Cyclic remodeling of the nonhuman primate endometrium: A model for understanding endometrial receptivity

Seminars in Reproductive Medicine

Volumn 32, Issue 5, 2014, Pages 385-391

  Slayden, Ov Daniel ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

endometrium; histology; menstrual cycle; progesterone; secretory differentiation

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; PROGESTERONE; STEROID; STEROID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CERCOPITHECIDAE; ENDOMETRIAL RECEPTIVITY; ENDOMETRIUM; FEMALE FERTILITY; FEMALE GENITAL TRACT PARAMETERS; FOLLICULAR PHASE; FUNCTIONAL ANATOMY; FUNCTIONAL GENOMICS; FUNCTIONAL MORPHOLOGY; HISTOLOGY; LUTEAL PHASE; MENSTRUAL CYCLE; MENSTRUATION; NIDATION; NONHUMAN; PROGESTERONE RELEASE; PROTEOMICS; RECEPTOR DOWN REGULATION; TISSUE DIFFERENTIATION; TISSUE REGENERATION; UTERUS FUNCTION; UTERUS GROWTH; ANIMAL; CELL DIFFERENTIATION; FEMALE; PHYSIOLOGY; PRIMATE;

ANIMALS; CELL DIFFERENTIATION; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; MENSTRUAL CYCLE; PRIMATES;

EID: 84903179838     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0034-1376357     Document Type: Article

References (56)

