Mesenchymal stem/progenitors and other endometrial cell types from women with polycystic ovary syndrome (PCOS) display inflammatory and oncogenic potential

Journal of Clinical Endocrinology and Metabolism

Volumn 98, Issue 9, 2013, Pages 3765-3775

  Piltonen, T T ^a,b   Chen, J ^a   Erikson, D W ^a   Spitzer, T L B ^a   Barragan, F ^a   Rabban, J T ^a   Huddleston, H ^a   Irwin, J C ^a   Giudice, L C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; OSTEONECTIN; SECRETED FRIZZLED RELATED PROTEIN 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ARTICLE; C4A/B GENE; CARCINOGENESIS; CCL2 GENE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENDOMETRIUM CELL; ENDOTHELIUM CELL; EPITHELIUM CELL; FEMALE; FIBROBLAST; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IL 6 GENE; INFLAMMATION; LCN2 GENE; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; OBESITY; ORM1 GENE; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; PROGENY; PROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SFRP4 GENE; SPARC GENE; SPRR3 GENE; TNAIFP6 GENE; TNFAIP3 GENE; UPREGULATION;

ADULT; BODY MASS INDEX; CELL PROLIFERATION; ENDOMETRIUM; FEMALE; GENE EXPRESSION; HUMANS; INFLAMMATION; INTERLEUKIN-6; INTERLEUKIN-8; MESENCHYMAL STROMAL CELLS; OBESITY; OVERWEIGHT; POLYCYSTIC OVARY SYNDROME; UP-REGULATION;

EID: 84883679792     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-1923     Document Type: Article

References (53)

