Cells with stem cell characteristics in somatic compartments of the ovary

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Kossowska Tomaszczuk, Katarzyna ^a   De Geyter, Christian ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN RECEPTOR; COLLAGEN TYPE 1; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, HUMAN;

CELL DIFFERENTIATION; CELL PROLIFERATION; GRANULOSA CELL; HUMAN; IN VITRO STUDY; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; PHENOTYPE; REVIEW; STEM CELL; STEROIDOGENESIS; SYNCYTIUM; ANIMAL; BIOSYNTHESIS; CULTURE TECHNIQUE; CYTOLOGY; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; GRANULOSA CELLS; HUMANS; LEUKEMIA INHIBITORY FACTOR; RECEPTORS, FSH; STEM CELLS;

EID: 84874615517     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/310859     Document Type: Review

References (82)

1. Gougeon A., Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrine Reviews 1996 17 2 121 155 2-s2.0-9244261908 10.1210/er.17.2.121 (Pubitemid 26119956)
2. Rodgers R. J., Lavranos T. C., van Wezel I. L., Irving-Rodgers H. F., Development of the ovarian follicular epithelium. Molecular and Cellular Endocrinology 1999 151 1-2 171 179 2-s2.0-0033602934 10.1016/S0303-7207(99) 00087-8 (Pubitemid 29295525)
3. Rodgers R. J., Irving-Rodgers H. F., van Wezel I. L., Krupa M., Lavranos T. C., Dynamics of the membrana granulosa during expansion of the ovarian follicular antrum. Molecular and Cellular Endocrinology 2001 171 1-2 41 48 2-s2.0-0035931303 10.1016/S0303-7207(00)00430-5 (Pubitemid 32098195)
4. Gomes J. E., Correia S. C., Gouveia-Oliveria A., Three dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth. Molecular Reproduction and Development 1999 54 2 163 172 (Pubitemid 29422271)
5. Vigo D., Villani S., Faustini M., Accorsi P. A., Galeati G., Spinaci M., Munari E., Russo V., Asti A., Conte U., Torre M. L., Follicle-like model by granulosa cell encapsulation in a barium alginate-protamine membrane. Tissue Engineering 2005 11 5-6 709 714 2-s2.0-21844470457 10.1089/ten.2005.11.709 (Pubitemid 40960775)
6. McNatty K. P., Hormonal correlates of follicular development in the human ovary. Australian Journal of Biological Sciences 1981 34 3 249 268 2-s2.0-0019347122
7. Niswender G. D., Juengel J. L., Silva P. J., Rollyson M. K., McIntush E. W., Mechanisms controlling the function and life span of the corpus luteum. Physiological Reviews 2000 80 1 1 29 2-s2.0-0033984010 (Pubitemid 30060560)
8. Bachvarova R., Baran M. M., Tejblum A., Development of naked growing mouse oocytes in vitro. Journal of Experimental Zoology 1980 211 2 159 169 2-s2.0-0018980171
9. Berkholtz C. B., Shea L. D., Woodruff T. K., Extracellular matrix functions in follicle maturation. Seminars in Reproductive Medicine 2006 24 4 262 269 2-s2.0-33748643187 10.1055/s-2006-948555 (Pubitemid 44387530)
10. Thomas R. M., Nechamen C. A., Mazurkiewicz J. E., Muda M., Palmer S., Dias J. A., Follice-stimulating hormone receptor forms oligomers and shows evidence of carboxyl-terminal proteolytic processing. Endocrinology 2007 148 5 1987 1995 2-s2.0-34249792937 10.1210/en.2006-1672 (Pubitemid 46997064)
11. van Blerkom J., Motta P. M., The Cellular Basis of Mammalian Reproduction 1979 Baltimore, Md, USA Urban & Schwarzenberg
12. Makabe S., Iwaki A., Hafez E. S. E., Motta P. M., Hafez E. S. E., Physiomorphology of fertile and infertile human ovaries. Biology of the Ovary 1980 Martinus Nijhoff 279 290
