Assessment of the proliferative status of epithelial cell types in the endometrium of young and menopausal transition women

Human Reproduction

Volumn 22, Issue 6, 2007, Pages 1778-1788

  Niklaus, Andrea L ^a,b   Aubuchon, Mira ^a,c   Zapantis, Gregory ^a   Li, Ping ^a   Qian, Hong ^a   Isaac, Barbara ^a   Kim, Mimi Y ^a   Adel, Goli ^a   Pollard, Jeffrey W ^a   Santoro, Nanette F ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Cell cycle; Endometrium; Laser capture; Menopausal transition; Proliferation

Indexed keywords

BIOLOGICAL MARKER; CYCLIN A1; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 1D; CYCLIN DEPENDENT KINASE INHIBITOR 1E; CYCLIN DEPENDENT KINASE INHIBITOR B; CYCLIN E; CYCLIN E1; CYCLINE; ESTRADIOL; ESTROGEN RECEPTOR; MESSENGER RNA; MINICHROMOSOME MAINTENANCE PROTEIN 2; MONOCLONAL ANTIBODY KI 67; NUCLEAR PROTEIN; PROGESTERONE RECEPTOR; STEROID RECEPTOR; UNCLASSIFIED DRUG;

ADULT; AGE DISTRIBUTION; ARTICLE; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; ENDOMETRIUM BIOPSY; ENDOMETRIUM CELL; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENE LOCATION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MENOPAUSE; MENSTRUAL CYCLE; NORMAL HUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STROMA; TISSUE DISTRIBUTION; UTERUS; UTERUS CAVITY;

EID: 34447333658     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dem032     Document Type: Article

References (65)

