Inhibition of Follicular Development Induced by Chronic Unpredictable Stress Is Associated with Growth and Differentiation Factor 9 and Gonadotropin in Mice

Biology of Reproduction

Volumn 86, Issue 4, 2012, Pages

  Wu, Li Min ^a   Liu, Yu Sheng ^a   Tong, Xian Hong ^a   Shen, Ni ^a   Jin, Ren Tao ^a   Han, Hui ^b   Hu, Mei Hong ^a   Wang, Wei ^a   Zhou, Gui Xiang ^a  

^a ANHUI PROVINCIAL HOSPITAL   (China)

^b ANHUI UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Chronic unpredictable stress; Follicular development; Growth and differentiation factor 9 (GDF9); Psychosocial stress

Indexed keywords

GONADOTROPIN; GROWTH DIFFERENTIATION FACTOR 9; MESSENGER RNA; GDF9 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; FEMALE; HORMONE ACTION; MENTAL STRESS; MOUSE; NONHUMAN; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; WESTERN BLOTTING; ANIMAL; DRUG EFFECT; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; OVARY FOLLICLE; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MUS;

ANIMALS; FEMALE; FOLLICULAR ATRESIA; GENE EXPRESSION; GENE EXPRESSION PROFILING; GONADOTROPINS; GROWTH DIFFERENTIATION FACTOR 9; MICE; OVARIAN FOLLICLE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS, PSYCHOLOGICAL;

EID: 84864019193     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.093468     Document Type: Article

References (46)