13. Motta P. M., Makabe S., Germ cells in the ovarian surface during fetal development in humans. A three-dimensional microanatomical study by scanning and transmission electron microscopy. Journal of Submicroscopic Cytology 1986 18 2 271 290 2-s2.0-0022588341 (Pubitemid 16111495)
14. Simkins C. S., Development of human ovary from birth to sexual maturity. American Journal of Anatomy 1932 51 2 465 505
15. Virant-Klun I., Skutella T., Stimpfel M., Sinkovec J., Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells. Journal of Biomedicine and Biotechnology 2011 2011 12 10.1155/2011/381928 381928
16. Parte S., Bhartiya D., Telang J., Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells and Development 2011 20 8 1451 1464
17. Bukovsky A., Svetlikova M., Caudle M. R., Oogenesis in cultures derived from adult human ovaries. Reproductive Biology and Endocrinology 2005 3, article 17 2-s2.0-27344446518 10.1186/1477-7827-3-17 (Pubitemid 41522102)
18. Bukovsky A., Keenan J. A., Caudle M. R., Wimalasena J., Upadhyaya N. B., van Meter S. E., Immunohistochemical studies of the adult human ovary: possible contribution of immune and epithelial factors to folliculogenesis. American Journal of Reproductive Immunology 1995 33 4 323 340 2-s2.0-0028936045
19. Bukovsky A., Caudle M. R., Svetlikova M., Upadhyaya N. B., Origin of germ cells and formation of new primary follicles in adult human ovaries. Reproductive Biology and Endocrinology 2004 2, article 20 2-s2.0-4344688026 10.1186/1477-7827-2-20 (Pubitemid 39130559)
20. Buccione R., Vanderhyden B. C., Caron P. J., Eppig J. J., FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Developmental Biology 1990 138 1 16 25 2-s2.0-0025234899 10.1016/0012-1606(90)90172-F (Pubitemid 20086964)
21. Dias J. A., Cohen B. D., Lindau-Shepard B., Nechamen C. A., Peterson A. J., Schmidt A., Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitamins and Hormones 2002 64 249 322 2-s2.0-0036370475 (Pubitemid 135763167)
22. Themmen A. P. N., Huhtaniemi I. T., Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocrine Reviews 2000 21 5 551 583 2-s2.0-0033711033
23. Drummond A. E., The role of steroids in follicular growth. Reproductive Biology and Endocrinology 2006 4 16 27
24. Seifer D. B., Charland C., Berlinsky D., Penzias A. S., Haning R. V., Naftolin F., Barker B. E., Proliferative index of human luteinized granulosa cells varies as a function of ovarian reserve. American Journal of Obstetrics and Gynecology 1993 169 6 1531 1535 2-s2.0-0027136292 (Pubitemid 24009190)
25. Hübner K., Fuhrmann G., Christenson L. K., Kehler J., Reinbold R., de La Fuente R., Wood J., Strauss J. F., Boiani M., Schöler H. R., Derivation of oocytes from mouse embryonic stem cells. Science 2003 300 5623 1251 1256 2-s2.0-18344408969 10.1126/science.1083452 (Pubitemid 36618231)
26. Ioannou J. M., Oogenesis in adult prosimians. Journal of Embryology & Experimental Morphology 1967 17 1 139 145
27. Johnson J., Canning J., Kaneko T., Pru J. K., Tilly J. L., Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004 428 6979 145 150 2-s2.0-1642349298 10.1038/nature02316 (Pubitemid 38374304)
28. Horie K., Fujita J., Takakura K., The expression of c-kit protein in human adult and fetal tissues. Human Reproduction 1993 8 1955 1962 (Pubitemid 23337165)
