009.

References 

  1. Arck PC, Merali FS, Manuel J, Chaouat G, Clark DA. Stress-triggered abortion: inhibition of protective suppression and promotion of tumor necrosis factor-alpha (TNF-alpha) release as a mechanism triggering resorptions in mice. Am. J. Reprod. Immunol. 1995;33:74–80
  2. Arck P, Hansen PJ, Mulac Jericevic B, Piccinni MP, Szekeres-Bartho J. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am. J. Reprod. Immunol. 2007;58:268–279
  3. Arck PC, Rücke M, Rose M, Szekeres-Bartho J, Douglas AJ, Pritsch M, et al. Early risk factors for miscarriage: a prospective cohort study in pregnant women. Reproduct. Biomed. online. 2008;17(1):101–113
  4. Bao L, Tessier C, Prigent-Tessier A, Li F, Buzzio OL, Callegari EA, et al. Decidual prolactin silences the expression of genes detrimental to pregnancy. Endocrinology. 2007;148:2326–2334
  5. Blois SM, Joachim R, Kandil J, Margni R, Tometten M, Klapp BF, et al. 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. 2004;172:5893–5899
  6. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, et al. A pivotal role for galectin-1 in fetomaternal tolerance. Nat. Med. 2007;13:1450–1457
  7. Brunton PJ, Russell JA, Douglas AJ. Adaptive responses of the maternal HPA axis in pregnancy and lactation. J. Neuroendocrinol. 2008;20:764–776
  8. Chrousos GP, Torpy DJ, Gold PW. Interactions between the hypothalamic–pituitary–adrenal axis and the female reproductive system: clinical implications. Ann. Intern. Med. 1998;129:229–240
  9. Druckmann R, Druckmann M-A. Progesterone and the immunology of pregnancy. J. Steroid Biochem. Mol. Biol. 2005;97:389–396
  10. Erlebacher A, Zhang D, Parlow AF, Glimcher LH. Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system. J. Clin. Invest. 2004;114(1):39–48
  11. Freeman ME, Kanyicska B, Lerant A, Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol Rev. 2000;80:1523–1631
  12. Gagnon A, Wilson RD, Audibert F, Allen VM, Blight C, Brock JA, et al. Obstetrical complications associated with abnormal maternal serum markers analytes. J. Obstet. Gynaecol. Can. 2008;30(10):918–949
  13. Gala RR. The physiology and mechanisms of the stress-induced changes in prolactin secretion in the rat. Life Sci. 1990;46:1407–1420
  14. Grattan DR, Steyn FJ, Kokay IC, Anderson GM, Bunn SJ. Pregnancy-induced adaptation in the neuroendocrine control of prolactin secretion. J. Neuroendocrinol. 2008;20:497–507
  15. Guerin LR, Prins JR, Robertson SA. Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment?. Hum. Reprod. Update. 2009;15(5):517–535
  16. Guzmán C, Cabrera R, Cárdenas M, Larrea F, Nathanielsz PW, Zambrano E. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J. Physiol. 2006;572:97–108
  17. Henderson TA, Saunders PTK, Moffett-King A, Groome NP, Critchley HOD. Steroid receptor expression in uterine natural killer cells. J. Clin. Endocrinol. Metab. 2003;88:40–449
  18. Holmes MC, Seckl JR. The role of 11beta-hydroxysteroid dehydrogenases in the brain. Mol. Cell Endocrinol. 2006;248(1–2):9–14
  19. Jabbour HN, Critchley HO. Potential roles of decidual prolactin in early pregnancy. Reproduction. 2001;121:197–205
  20. Joachim R, Zenclussen AC, Polgar B, Douglas AJ, Fest S, Knackstedt M, et al. The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune response. Steroids. 2003;68:931–940
  21. Jones RL, Critchley HO, Brooks J, Jabbour HN, McNeilly AS. Localization and temporal expression of prolactin receptor in human endometrium. J. Clin. Endocrinol. Metab. 1998;83:258–262
  22. Matalka KZ, Ali DA. Stress-induced versus preovulatory and pregnancy hormonal levels in modulating cytokine production following whole blood stimulation. Neuroimmunomodulation. 2005;12:366–374
  23. Matsuwaki T, Watanabe E, Suzuki M, Yamanouchi K, Nishihara M. Glucocorticoid maintains pulsatile accretion of luteinizing hormone under infectious stress condition. Endocrinology. 2003;144:3477–3482
  24. Nakamura H, Nagase H, Ogino K, Hatta K, Matsuzaki I. Involvement of central, but not placental corticotropin releasing hormone (CRH) in heat stress induced immunosuppression during pregnancy. Brain Behav. Immun. 2001;15:43–53