1. Abdulla H, Burton G, Kirkland A. Age, pregnancy and miscarriage: Uterine versus ovarian factors. Human Reprod 1993;8:1512-1517.
2. Anastasiadis PG, Koutlaki NG, Skaphida. PG, Galazios GC, Tsikouras PN, Liberis VA. Endometrial polyps: Prevalence, detection, and malignant potential in women with abnormal uterine bleeding. Eur J Gynaecol Oncol 2000a;21:180-183.
3. Anastasiadis PG, Skaphida PG, Koutlaki NG, Galazios GC, Tsikouras PN, Liberis VA. Descriptive, epidemiology of endometrial. hyperplasia in patients with abnormal uterine bleeding. Eur J Gynaecol Oncol 2000b;21:131-134.
4. Bamberger AM, Riethdorf L, Milde-Langosch K, Bamberger CM, Thuneke I, Erdmann I, Schulte HM, Loning T. Strongly reduced expression of the cell cycle inhibitor p27 in endometrial neoplasia. Virchows Arch 1999;434:423-428.
5. Borini A, Bianchi L, Violini F. Oocyte donation program: Pregnancy and implication rates in women of different ages sharing oocytes from single donor. Fertil Steril 1996;64:94-97.
6. Brenner RM, Slayden OD. Progesterone receptor antagonists and the endometrial antiproliferative effect. Semin Reprod med 2005;23 74-81.
7. Brenner RM, Slayden OD, Rodgers WH, Critchley HOD, Carroll R, Nie XJ, Mah K. Immunocytochemical assessment of mitotic activity with an antibody to phosphorylated histone h3 in the macaque and human endometrium. Human Reprod 2003;18:1185-1193.
8. Cano F, Simon C, Remohi J, Pellicer A. Effect of aging on the female reproductive system: Evidence for a role of uterine senescence in the decline in female fecundity. Fertil Steril 1995;64:584-589.
9. Cao QJ, Einstein MH, Anderson PS, Runowicz CD, Balan R, Jones JG. Expression of cox-2, ki-67, cyclin d1, and p21 in endometrial endometrioid carcinomas. Int J Gynecol Pathol 2002;21 147-154.
10. Check J, Askari H, Fisher C. The use of a shared donor oocyte program to evaluate the effect of uterine senescence. Fert Ster 1994;61 252-256.
11. Company MLI. New weight standards for men and women. Stat Bull Metrop Life Found 1983;64:1-4.
12. Critchley HO, Brenner RM, Henderson TA, Williams K, Nayak NR, Slayden OD, Millar M, R, Saunders PT. Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium. of the human and nonhuman primate endometrium. J Clin Endocrinol Metabo 2001;86 1370-1378.
13. Dubowy RL, Feinberg RF, Keefe DL, Doncel GF, Williams SC, McSweet JC, Kliman HJ. Improved endometrial assessment using cyclin e and p27. Fert Steril 2003;80:1456-156.
14. Erel CT, Aydin Y, Kaleli S, Ilvan S, Senturk LM. Is endometrial apoptosis evidence of endometrial aging in unexplained infertility? A preliminary report. Eur J Obstet, Gyneco, Reprod biol 2005;121 195-201.
15. Filicori M, Butler JP, Crowley WFJ. Neuroendocrine regulation of the corpus luteum in the human. Evidence for pulsatile progesterone secretion. J Clini Invest 1984;73:1638-1647.
16. Flamigni C, Borini A, Violini F. Oocyte donation: Comparison between recipients from different age groups. Human Reprod 1993;8 2088-2092.
17. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody ki-67. J Immuno 1984;133 1710-1715.
18. Hayama M, Ota H, Toki T, Ishii K, Honda T, Momose M, Nakata R. Cell kinetic study of the endometrium by nonisotopic in situ hybridization for histone h3 messenger rna and immunohistochemistry for ki-67 and for estrogen and progesterone receptors. Anat Rec 2002;266 234-240.
19. Hewitt SC, Harrell JC, Korach KS. Lessons in estrogen biology from knockout and transgenic animals. Annual Rev physiol 2005;67 285-308.
20. Israel R, Mishell DR, Stone SS, Thorneycroft IH, Moyer DL. Single luteal phase serum progesterone assay as an indicator of ovulation. Am J Obstet Gynecol 1972;112:1043-1046.
21. Jabbour HN, Kelly RW, Fraser HM, Critchley HOD. Endocrine regulation of menstruation. Endoc Rev 2006;27:17-46.
22. Kato K, Toki T, Shimizu M, Shiozawa T, Fujii S, Nikaido T, Konishi I. Expression of replication-licensing factors mcm2 and mcm3 in normal, hyperplastic, and carcinomatous endometrium: Correlation with expression of ki67 and estrogen and progesterone receptors. Int J Gynecol Pathol 2003;22:334-340.