29. Bazer F. W., Strong science challenges conventional wisdom: new perspectives on ovarian biology. Reproductive Biology and Endocrinology 2004 2, article 28 2-s2.0-4344679287 10.1186/1477-7827-2-28 (Pubitemid 39130551)
30. Gosden R. G., Germline stem cells in the postnatal ovary: is the ovary more like a testis? Human Reproduction Update 2004 10 3 193 195 2-s2.0-2942520096 10.1093/humupd/dmh023
31. Bowen N. J., Walker L. D., Matyunina L. V., Logani S., Totten K. A., Benigno B. B., McDonald J. F., Gene expression profiling supports the hypothesis that human ovarian surface epithelia are multipotent and capable of serving as ovarian cancer initiating cells. BMC Medical Genomics 2009 2, article 71 2-s2.0-74849123453 10.1186/1755-8794-2-71
32. Virant-Klun I., Rožman P., Cvjeticanin B., Vrtacnik-Bokal E., Novakovic S., Rülicke T., Dovc P., Meden-Vrtovec H., Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocyte. Stem Cells and Development 2009 18 1 7 137 150
33. Virant-Klun I., Zech N., Rožman P., Vogler A., Cvjetičanin B., Klemenc P., Maličev 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 8 843 856 2-s2.0-50449109625 10.1111/j.1432-0436.2008.00268.x
34. Okamura H., Katabuchi H., Ohba T., What we have learned from isolated cells from human ovary? Molecular and Cellular Endocrinology 2003 202 1-2 37 45 2-s2.0-0037613388 10.1016/S0303-7207(03)00060-1 (Pubitemid 36593391)
35. Lie B. L., Leung E., Leung P. C. K., Auersperg N., Long-term growth and steroidogenic potential of human granulosa-lutein cells immortalized with SV40 large T antigen. Molecular and Cellular Endocrinology 1996 120 2 169 176 2-s2.0-0030200118 10.1016/0303-7207(96)03835-X (Pubitemid 26241614)
36. Hosokawa K., Dantes A., Schere-levy C., Barash A., Yoshida Y., Kotsuji F., Vlodavsky I., Amsterdam A., Induction of Ad4BP/SF-1, steroidogenic acute regulatory protein, and cytochrome P450scc enzyme system expression in newly established human granulosa cell lines. Endocrinology 1998 139 11 4679 4687 2-s2.0-0031792286 10.1210/en.139.11.4679 (Pubitemid 28487787)
37. Zhang H., Vollmer M., de Geyter M., Litzistorf Y., Ladewig A., Dürrenberger M., Guggenheim R., Miny P., Holzgreve W., de Geyter C., Characterization of an immortalized human granulosa cell line (COV434). Molecular Human Reproduction 2000 6 2 146 153 2-s2.0-12944270510 (Pubitemid 30094277)
38. Nishi Y., Yanase T., Mu Y. M., Oba K., Ichino I., Saito M., Nomura M., Mukasa C., Okabe T., Goto K., Takayanagi R., Kashimura Y., Haji M., Nawata H., Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor. Endocrinology 2001 142 1 437 445 2-s2.0-17744364049 10.1210/en.142.1.437 (Pubitemid 32183706)
39. Kossowska-Tomaszczuk K., de Geyter C., de Geyter M., Martin I., Holzgreve W., Scherberich A., Zhang H., The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells 2009 27 1 210 219 2-s2.0-59849087445 10.1634/stemcells.2008-0233
40. Dahéron L., Opitz S. L., Zaehres H., Lensch W. M., Andrews P. W., Itskovitz-Eldor J., Daley G. Q., LIF/STAT3 signaling fails to maintain self-renewal of human embryonic stem cells. Stem Cells 2004 22 5 770 778 2-s2.0-4444309648 (Pubitemid 39166934)
41. Bauer S., Patterson P. H., Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. Journal of Neuroscience 2006 26 46 12089 12099 2-s2.0-33751079857 10.1523/JNEUROSCI.3047-06.2006 (Pubitemid 44772119)