1. Zangeneh FZ, Shooshtary FS. Chronic stress and limbic-hypothalamopituitary-adrenal axis (LHPA) response in female reproductive system. J Fam Reprod Health 2009; 3:101-108.
2. Rivier C, Rivest S. Effect of stress on the activity of the hypothalamicpituitary-gonadal axis: peripheral and central mechanisms. Biol Reprod 1991; 45:523-532.
3. Moberg GP. How behavioral stress disrupts the endocrine control of reproduction in domestic animals. J Dairy Sci 1991; 74:304-311.
4. Schenker JG, Meirow D, Schenker E. Stress and human reproduction. Eur J Obstet Gynecol Reprod Biol 1992; 45:1-8.
5. 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.
6. Berga SL, Mortola JF, Girton L, Suh B, Laughlin G, Pham P, Yen SSC. Neuroendocrine aberrations in women with functional hypothalamic amenorrhea. J Clin Endocrin Metab 1989; 68:301-308.
7. Dorfman M, Arancibia S, Fiedler JL, Lara HE. Chronic intermittent cold stress activates ovarian sympathetic nerves and modifies ovarian follicular development in the rat. Biol Reprod 2003; 68:2038-2043.
8. Xiao E, Xia-Zhang L, Ferin M. 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 Endocrin Metab 2002; 87: 2232-2237.
9. Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 2002; 53:865-871.
10. Gore AC, Attardi B, DeFranco DB. Glucocorticoid repression of the reproductive axis: effects on GnRH and gonadotropin subunit mRNA levels. Mol Cell Endocrinol 2006; 256:40-48.
11. Kamel F, Kubajak CL. Modulation of gonadotropin secretion by corticosterone: interaction with gonadal steroids and mechanism of action. Endocrinology 1987; 121:561-568.
12. Breen KM, Oakley AE, Pytiak AV, Tilbrook AJ, Wagenmaker ER, Karsch FJ. Does cortisol acting via the type II glucocorticoid receptor mediate suppression of pulsatile luteinizing hormone secretion in response to psychosocial stress? Endocrinology 2007; 148:1882-1890.
13. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 2002; 296:2178-2180.
14. Knight PG, Glister C. TGF-fbetag superfamily members and ovarian follicle development. Reproduction 2006; 132:191-206.
15. Su YQ, Wu X, O'Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol 2004; 276:64-73.
16. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 2001; 15:854-866.
17. Kovanci E, Rohozinski J, Simpson JL, Heard MJ, Bishop CE, Carson SA. Growth differentiating factor-9 mutations may be associated with premature ovarian failure. Fert Steril 2007; 87:143-146.
18. Bromberger JT, Matthews KA, Kuller LH, Wing RR, Meilahn EN, Plantinga P. Prospective study of the determinants of age at menopause. Am J Epidemiol 1997; 145:124-133.
19. De Vry J, Schreiber R. The chronic mild stress depression model: future developments from a drug discovery perspective. Psychopharmacology 1997; 134:349-350.
20. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology 1997; 134:319-329.
21. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 1987; 93:358-364.
22. Wu LM, Han H, Wang QN, Hou HL, Tong H, Yan XB, Zhou JN. Mifepristone repairs region-dependent alteration of synapsin I in hippocampus in rat model of depression. Neuropsychopharmacol 2007; 32:2500-2510.
23. Vitt UA, Hayashi M, Klein C, Hsueh AJ. Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormoneinduced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod 2000; 62:370-377.
24. Hall CS. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J Comp Physiol 1934; 18:385-403.
25. Chen GH, Wang YJ, Zhang LQ, Zhou JN. Age-and sex-related disturbance in a battery of sensorimotor and cognitive tasks in Kunming mice. Physiol Behav 2004; 83:531-541.
26. Livera G, Petre-Lazar B, Guerquin MJ, Trautmann E, Coffigny H, Habert R. p63 null mutation protects mouse oocytes from radio-induced apoptosis. Reproduction 2008; 135:3-12.
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta] CT method. Methods 2001; 25:402-408.
28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193:265-275.
29. Oktay K, Schenken RS, Nelson JF. Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol Reprod 1995; 53: 295-301.
30. Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 2005; 162:127-134.
31. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996; 383:531-535.
32. McGrath SA, Esquela AF, Lee SJ. Oocyte-specific expression of growth/ differentiation factor-9. Mol Endocrinol 1995; 9:131-136.
33. Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 1998; 204:373-384.
34. McNatty KP, Hudson NL, Whiting L, Reader KL, Lun S, Western A, Heath DA, Smith P, Moore LG, Juengel JL. The effects of immunizing sheep with different BMP15 or GDF9 peptide sequences on ovarian follicular activity and ovulation rate. Biol Reprod 2007; 76:552-560.
35. Vitt UA, McGee EA, Hayashi M, Hsueh AJ. In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 2000; 141: 3814-3820.
36. Guéripel X, Brun V, Gougeon A. Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropininduced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod 2006; 75:836-843.
37. Boivin J, Takefnan JE. Impact of the in-vitro fertilization process on emotional, physical and relational variables. Hum Reprod 1996; 11: 903-907.
38. Cousineau TM, Domar AD. Psychological impact of infertility. Best Pract Res Clin Obstet Gynaecol 2007; 21:293-308.
39. Csemiczky G, Landgren BM, Collins A. The influence of stress and state anxiety on the outcome of IVF-treatment: psychological and endocrinological assessment of Swedish women entering IVF-treatment. Acta Obstet Gynecol Scand 2000; 79:113-118.
40. Boivin J, Schmidt L. Infertility-related stress in men and women predicts treatment outcome 1 year later. Fert Steril 2005; 83:1745-1752.
41. Campagne DM. Should fertilization treatment start with reducing stress? Hum Reprod 2006; 21:1651-1658.
42. Demyttenaere K, Bonte L, Gheldof M, Vervaeke M, Meuleman C, Vanderschuerem D, d'Hooghe T. Coping style and depression level influence outcome in in vitro fertilization. Fert Steril 1998; 69:1026-1033.
43. Li XH, Ma YG, Geng LH, Qin L, Hu H, Li SW. Baseline psychological stress and ovarian norepinephrine levels negatively affect the outcome of in vitro fertilisation. Gynecol Endocrinol 2011; 27:139-143.
44. Domar AD, Broome A, Zuttermeister PC, Seibel M, Friedman R. The prevalence and predictability of depression in infertile women. Fert Steril 1992; 58:1158-1163.
45. Boivin J. A review of psychosocial interventions in infertility. Soc Sci Med 2003; 57:2325-2341.
46. Boivin J, Griffiths E, Venetis CA. Emotional distress in infertile women and failure of assisted reproductive technologies: meta-analysis of prospective psychosocial studies. BMJ 342:d223.