23. Kayaselcuk F, Erkanli S, Bolat F, Seydaoglu G, Kuscu E, Demirhan B. Expression of cyclin h in normal and cancerous endometrium, its correlation with other cyclins, and association with clinicopathologic parameters. Int J Gynecol Cancer 2006;16:402-408.
24. Lessey BA, Killam AP, Metzger DA, Haney AF, Greene G, L, McCarty KSJ. Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J Clin Endocrinol Metabol 1988;67:334-340.
25. Levran D, Ben-Shlomo I, Dor J. Aging of endometrium and oocytes: observations on conception and abortion rates in an egg donation model. Fertil Steril 1991;56:1091-1094.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression using real-time quantitative per and the 2(-delta delta ct) method. Methods 2001;25:402-408.
27. Maiorano D, Lutzmann M, Mechali M. Mcm proteins and DNA replication. Curr Opin Cell Biol 2006;18:130-136.
28. Maldonado V, Castilla JA, Martínez L, Herruzo A, Concha Á, Fontes J, Mendoza N, García-Peña ML, Mendoza JL, Magán R et al. Expression of transcription factors in endometrium during natural cycles. J Assist Reprod Genet 2003;20:474-481.
29. Matsuzaki S, Canis M, Vaurs-Barriere C, Pouly JL, Boespflug-Tanguy O, Penault-Llorca F, Dechelotte P, Dastugue B, Okamura K, Mage G. DNA microarray analysis of gene expression profiles in deep endometriosis using laser capture microdissection. Mol Hum Reprod 2004;10 719-728.
30. Matsuzaki S, Canis M, Vaurs-Barriere C, Boespflug-Tanguy O, Dastugue B, Mage G. DNA microarray analysis of gene expression in eutopic endometrium from patients with deep endometriosis using laser capture microdissection. Fertil Steril 2005;84 (Suppl 2):1180-1190.
31. Matsuzaki S, Canis M, Pouly JL, Botchorishvili R, Dechelotte PJ, Mage G. Differential expression of genes in eutopic and ectopic endometrium from patients with ovarian endometriosis. Fertil Steril 2006;86 548-553.
32. Meldrum DR. Female reproductive aging - ovarian and uterine factors. Fertil steril 1993;59:1-5.
33. Niklaus AL, Pollard JW. Mining the mouse transcriptome of receptive endometrium reveals distinct molecular signatures for the luminal and glandular epithelium. Endocrinology 2006;147:3375-3390.
34. Niklaus AL, Babischkin JS, Aberdeen GW, Pepe GJ, Albrecht ED. Expression of vascular endothelial growth/permeability factor by endometrial glandular epithelial and stromal cells in baboons during the menstrual cycle and after ovariectomy. Endocrinology 2002;143 4007-4017.
35. Oshita T, Shigemasa K, Nagai N, Ohama K. P27, cyclin e, and cdk2 expression in normal and cancerous endometrium. Int J Oncol 2002;21:737-743.
36. Ozuysal S, Ozturk H, Bilgin T, Filiz G. Expression of cyclin d1 in normal, hyperplastic and neoplastic endometrium and its correlation with ki-67 and clinicopathological variables. Arch Gynecol Obstet 2005;271:123-126.
37. Pan H, Deng Y, Pollard JW. Progesterone blocks estrogen induced DNA synthesis through the inhibition of replication liscensing. Proc Nat Acad Sci USA 2006;103:14021-14026.
38. Parazzini F, La Vecchia C, Bocciolone L, Franceschi S. The epidemiology of endometrial cancer. Gynecol Oncol 1991;41:1-16.
39. Pedeutour F, Quade BJ, Weremowicz S, Dal Cin P, Ali S, Morton CC. Localization and expression of the human estrogen receptor beta gene in uterine leiomyomata. Gene Chromosome Cancer 1998;23:361-366.
40. Press MF, Udove JA, Greene GL. Progesterone receptor distribution in the human endometrium. Am J Pathol 1988;131:112-124.
41. Rowe T. Fertility and a woman's age. J Reprod Med 2006;51 157-163.
42. Santoro N, Banwell T, Tortoriello D, Lieman H, Adel T, Skurnick J. Effects of aging and gonadal failure on the hypothalamic-pituitary axis in women. Am J Obstet Gynecol 1998;178:732-741.
43. Santoro N, Goldsmith LT, Heller D, Illsley N, McGovern P, Molina C, Peters S, Skurnick JH, Forst C, Weiss G. Luteal progesterone relates to histological endometrial maturation in fertile women. J Clin Endocrinol Metabol 2000;85:4207-4211.