42. Kalabis J., Patterson M. J., Enders G. H., Marian B., Iozzo R. V., Rogler G., Gimotty P. A., Herlyn M., Stimulation of human colonic epithelial cells by leukemia inhibitory factor is dependent on collagen-embedded fibroblasts in organotypic culture. FASEB Journal 2003 17 9 1115 1117 2-s2.0-0038718739
43. Jiang Y., Vaessen B., Lenvik T., Blackstad M., Reyes M., Verfaillie C. M., Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Experimental Hematology 2002 30 8 896 904 2-s2.0-0036322544 10.1016/S0301-472X(02)00869-X (Pubitemid 34845893)
44. Abir R., Fisch B., Jin S., Barnnet M., Freimann S., van den Hurk R., Feldberg D., Nitke S., Krissi H., Ao A., Immunocytochemical detection and RT-PCR expression of leukaemia inhibitory factor and its receptor in human fetal and adult ovaries. Molecular Human Reproduction 2004 10 5 313 319 2-s2.0-2642534631 10.1093/molehr/gah047 (Pubitemid 38720149)
45. Nilsson E. E., Kezele P., Skinner M. K., Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Molecular and Cellular Endocrinology 2002 188 1-2 65 73 2-s2.0-0037169813 (Pubitemid 34242667)
46. Kreeger P. K., Woodruff T. K., Shea L. D., Murine granulosa cell morphology and function are regulated by a synthetic Arg-Gly-Asp matrix. Molecular and Cellular Endocrinology 2003 205 1-2 1 10 2-s2.0-0142124791 10.1016/S0303-7207(03)00209-0 (Pubitemid 37297346)
47. Cortvrindt R., Smitz J., van Steirteghem A. C., In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Human Reproduction 1996 11 12 2656 2666 2-s2.0-0030454751 (Pubitemid 27060736)
48. West E. R., Shea L. D., Woodruff T. K., Engineering the follicle microenvironment. Seminars in Reproductive Medicine 2007 25 4 287 299 2-s2.0-34447248528 10.1055/s-2007-980222 (Pubitemid 47047912)
49. Abir R., Fisch B., Nitke S., Okon E., Raz A., Ben Rafael Z., Morphological study of fully and partially isolated early human follicles. Fertility and Sterility 2001 75 1 141 146 2-s2.0-0035174134 10.1016/S0015- 0282(00)01668-X (Pubitemid 32041236)
50. Carnegie J. A., Byard R., Dardick I., Tsang B. K., Culture of granulosa cells in collagen gels: the influence of cell shape on steroidogenesis. Biology of Reproduction 1988 38 4 881 890 2-s2.0-0023814785
51. Wang X., Otsu K., Saito H., Hiroi M., Ishikawa K., Sandwich configuration of type I collagen suppresses progesterone production in primary cultured porcine granulosa cells by reducing gene expression of cytochrome P450 cholesterol side-chain cleavage enzyme. Archives of Biochemistry and Biophysics 2000 376 1 117 123 2-s2.0-0034177085 10.1006/abbi.1999.1688 (Pubitemid 30205121)
52. Xu M., Uemura R., Dai Y., Wang Y., Pasha Z., Ashraf M., In vitro and in vivo effects of bone marrow stem cells on cardiac structure and function. Journal of Molecular and Cellular Cardiology 2007 42 2 441 448 2-s2.0-33846395496 10.1016/j.yjmcc.2006.10.009 (Pubitemid 46135600)
53. Hynes R. O., Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992 69 1 11 25 2-s2.0-0026770377 10.1016/0092-8674(92)90115-S
54. Irving-Rodgers H. F., Rodgers R. J., Extracellular matrix in ovarian follicular development and disease. Cell and Tissue Research 2005 322 1 89 98 2-s2.0-27944440580 10.1007/s00441-005-0042-y (Pubitemid 41677659)
55. Irving-Rodgers H. F., Rodgers R. J., Extracellular matrix of the developing ovarian follicle. Seminars in Reproductive Medicine 2006 24 4 195 203 2-s2.0-33748653563 10.1055/s-2006-948549 (Pubitemid 44387524)
