The mouse ovarian surface epithelium contains a population of LY6A (SCA-1) expressing progenitor cells that are regulated by ovulation-associated factors

Biology of Reproduction

Volumn 87, Issue 4, 2012, Pages

  Gamwell, Lisa F ^a,b   Collins, Olga ^a,b   Vanderhyden, Barbara C ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Ovarian surface epithelium; Ovulation; Stem cells; Wound healing

Indexed keywords

ATAXIN 1; LEUKEMIA INHIBITORY FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; CELL EXPANSION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; GENETIC MARKER; IN VITRO STUDY; NONHUMAN; OVARY FOLLICLE FLUID; OVULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; ANTIGENS, LY; CALCIUM CHANNEL BLOCKERS; CELLS, CULTURED; EPITHELIAL CELLS; EPITHELIUM; FEMALE; FOLLICULAR FLUID; GENE EXPRESSION REGULATION; MEMBRANE PROTEINS; MICE; OVARY; OVULATION; SPHEROIDS, CELLULAR; STEM CELLS; VERAPAMIL; WOUND HEALING;

EID: 84869445164     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.100347     Document Type: Article

References (55)

1. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 2001; 22:255-288.
2. Murdoch W, Van Kirk E. Steroid hormonal regulation of proliferative, p53 tumor suppressor, and apoptotic responses of sheep ovarian surface epithelial cells. Mol Cell Endocrinol 2002; 186:61-67.
3. Osterholzer HO, Johnson JH, Nicosia SV. An autoradiographic study of rabbit ovarian surface epithelium before and after ovulation. Biol Reprod 1985; 33:729-738.
4. Ackerman RC, Murdoch WJ. Prostaglandin-induced apoptosis of ovarian surface epithelial cells. Prostaglandins 1993; 45:475-485.
5. Burdette J, Kurley S, Kilen S, Mayo K, Woodruff T. Gonadotropininduced superovulation drives ovarian surface epithelia proliferation in CD1 mice. Endocrinology 2006; 147:2338-2345.
6. Ismail RS, Cada M, Vanderhyden BC. Transforming growth factor-beta regulates Kit ligand expression in rat ovarian surface epithelial cells.Oncogene 1999; 18:4734-4741.
7. Wong AS, Leung PC. Role of endocrine and growth factors on the ovarian surface epithelium. J Obstet Gynaecol Res 2007; 33:3-16.
8. Blanpain C, Horsley V, Fuchs E. Epithelial stem cells: turning over new leaves. Cell 2007; 128:445-458.
9. Moore DJ, Markmann JF, Deng S. Avenues for immunomodulation and graft protection by gene therapy in transplantation. Transpl Int 2006; 19:435-445.
10. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004; 428:145-150.
11. Bukovsky A, Gupta SK, Virant-Klun I, Upadhyaya NB, Copas P, Van Meter SE, Svetlikova M, Ayala ME, Dominguez R. Study origin of germ cells and formation of new primary follicles in adult human and rat ovaries. Methods Mol Biol 2008; 450:233-265.
12. Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, Malicev E, Meden-Vrtovec H. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 2008; 76:843-856.
13. White YAR, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med 2012; 18:413-421.
14. Szotek P, Chang H, Brennand K, Fujino A, Pieretti-Vanmarcke R, Lo Celso C, Dombkowski D, Preffer F, Cohen K, Teixeira J, Donahoe P.Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc Natl Acad Sci U S A 2008; 105:12469-12473.14
15. Nagy A, Gertsenstein M, Vintersten K, Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2003.
16. Preffer FI, Dombkowski D, Sykes M, Scadden D, Yang YG. Lineagenegative side-population (SP) cells with restricted hematopoietic capacity circulate in normal human adult blood: immunophenotypic and functional characterization. Stem Cells 2002; 20:417-427.
17. Fried G, Wramsby H, Tally M. Transforming growth factor-beta1, insulinlike growth factors, and insulin-like growth factor binding proteins in ovarian follicular fluid are differentially regulated by the type of ovarian hyperstimulation used for in vitro fertilization. Fertil Steril 1998; 70:129-134.
18. Doyle LK, Donadeu FX. Regulation of the proliferative activity of ovarian surface epithelial cells by follicular fluid. Anim Reprod Sci 2009; 114:443-448.
19. Hsieh M, Zamah A, Conti M. Epidermal growth factor-like growth factors in the follicular fluid: role in oocyte development and maturation. Semin Reprod Med 2009; 27:52-61.
20. Arici A, Oral E, Bahtiyar O, Engin O, Seli E, Jones E. Leukemia inhibitory factor expression in human follicular fluid and ovarian cells.Hum Reprod 1997; 12:1233-1239.
21. Challen GA, Little MH. A side order of stem cells: the SP phenotype.Stem Cells 2006; 24:3-12.
22. Welm BE, Tepera SB, Venezia T, Graubert TA, Rosen JM, Goodell MA.Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 2002; 245:42-56.
23. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183:1797-1806.
24. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF.Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003; 100:3983-3988.
25. Bhatt RI, Brown MD, Hart CA, Gilmore P, Ramani VA, George NJ, Clarke NW. Novel method for the isolation and characterization of the putative prostatic stem cell. Cytometry 2003; 54A:89-99.
26. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF, Mori M. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006; 24:506-513.
27. Jonker JW, Freeman J, Bolscher E, Musters S, Alvi AJ, Titley I, Schinkel AH, Dale TC. Contribution of the ABC transporters Bcrp1 and Mdr1a/1b to the side population phenotype in mammary gland and bone marrow of mice. Stem Cells 2005; 23:1059-1065.
28. Wulf GG, Wang RY, Kuehnle I, Weidner D, Marini F, Brenner MK, Andreeff M, Goodell MA. A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood 2001; 98:1166-1173.
29. Ono M, Maruyama T, Masuda H, Kajitani T, Nagashima T, Arase T, Ito M, Ohta K, Uchida H, Asada H, Yoshimura Y, Okano H, et al. Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells. Proc Natl Acad Sci U S A 2007; 104:18700-18705.
30. Hosonuma S, Kobayashi Y, Kojo S, Wada H, Seino K, Kiguchi K, Ishizuka B. Clinical significance of side population in ovarian cancer cells.Hum Cell 2011; 24:9-12.
31. Szotek P, Pieretti-Vanmarcke R, Masiakos P, Dinulescu D, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin D, Donahoe P. Ovarian cancer side population defines cells with stem cell-like characteristics and mullerian inhibiting substance responsiveness. Proc Natl Acad Sci U S A 2006; 103:11154-11159.
32. Osawa M, Nakamura K, Nishi N, Takahasi N, Tokuomoto Y, Inoue H, Nakauchi H. In vivo self-renewal of c-Kit+ Sca-1+ Lin(low/-)hemopoietic stem cells. J Immunol 1996; 156:3207-3214.
33. Storm MP, Bone HK, Beck CG, Bourillot PY, Schreiber V, Damiano T, Nelson A, Savatier P, Welham MJ. Regulation of Nanog expression by phosphoinositide 3-kinase-dependent signaling in murine embryonic stem cells. J Biol Chem 2007; 282:6265-6273.
34. Noaksson K, Zoric N, Zeng X, Rao MS, Hyllner J, Semb H, Kubista M, Sartipy P. Monitoring differentiation of human embryonic stem cells using real-time PCR. Stem Cells 2005; 23:1460-1467.
35. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell.Dev Biol 1996; 175:1-13.
36. Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D. Is there a neural stem cell in the mammalian forebrain? Trends Neurosci 1996; 19:387-393.
37. Liao MJ, Zhang CC, Zhou B, Zimonjic DB, Mani SA, Kaba M, Gifford A, Reinhardt F, Popescu NC, Guo W, Eaton EN, Lodish HF, et al.Enrichment of a population of mammary gland cells that form mammospheres and have in vivo repopulating activity. Cancer Res 2007; 67: 8131-8138.
38. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17:1253-1270.
39. Woodward WA, Chen MS, Behbod F, Rosen JM. On mammary stem cells. J Cell Sci 2005; 118:3585-3594.
40. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006; 132:191-206.
41. Ouellette Y, Price CA, Carrie're PD. Follicular fluid concentration of transforming growth factor-beta1 is negatively correlated with estradiol and follicle sizeat the early stage of development of the first-wave cohort of bovine ovarian follicles. Domest Anim Endocrinol 2005; 29:623-633.
42. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell 2008; 132:681-696.
43. Spangrude GJ, Smith L, Uchida N, Ikuta K, Heimfeld S, Friedman J, Weissman IL. Mouse hematopoietic stem cells. Blood 1991; 78:1395-1402.
44. Okada S, Nakauchi H, Nagayoshi K, Nishikawa S, Miura Y, Suda T. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood 1992; 80:3044-3050.
45. Holmes C, Stanford W. Concise review: stem cell antigen-1: expression,function, and enigma. Stem Cells 2007; 25:1339-1347.
46. Ma X, de Bruijn M, Robin C, Peeters M, Kong ASJ, de Wit T, Snoijs C, Dzierzak E. Expression of the Ly-6A (Sca-1) lacZ transgene in mouse hematopoietic stem cells and embryos. Br J Haematol 2002; 116:401-408.
47. Ma X, Robin C, Ottersbach K, Dzierzak E. The Ly-6A (Sca-1) GFP transgene is expressed in all adult mouse hematopoietic stem cells. Stem Cells 2002; 20:514-521.
48. Miles C, Sanchez MJ, Sinclair A, Dzierzak E. Expression of the Ly-6E.1 (Sca-1) transgene in adult hematopoietic stem cells and the developing mouse embryo. Development 1997; 124:537-547.
49. Hanson P, Mathews V, Marrus SH, Graubert TA. Enhanced green fluorescent protein targeted to the Sca-1 (Ly-6A) locus in transgenic mice results in efficient marking of hematopoietic stem cells in vivo. Exp Hematol 2003; 31:159-167.
50. Gaytán M, Sánchez MA, Morales C, Bellido C, Millán Y, Martín de Las Mulas J, Sánchez-Criado JE, Gaytán F. Cyclic changes of the ovarian surface epithelium in the rat. Reproduction 2005; 129:311-321.
51. Wright JW, Pejovic T, Fanton J, Stouffer RL. Induction of proliferation in the primate ovarian surface epithelium in vivo. Hum Reprod 2008; 23:129-138.
52. Fathalla MF. Incessant ovulation-a factor in ovarian neoplasia? Lancet 1971; 2:163.
53. Zavadil J, Böttinger E. TGF-beta and epithelial-to-mesenchymal transitions.Oncogene 2005; 24:5764-5774.
54. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zürrer-Härdi U, Bell G, Tam WL, Mani SA, et al.Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012; 148:1015-1028.
55. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704-715.