44. Santoro N, Isaac B, Neal-Perry G, Weingart L, Nussbaum A, Thakur S, Jinnai H, Khosla N, Barad D. Impaired folliculogenesis and ovulation in older reproductive aged women. J Clin Endocrinol Metabol 2003; 88:5502-5509.
45. Sauer MV. The impact of age on reproductive potential: Lessons learned from oocyte donation. Maturitas 1998;30:221-225.
46. Sauer M, Paulson R, Lobo R. Reversing the natural decline in human fertility. An extended clinical trial of oocyte donation to women of advanced reproductive age. J Am Med Assoc 1992;268:1275-1279.
47. Sauer M, Miles R, Damoush L. Evaluating the effect of age on endometrial responsiveness to hormone replacement therapy: A histologic, ultrasonographic, and tissue receptor analysis. J Assist Reprod Genet 1993;10: 47-52.
48. Sauer M, Paulson R, Ary B. Three hundred cycles of oocyte donation at the university of southern california: Assessing the effect of age and infertility diagnosis on pregnancy and implantation rates. J Assist Reprod Genet 1994;11:92-96.
49. Sauer M, Paulson R, Lobo R. Oocyte donation to women of advanced reproductive age: Results and obstetrical outcomes in patients 45 years and older. Human Reprod 1996;11:2540-2543.
50. Schrader C, Janssen D, Klapper W, Siebmann J-U, Meusers P, Brittinger G, Kneba M, Tiemann M, Parwaresch R. Minichromosome maintenance protein 6, a proliferation marker superior to ki-67 and independent predictor of survival in patients with mantle cell lymphoma. Brit J Cancer 2005;93:939-945.
51. Sherr CJ, Roberts JM. Inhibitors of mammalian g1 cyclin-dependent kinases. Gene Dev 1995;9:1149-1163.
52. Shiozawa T, Li S-F, Nakayama K, Nikaido T, Fujii S. Relationship between the expression of cyclins/cyclin-dependent kinases and sex-steroid receptors/ki67 in normal human endometrial glands and stroma during the menstrual cycle. Mol Human Reprod 1996;2:745-752.
53. Shiozawa T, Nikaido T, Shimizu M, Zhai Y, Fujii S. Immuno histochemical analysis of the expression of cdk4 and p16ink4 in human endometrioid-type endometrial carcinoma. Cancer 1997;80 2250-2256.
54. kip1 in growth inhibition of endometrium in the secretory phase and of hyperplastic endometrium treated with progesterone. Mol Human Reprod 1998;4:899-905.
55. Slayden OD, Brenner RM. 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;67:393-409.
56. Soules M, Sherman S, Parrott E. Executive summary: Stages of reproductive aging workshop (straw). Fertil Steril 2001;76 874-878.
57. Tong W, Pollard JW. Progesterone inhibits estrogen-induced cyclin d1 and cdk4 nuclear translocation, cyclin e- and cyclin a-cdk2 kinase activation, and cell proliferation in uterine epithelial cells in mice. Mol Cell Biol 1999;19:2251-2264.
58. Tong W, Pollard JW. Female sex-steroid hormone regulation of cell proliferation in the endometrium. In Glasser SR, Aplin JD, Giudice LC, Tabibzadeh S. (eds) The Endometrium. Taylor and Francis, New York 2002;94-109.
59. Warbrick E. The puzzle of pcna's many partners. Bioessays 2000; 22:997-1006.
60. Weiss G, Skurnick JH, Goldsmith LT, Santoro NF, Park SJ. Menopause and hypothalamic-pituitary sensitivity to estrogen. JAMA 2004;292 2991-2996.
61. Weiss JM, Saltzman BS, Doherty JA, Voigt LF, Chen C, Beresford SAA, Hill DA, Weiss NS. Risk factors for the incidence of endometrial cancer according to the aggressiveness of disease. Am J Epidemiol 2006; 164:56-62.
62. Winking H, Gerdes J, Traut W. Expression of the proliferation marker ki-67 during early mouse development. Cytogenet Genome Res 2004; 105: 251-256.
63. Wu Y, Basir Z, Kajdacsy-Balla A, Strawn E, Macias V, Montgomery K, Guo SW. Resolution of clonal origins for endometriotic lesions using laser capture microdissection and the human androgen receptor (humara) assay. Fertil Steril 2003;79 (Suppl 1),710-717.
64. Wu Y, Kajdacsy-Balla A, Strawn E, Basir Z, Halverson G, Jailwala P, Wang Y, Wang X, Ghosh S, Guo SW. Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology 2006;147:232-246.
65. Zhang H, McElrath T, Tong W, Pollard JW. The molecular basis of tamoxifen induction of mouse uterine epithelial cell proliferation. J Endocrinol 2005;184:129-140.