56. Ben-Ze'ev A., Amsterdam A., Regulation of cytoskeletal proteins involved in cell contact formation during differentiation of granulosa cells on extracellular matrix. Proceedings of the National Academy of Sciences 1986 83 9 2894 2898 (Pubitemid 16041768)
57. Yamada S., Fujiwara H., Honda T., Higuchi T., Nakayama T., Inoue T., Maeda M., Fujii S., Human granulosa cells express integrin α 2 and collagen type IV: possible involvement of collagen type IV in granulosa cell luteinization. Molecular Human Reproduction 1999 5 7 607 617 2-s2.0-0033057376 10.1093/molehr/5.7.607 (Pubitemid 29317750)
58. Lind A. K., Weijdegard B., Dahm-Kähler P., Collagens in the human ovary and their changes in the perifollicular stroma during ovulation. Acta Obstetricia et Gynecologica Scandinavica 2006 85 12 1476 1484 (Pubitemid 44863767)
59. Le Bellego F., Pisselet C., Huet C., Monget P., Monniaux D., Laminin- α 6 β 1 integrin interaction enhances survival and proliferation and modulates steroidogenesis of ovine granulosa cells. Journal of Endocrinology 2002 172 1 45 59 2-s2.0-0036007211 10.1677/joe.0.1720045 (Pubitemid 34082944)
60. Kossowska-Tomaszczuk K., Pelczar P., Güven S., Kowalski J., Volpi E., de Geyter C., Scherberich A., A novel three-dimensional culture system allows prolonged culture of functional human granulosa cells and mimics the ovarian environment. Tissue Engineering 2010 16 6 2063 2073 2-s2.0-77953340356 10.1089/ten.tea.2009.0684
61. Ben-Rafael Z., Benadiva C. A., Mastroianni L., Garcia C. J., Minda J. M., Iozzo R. V., Flickinger G. L., Collagen matric influences the morphologic features and steroid secretion of human granulosa cells. American Journal of Obstetrics and Gynecology 1988 159 6 1570 1574 2-s2.0-0024166135 (Pubitemid 19021617)
62. Amsterdam A., Rotmensch S., Furman A., Venter E. A., Vlodavsky I., Synergistic effect of human chorionic gonadotropin and extracellular matrix on in vitro differentiation of human granulosa cells: progesterone production and gap junction formation. Endocrinology 1989 124 4 1956 1964 2-s2.0-0024563964 (Pubitemid 19105470)
63. Mauchamp J., Mirrione A., Alquier C., André F., Follicle-like structure and polarized monolayer: role of the extracellular matrix on thyroid cell organization in primary culture. Biology of the Cell 1998 90 5 369 380 2-s2.0-0032158327 10.1016/S0248-4900(98)80086-5 (Pubitemid 29412675)
64. Richardson M. C., Slack C., Stewart I. J., Rearrangement of extracellular matrix during cluster formation by human luteinising granulosa cells in culture. Journal of Anatomy 2000 196 2 243 248 2-s2.0-0034057626 10.1017/S0021878299005920 (Pubitemid 30148173)
65. Amsterdam A., Koch Y., Lieberman M. E., Lindner H. R., Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. Journal of Cell Biology 1975 67 3 894 900 2-s2.0-0016744392
66. Andersen M. M., Kroll J., Byskov A. G., Faber M., Protein composition in the fluid of individual bovine follicles. Journal of Reproduction and Fertility 1976 48 1 109 118 2-s2.0-0017144265
67. van Wezel I. L., Rodgers H. F., Rodgers R. J., Differential localization of laminin chains in bovine follicles. Journal of Reproduction and Fertility 1998 112 2 267 278 2-s2.0-0031746306