1. Fauser BC, Tarlatzis BC, Rebar RW, et al. Consensus on women's health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/ASRM-sponsored 3rd PCOS Consensus Workshop Group. Fertil Steril. 2012;97(1):28-38.e25.
2. Villavicencio A, Bacallao K, Avellaira C, Gabler F, Fuentes A, Vega M. Androgen and estrogen receptors and co-regulators levels in endometria from patients with polycystic ovarian syndrome with and without endometrial hyperplasia. Gynecol Oncol. 2006;103(1): 307-314.
3. Savaris RF, Groll JM, Young SL, et al. Progesterone resistance in PCOS endometrium: a microarray analysis in clomiphene citratetreated and artificial menstrual cycles. J Clin Endocrinol Metab. 2011;96(6):1737-1746.
4. Matteo M, Serviddio G, Massenzio F, et al. Reduced percentage of natural killer cells associated with impaired cytokine network in the secretory endometrium of infertile women with polycystic ovary syndrome. Fertil Steril. 2010;94(6):2222-7, 2227.e1-3.
5. Apparao KB, Lovely LP, Gui Y, Lininger RA, Lessey BA. Elevated endometrial androgen receptor expression inwomenwith polycystic ovarian syndrome. Biol Reprod. 2002;66(2):297-304.
6. Sagle M, Bishop K, Ridley N, Alexander FM, et al. Recurrent early miscarriage and polycystic ovaries. BMJ. 1988;297(6655):1027-1028.
7. Tulppala M, Stenman UH, Cacciatore B, Ylikorkala O. Polycystic ovaries and levels of gonadotrophins and androgens in recurrent miscarriage: prospective study in 50 women. Br J Obstet Gynaecol. 1993;100(4):348-352.
8. Koivunen R, Pouta A, Franks S, et al. Northern Finland Birth Cohort 1966 Study. Fecundability and spontaneous abortions in women with self-reported oligo-Amenorrhea and/or hirsutism: Northern Finland Birth Cohort 1966 study. Hum Reprod. 2008;23(9):2134-2139.
9. Boomsma CM, Eijkemans MJ, Hughes EG, Visser GH, Fauser BC, Macklon NS. A meta-Analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update. 2006;12(6): 673-683.
10. Wild S, Pierpoint T, Jacobs H, McKeigue P. Long-Term consequences of polycystic ovary syndrome: results of a 31 year follow-up study. Hum Fertil (Camb). 2000;3(2):101-105.
11. Fearnley EJ, Marquart L, Spurdle AB, Weinstein P, Webb PM. Australian Ovarian Cancer Study Group and Australian National Endometrial Cancer Study Group. Polycystic ovary syndrome increases the risk of endometrial cancer in women aged less than 50 years: an Australian case-control study. Cancer Causes Control. 2010 21(12):2303-2308.
12. Modugno F, Ness RB, Chen C, Weiss NS. Inflammation and endometrial cancer: a hypothesis. Cancer Epidemiol Biomarkers Prev. 2005;14(12):2840-2847.
13. Haoula Z, Salman M, Atiomo W. Evaluating the association between endometrial cancer and polycystic ovary syndrome.HumReprod. 2012;27(5):1327- 1331.
14. Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod. 2007;22(11):2903-2911.
15. Spitzer TL, Rojas A, Zelenko Z, et al. Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod. 2012;86(2):58.
16. Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol. 2008;9(1):11-21.
17. Zawadski J. Diagnostic criteria for polycystic ovary syndrome: towards a rational approach. In: Dunaif A, ed. Polycystic Ovary Syndrome. Boston: Blackwell Scientific: 1992:377-384.
18. Detre S, Saclani Jotti G, Dowsett M. A "quickscore" method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas. J Clin Pathol. 1995;48(9):876-878.
19. Rackow BW, Taylor HS. Submucosal uterine leiomyomas have a global effect on molecular determinants of endometrial receptivity. Fertil Steril. 2010;93(6):2027-2034.
20. Rackow BW, Jorgensen E, Taylor HS. Endometrial polyps affect uterine receptivity. Fertil Steril. 2011;95(8):2690-2692.
21. Dimitriadis E, White CA, Jones RL, Salamonsen LA. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update. 2005;11(6):613-630.
22. Conti I, Rollins BJ. CCL2 (monocyte chemoattractant protein-1) and cancer. Semin Cancer Biol. 2004;14(3):149-154.
23. Caballero-Campo P, Dominguez F, Coloma J, et al. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod. 2002;8(4):375-384.
24. Ulukus M, Ulukus EC, Tavmergen Goker EN, Tavmergen E, Zheng W, Arici A. Expression of interleukin-8 and monocyte chemotactic protein 1 in women with endometriosis. Fertil Steril. 2009;91(3): 687-693.
25. Meter RA, Wira CR, Fahey JV. Secretion of monocyte chemotactic protein-1 by human uterine epithelium directs monocyte migration in culture. Fertil Steril. 2005;84(1):191-201.
26. Arici A, Senturk LM, Seli E, Bahtiyar MO, Kim G. Regulation of monocyte chemotactic protein-1 expression in human endometrial stromal cells by estrogen and progesterone. Biol Reprod. 1999; 61(1):85-90.
27. Naka T, Nishimoto N, Kishimoto T. The paradigm of IL-6: from basic science to medicine. Arthritis Res. 2002;4(suppl 3):S233-S242.