  25. Nakamura H, Kimura T, Ogita K, Nakamura T, Takemura M, Shimoya K, et al. NF-kappaB activation at implantation window of the mouse uterus. Am. J. Reprod. Immunol. 2004;51(1):16–21
  26. Nakamura H, Seto T, Nagase H, Yoshida M, Dan S, Ogino K. Inhibitory effect of pregnancy on stress-induced immunosuppression through corticotropin releasing hormone (CRH) and dopaminergic systems. J. Neuroimmunol. 1997;75(1–2):1–8
  27. Nakamura K, Sheps S, Arck PC. Stress and reproductive failure: past notions, present insights and future directions. J. Assist. Reprod. Genet. 2008;25:47–62
  28. Nepomnaschy PA, Welch K, McConnell D, Strassmann BI, England BG. 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. 2004;16:523–532
  29. Nepomnaschy PA, Welch KB, McConnell DS, Low BS, Strassmann BI, England BG. Cortisol levels and very early pregnancy loss in humans. Proc. Natl. Acad. Sci. U.S.A. 2006;103:3938–3942
  30. Neumann ID, Johnstone HA, Hatzinger M, Liebsch G, Shipston M, Russell JA, et al. Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J. Physiol. 1998;508:289–300
  31. Nierop A, Bratsikas A, Klinkenberg A, Nater UM, Zimmerman R, Ehlert U. Prolonged salivary cortisol recovery in second trimester pregnant women and attenuated salivary a-amylase responses to psychosocial stress in human pregnancy. J. Clin. Endo. Metab. 2008;91:1329–1335
  32. Obel C, Hedegaard M, Henriksen TB, Secher NJ, Olsen J, Levine S. Stress and salivary cortisol during pregnancy. Psychoneuroendocrinology. 2005;30:647–656
  33. Perks CM, Newcomb PV, Grohmann M, Wright RJ, Mason HD, Holly JM. Prolactin acts as a potent survival factor against C2-ceramide-induced apoptosis in human granulosa cells. Hum. Reprod. 2003;18:2672–2677
  34. Pincus, M., Keil, T., Rücke, M., Bruenahl, C., Magdorf, K., Klapp, B.F., Douglas, A.J., Paus, R., Wahn, U., Arck, P., in press. Low levels of progesterone during early pregnancy predict increased risk for atopic dermatitis in female children in later life. J. All. Clin. Immunol.
  35. Raghupathy R, Makhseed M, Azizieh F, Omu A, Gupta M, Farhat R. Cytokine production by maternal lymphocytes during normal human pregnancy and in unexplained recurrent spontaneous abortion. Hum. Reprod. 2000;15:713–718
  36. Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic–pituitary–gonadal axis: peripheral and central mechanisms. Biol. Reprod. 1991;45:523–532
  37. Seckl JR, Meaney MJ. Glucocorticoid programming. Ann. N.Y. Acad. Sci. 2004;1032:63–84
  38. Stefanski V, Raabe C, Schulte M. Pregnancy and social stress in female rats: influences on blood leukocytes and corticosterone concentrations. J. Neuroimmunol. 2005;162:81–88
  39. Suda T, Chida K, Matsuda H, Hashizume H, Ide K, Yokomura K, et al. High-dose intravenous glucocorticoid therapy abrogates circulating dendritic cells. J. Allergy Clin. Immunol. 2003;112(6):1237–1239
  40. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L. Progesterone as an immunomodulatory molecule. Int. Immunopharmacol. 2001;1:1037–1048
  41. Szekeres-Bartho J, Wegmann TG. A progesterone-dependent immunomodulatory protein alters the Th1/Th2 balance. J. Reprod. Immunol. 1996;31:81–95
  42. Szekeres-Bartho J, Par G, Dombay G, Smart YC, Volgyi Z. The antiabortive effect of progesterone-induced blocking factor in mice is manifested by modulating NK activity. Cell Immunol. 1997;177:194–199
  43. Van den Heuvel M, McNey BA, Hahnel AC, Croy BA. An analysis of the uterine lymphocyte-derived hybridoma cell line GWM 1-2 expression of receptors for estrogen, progesterone and interleukin 2. J. Reprod. Immunol. 1996;31:37–50
  44. Wadhwa PD. Psychoneuroendocrine processes in human pregnancy influence fetal development and heath. Psychoneuroendocrinology. 2005;8:724–743

PII: S0165-0378(09)00552-X

doi: 10.1016/j.jri.2009.10.011

Journal of Reproductive Immunology
Volume 85, Issue 1 , Pages 86-92 , May 2010

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