1. Shively C. A., Clarkson T. B. The unique value of primate models in translational research. Nonhuman primate models of women's health: introduction and overview. Am J Primatol: 2009; 71 9 715 721
2. Brenner R. M., Slayden O. D. Cyclic changes in the primate oviduct and endometrium. In: Knobil E., Neill J. D., eds. The Physiology of Reproduction. New York Raven Press: 1994; 2 (10): 541 569
3. Slayden O. D., Brenner R. M. Role of progesterone in the structural and biochemical remodeling of the primate endometrium. Ernst Schering Res Found Workshop: 2005; 52 89 118
4. Brenner R. M., Slayden O. D. Molecular and functional aspects of menstruation in the macaque. Rev Endocr Metab Disord: 2012; 13 4 309 318
5. Carroll R. L., Mah K., Fanton J. W., Maginnis G. N., Brenner R. M., Slayden O. D. Assessment of menstruation in the vervet (Cercopithecus aethiops). Am J Primatol: 2007; 69 8 901 916 (Pubitemid 47280331)
6. Van Esch E., Buse E., Weinbauer G. F., Weinberg C. R., Cline J. M. The macaque endometrium, with special reference to the Cynomolgus monkey (Macaca fascicularis). Toxicol Pathol: 2008; 36 67S 100S
7. Kraemer D. C., Maqueo M., Hendrickx A. G., Vera Cruz N. C. Histology of the baboon endometrium during the menstrual cycle and pregnancy. Fertil Steril: 1977; 28 4 482 487 (Pubitemid 8083160)
8. Rosario G. X., Modi D. N., Sachdeva G., Manjramkar D. D., Puri C. P. Morphological events in the primate endometrium in the presence of a preimplantation embryo, detected by the serum preimplantation factor bioassay. Hum Reprod: 2005; 20 1 61 71
9. Gilardi K. V., Shideler S. E., Valverde C. R., Roberts J. A., Lasley B. L. Characterization of the onset of menopause in the rhesus macaque. Biol Reprod: 1997; 57 2 335 340 (Pubitemid 27343692)
10. Nyachieo A., Chai D. C., Deprest J., Mwenda J. M., D'Hooghe T. M. The baboon as a research model for the study of endometrial biology, uterine receptivity and embryo implantation. Gynecol Obstet Invest: 2007; 64 3 149 155 (Pubitemid 47574874)
11. Molskness T. A., Hess D. L., Maginnis G. M., Wright J. W., Fanton J. W., Stouffer R. L. Characteristics and regulation of the ovarian cycle in vervet monkeys (Chlorocebus aethiops). Am J Primatol: 2007; 69 8 890 900 (Pubitemid 47280330)
12. Vandevoort C. A., Mtango N. R., Latham K. E., Stewart D. R. Primate preimplantation embryo is a target for relaxin during early pregnancy. Fertil Steril: 2011; 96 1 203 207
13. VandeVoort C. A., Mtango N. R., Lee Y. S., Smith G. W., Latham K. E. Differential effects of follistatin on nonhuman primate oocyte maturation and pre-implantation embryo development in vitro. Biol Reprod: 2009; 81 6 1139 1146
14. Hisaw F. L., Hisaw F. L. Jr. Action of estrogen and progesterone on the reproductive tract of lower primates. In: Young W. C., ed. Sex and Internal Secretions. Baltimore, MD Lippincott Williams & Wilkins: 1961; 556 589
15. Cox K. E., Sharpe-Timms K. L., Kamiya N., Saraf M., Donnelly K. M., Fazleabas A. T. Differential regulation of stromelysin-1 (matrix metalloproteinase-3) and matrilysin (matrix metalloproteinase-7) in baboon endometrium. J Soc Gynecol Investig: 2000; 7 4 242 248 (Pubitemid 30665622)
16. Slayden O. D., Brenner R. M. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol: 2004; 67 5 393 409 (Pubitemid 40417399)
17. Hodgen G. D. Surrogate embryo transfer combined with estrogen- progesterone therapy in monkeys. Implantation, gestation, and delivery without ovaries. JAMA: 1983; 250 16 2167 2171 (Pubitemid 13018164)
18. Ferenczy A. Surface ultrastructural response of the human uterine lining epithelium to hormonal environment. A scanning electron microscopic study. Acta Cytol: 1977; 21 4 566 572 (Pubitemid 8195631)
19. Kraemer D. C.. Comparative assessment of endometrial morphology and function in nonhuman primate models. In: Diczfalusy E, Fraser IS, Webb FTG, eds. Endometrial Bleeding and Steroidal Contraception (Proceedings of a Symposium on Steroid Contraception and Mechanisms of Endometrial Bleeding Organized by WHO, September 12-14, 1979). Bath, England: Pitman Press Ltd.; 1980;:366-383
20. Bartelmez G. W. Histological studies on the menstruating mucous membrane of the human uterus. Contrib Embryol: 1933; 142 142 186
21. Bartelmez G. W. Cyclic changes in the endometrium of the rhesus monkey (Macaca mulatta). Contrib Embryol: 1951; 34 99 144
22. Padykula H. A., Coles L. G., McCracken J. A., King N. W. Jr, Longcope C., Kaiserman-Abramof I. R. A zonal pattern of cell proliferation and differentiation in the rhesus endometrium during the estrogen surge. Biol Reprod: 1984; 31 5 1103 1118 (Pubitemid 15160412)
23. Fusi L., Cloke B., Brosens J. J. The uterine junctional zone. Best Pract Res Clin Obstet Gynaecol: 2006; 20 4 479 491 (Pubitemid 44688629)
24. Keator C. S., Lindner J. R., Belcik J. T., Bishop C. V., Slayden O. D. Contrast-enhanced ultrasound reveals real-time spatial changes in vascular perfusion during early implantation in the macaque uterus. Fertil Steril: 2011; 95 4 1316 1321, e1-e3
25. Enders A. C. Implantation in the macaque: expansion of the implantation site during the first week of implantation. Placenta: 2007; 28 8-9 794 802 (Pubitemid 47074374)
26. Enders A. C., Blankenship T. N., Fazleabas A. T., Jones C. J. Structure of anchoring villi and the trophoblastic shell in the human, baboon and macaque placenta. Placenta: 2001; 22 4 284 303 (Pubitemid 32537051)
27. Markee J. E. The morphological and endocrine basis for menstrual bleeding. In: Meigs J. V., Surgis S. H., eds. Progress in Gynecology. New York Grune & Stratton: 1950; 63 74
28. Lydon J. P., DeMayo F. J., Conneely O. M., O'Malley B. W. Reproductive phenotypes of the progesterone receptor null mutant mouse. J Steroid Biochem Mol Biol: 1996; 56 1-6, Spec No 67 77 (Pubitemid 26106510)