28. Lim KJ, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID. Profile of cytokine mRNA expression in peri-implantation human endometrium. Mol Hum Reprod. 1998;4(1):77-81.
29. Prins JR, Gomez-Lopez N, Robertson SA. Interleukin-6 in pregnancy and gestational disorders. J Reprod Immunol. 2012;95(1-2): 1-14.
30. Jovanovic M, Vicovac L. Interleukin-6 stimulates cell migration, invasion and integrin expression in HTR-8/SVneo cell line. Placenta. 2009;30(4):320-328.
31. Jacobs AL, Sehgal PB, Julian J, Carson DD. Secretion and hormonal regulation of interleukin-6 production by mouse uterine stromal and polarized epithelial cells cultured in vitro. Endocrinology. 1992; 131(3):1037-1046.
32. Naz RK, Butler A. Interleukins-6 and -8 levels in sera and cervical mucus of fertile, idiopathic infertile, and immunoinfertile women: implication in infertility. Am J Reprod Immunol. 1996;35(6):534-540.
33. Demir B,GuvenS,GuvenES, Atamer Y, Gul T. Serum IL-6 levelmay have role in the pathophysiology of unexplained infertility. Am J Reprod Immunol. 2009;62(4):261-267.
34. Roca H, Varsos ZS, Mizutani K, Pienta KJ. CCL2, survivin and autophagy: new links with implications in human cancer. Autophagy. 2008;4(7):969-971.
35. LiMQ,Li HP, Meng YH, et al. Chemokine CCL2 enhances survival and invasiveness of endometrial stromal cells in an autocrine mannerby activating akt and MAPK/ERK1/2 signal pathway. Fertil Steril. 2012;97(4):919-929.
36. Dossus L, Rinaldi S, Becker S, et al. Obesity, inflammatory markers, and endometrial cancer risk: a prospective case-control study. Endocr Relat Cancer. 2010;17(4):1007-1019.
37. Grivennikov S, Karin E, Terzic J, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitisassociated cancer. Cancer Cell. 2009;15(2):103-113.
38. Sharma I, Dhawan V, Mahajan N, Saha SC, Dhaliwal LK. In vitro effects of atorvastatin on lipopolysaccharide-induced gene expression in endometriotic stromal cells. Fertil Steril. 2010;94(5):1639- 46.e1.
39. Takemura Y, Osuga Y, Yoshino O, et al. Metformin suppresses interleukin (IL)-1-induced IL-8 production, aromatase activation, and proliferation of endometriotic stromal cells. J Clin Endocrinol Metab. 2007;92(8):3213-3218.
40. Liao X, Siu MK, Au CW, et al. Aberrant activation of hedgehog signaling pathway contributes to endometrial carcinogenesis through-catenin. Mod Pathol. 2009;22(6):839-847.
41. Petracco RG, Kong A, Grechukhina O, Krikun G, Taylor HS. Global gene expression profiling of proliferative phase endometrium reveals distinct functional subdivisions. Reprod Sci. 2012; 19(10):1138-1145.
42. Carmon KS, Loose DS. Secreted frizzled-related protein 4 regulates two Wnt7a signaling pathways and inhibits proliferation in endometrial cancer cells. Mol Cancer Res. 2008;6(6):1017-1028.
43. Jacob F, Ukegjini K, Nixdorf S, et al. Loss of secreted frizzled-related protein 4 correlates with an aggressive phenotype and predicts poor outcome in ovarian cancer patients. PLoS One. 2012;7(2):e31885.
44. Nagaraju GP, Sharma D. Anti-cancer role of SPARC, an inhibitor of adipogenesis. Cancer Treat Rev. 2011;37(7):559-566.
45. Said NA, Elmarakby AA, Imig JD, Fulton DJ, Motamed K. SPARC ameliorates ovarian cancer-Associated inflammation. Neoplasia. 2008;10(10):1092-1104.
46. Senchenko VN, Krasnov GS, Dmitriev AA, et al. Differential expression of CHL1 gene during development of major human cancers. PLoS One. 2011;6(3):e15612.
47. Pan XY, Wang B, Che YC, Weng ZP, Dai HY, Peng W. Expression of claudin-3 and claudin-4 in normal, hyperplastic, and malignant endometrial tissue. Int J Gynecol Cancer. 2007;17(1):233-241.
48. Le Blanc K, Mougiakakos D. Multipotent mesenchymal stromal cells and the innate immune system. Nat Rev Immunol. 2012;12(5): 383-396.
49. Barbet R, Peiffer I, Hatzfeld A, Charbord P, Hatzfeld JA. Comparison of gene expression in human embryonic stem cells, hESC-derived mesenchymal stem cells and human mesenchymal stem cells. Stem Cells Int. 2011;2011:368192.
50. Hwang WL, Yang MH, Tsai ML, et al. SNAIL regulates interleukin- 8 expression, stem cell-like activity, and tumorigenicity of human colorectal carcinoma cells. Gastroenterology. 2011;141(1): 279-91, 291.e1-5.
51. Cowland JB, Sorensen OE, Sehested M, Borregaard N. Neutrophil gelatinase-Associated lipocalin is up-regulated in human epithelial cells by IL-1-, but not by TNF-. J Immunol. 2003;171(12):6630-6639.
52. Mannelqvist M, Stefansson IM, Wik E, et al. Lipocalin 2 expression is associated with aggressive features of endometrial cancer. BMC Cancer. 2012;12(1):169.
53. Cabarcas SM, Mathews LA, Farrar WL. The cancer stem cell niche-There goes the neighborhood? Int J Cancer. 2011;129(10): 2315-2327.