68. Richardson M. C., Davies D. W., Watson R. H., Dunsford M. L., Inman C. B., Masson G. M., Cultured human granulosa cells as a model for corpus luteum function: relative roles of gonadotrophin and low density lipoprotein studied under defined culture conditions. Human Reproduction 1992 7 1 12 18 2-s2.0-0026540767
69. Luck M. R., The gonadal extracellular matrix. Oxford Reviews of Reproductive Biology 1994 16 33 85
70. Bruckova L., Soukup T., Visek B., Proliferative potential and phenotypic analysis of long-term cultivated human granulosa cells initiated by addition of follicular fluid. Journal of Assisted Reproduction and Genetics 2011 28 10 939 950
71. Cecconi S., Rossi G., Mouse antral oocytes regulate preantral granulosa cell ability to stimulate oocyte growth in vitro. Developmental Biology 2001 233 1 186 191 2-s2.0-0035339089 10.1006/dbio.2001.0209 (Pubitemid 32411303)
72. Hatzirodos N., Nigro J., Irving-Rodgers H. F., Glycomic analyses of ovarian follicles during development and atresia. Matrix Biology 2012 31 1 45 56
73. Tai M. H., Chang C. C., Olson L. K., Trosko J. E., Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 2005 26 2 495 502 2-s2.0-13844280894 10.1093/carcin/bgh321 (Pubitemid 40246573)
74. Potten C. S., Loeffler M., Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990 110 4 1001 1020 2-s2.0-0025641727 (Pubitemid 120009472)
75. Rodgers H. F., Lavranos T. C., Vella C. A., Rodgers R. J., Basal lamina and other extracellular matrix produced by bovine granulosa cells in anchorage-independent culture. Cell and Tissue Research 1995 282 3 463 471 2-s2.0-0028803296 10.1007/s004410050497
76. Hochedlinger K., Jaenisch R., Nuclear reprogramming and pluripotency. Nature 2006 441 7097 1061 1067 2-s2.0-33745632618 10.1038/nature04955 (Pubitemid 43990717)
77. van Deerlin P. G., Cekleniak N., Coutifaris C., Boyd J., Strauss J. F., Evidence for the oligoclonal origin of the granulosa cell population of the mature human follicle. Journal of Clinical Endocrinology and Metabolism 1997 82 9 3019 3024 2-s2.0-0030952638 10.1210/jc.82.9.3019 (Pubitemid 27385665)
78. Carlsson I. B., Laitinen M., Scott J. E., Kit ligand and c-Kit are expressed during early human ovarian follicular development and their interaction is required for the survival of follicles in long-term culture. Reproduction 2006 131 641 649
79. Tanikawa M., Harada T., Mitsunari M., Onohara Y., Iwabe T., Terakawa N., Expression of c-kit messenger ribonucleic acid in human oocyte and presence of soluble c-kit in follicular fluid. Journal of Clinical Endocrinology and Metabolism 1998 83 4 1239 1242 2-s2.0-0031764509 10.1210/jc.83.4.1239 (Pubitemid 28496400)
80. Antczak M., van Blerkom J., The vascular character of ovarian follicular granulosa cells: phenotypic and functional evidence for an endothelial-like cell population. Human Reproduction 2000 15 11 2306 2318 2-s2.0-0033758186
81. Honda A., Hirose M., Hara K., Isolation, characterization, and in vitro and in vivo differentiation of putative thecal stem cells. Proceedings of the National Academy of Sciences of the United States of America 2007 104 12389 12394 (Pubitemid 47206147)
82. Zou K., Yuan Z., Yang Z., Luo H., Sun K., Zhou L., Xiang J., Shi L., Yu Q., Zhang Y., Hou R., Wu J., Production of offspring from a germline stem cell line derived from neonatal ovaries. Nature Cell Biology 2009 11 5 631 636 2-s2.0-67349113847 10.1038/ncb1869