29. Hild-Petito S., Verhage H. G., Fazleabas A. T. Immunocytochemical localization of estrogen and progestin receptors in the baboon (Papio anubis) uterus during implantation and pregnancy. Endocrinology: 1992; 130 4 2343 2353
30. Noel S. D., Keen K. L., Baumann D. I., Filardo E. J., Terasawa E. Involvement of G protein-coupled receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol Endocrinol: 2009; 23 3 349 359
31. Keator C. S., Mah K., Slayden O. D. Alterations in progesterone receptor membrane component 2 (PGRMC2) in the endometrium of macaques afflicted with advanced endometriosis. Mol Hum Reprod: 2012; 18 6 308 319
32. Brenner R. M., Slayden O. D. Steroid receptors in blood vessels of the rhesus macaque endometrium: a review. Arch Histol Cytol: 2004; 67 5 411 416 (Pubitemid 40417400)
33. Noyes R. W., Hertig A. T., Rock J. Dating the endometrial biopsy. Fertil Steril: 1950; 1 3 25
34. Noyes R. W. The underdeveloped secretory endometrium. Am J Obstet Gynecol: 1959; 77 5 929 945
35. Murray M. J., Meyer W. R., Zaino R. J., et al. A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertil Steril: 2004; 81 5 1333 1343 (Pubitemid 38609319)
36. Batista M. C., Cartledge T. P., Merino M. J., et al. Midluteal phase endometrial biopsy does not accurately predict luteal function. Fertil Steril: 1993; 59 2 294 300 (Pubitemid 23057779)
37. Rudolph-Owen L. A., Slayden O. D., Matrisian L. M., Brenner R. M. Matrix metalloproteinase expression in Macaca mulatta endometrium: evidence for zone-specific regulatory tissue gradients. Biol Reprod: 1998; 59 6 1349 1359 (Pubitemid 28549849)
38. Markee J. E. Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib Embryol: 1940; 177 219 308
39. Nayak N. R., Brenner R. M. Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium. J Clin Endocrinol Metab: 2002; 87 4 1845 1855 (Pubitemid 34615279)
40. Kreitmann-Gimbal B., Goodman A. L., Bayard F., Hodgen G. D. Characterization of estrogen and progesterone receptors in monkey endometrium: methodology and effects of estradiol and/or progesterone on endometrium of castrate monkeys. Steroids: 1979; 34 7 749 770 (Pubitemid 10106607)
41. Chan R. WS, Schwab K. E., Gargett C. E. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod: 2004; 70 6 1738 1750 (Pubitemid 38715630)
42. Brenner R. M., Slayden O. D., Rodgers W. H., et al. Immunocytochemical assessment of mitotic activity with an antibody to phosphorylated histone H3 in the macaque and human endometrium. Hum Reprod: 2003; 18 6 1185 1193 (Pubitemid 36740562)
43. Slayden O. D., Brenner R. M. RU 486 action after estrogen priming in the endometrium and oviducts of rhesus monkeys (Macaca mulatta). J Clin Endocrinol Metab: 1994; 78 2 440 448 (Pubitemid 24061767)
44. Critchley H. OD, Brenner R. M., Henderson T. A., et al. Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium of the human and nonhuman primate endometrium. J Clin Endocrinol Metab: 2001; 86 3 1370 1378
45. Ace C. I., Okulicz W. C. Microarray profiling of progesterone-regulated endometrial genes during the rhesus monkey secretory phase. Reprod Biol Endocrinol: 2004; 2 54
46. Okulicz W. C., Ace C. I. Temporal regulation of gene expression during the expected window of receptivity in the rhesus monkey endometrium. Biol Reprod: 2003; 69 5 1593 1599
47. Critchley H. OD, Brenner R. M., Drudy T. A., Williams K., Groome N. P., Saunders P. TK. Oestrogen receptor beta (ERb) is uniquely expressed by the vascular endothelium of the human and non-human primate endometrium. J Endocrinol: 2000; 167 (Suppl): 69
48. Neulen J., Williams R. F., Breckwoldt M., Chwalisz K., Baulieu E. E., Hodgen G. D. Non-competitive anti-oestrogenic actions of progesterone antagonists in primate endometrium: enhancement of oestrogen and progesterone receptors with blockade of post-receptor proliferative mechanisms. Hum Reprod: 1996; 11 7 1533 1537
49. Enders A. C. Current topic: structural responses of the primate endometrium to implantation. Placenta: 1991; 12 4 309 325
50. Fazleabas A. T., Hild-Petito S., Verhage H. G. Secretory proteins and growth factors of the baboon (Papio anubis) uterus: potential roles in pregnancy. Cell Biol Int: 1994; 18 12 1145 1153
51. Brenner R. M., Cao W. G., Citruk-Ware R., Mah K., Slayden O. D., Tsong Y. Y. Zonal differences in hormonal responsiveness during decidualization in the primate endometrium. The Endocrine Society's 88th Annual Meeting, June 24-27, 2006:P2-56
52. Moghadam K. K., Kessler C. A., Schroeder J. K., Buckley A. R., Brar A. K., Handwerger S. Cannabinoid receptor I activation markedly inhibits human decidualization. Mol Cell Endocrinol: 2005; 229 1-2 65 74 (Pubitemid 40018084)
53. Coutifaris C., Myers E. R., Guzick D. S., et al. NICHD National Cooperative Reproductive Medicine Network. Histological dating of timed endometrial biopsy tissue is not related to fertility status. Fertil Steril: 2004; 82 5 1264 1272 (Pubitemid 39469442)
54. Bogan R. L., Murphy M. J., Stouffer R. L., Hennebold J. D. Systematic determination of differential gene expression in the primate corpus luteum during the luteal phase of the menstrual cycle. Mol Endocrinol: 2008; 22 5 1260 1273 (Pubitemid 351629624)
55. Almeida-Francia C. C., Keator C. S., Mah K., Holden L., Hergert C., Slayden O. D. Localization and hormonal regulation of endometrial matrix metalloproteinase-26 in the rhesus macaque. Hum Reprod: 2012; 27 6 1723 1734
56. Torres M. S., Ace C. I., Okulicz W. C. Assessment and application of laser microdissection for analysis of gene expression in the rhesus monkey endometrium. Biol Reprod: 2002; 67 4 1067 1072