Current understanding of somatic stem cells in leiomyoma formation

Fertility and Sterility

Volumn 102, Issue 3, 2014, Pages 613-620

  Mas, Aymara ^a   Cervello, Irene ^a   Gil Sanchis, Claudia ^a   Simón, Carlos ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Myometrium; side population; somatic stem cells; tumor initiating cells; uterine leiomyomas

Indexed keywords

BROXURIDINE; GROWTH FACTOR; STEROID HORMONE;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; HUMAN; LEIOMYOMA; MYOMETRIUM; NEOPLASM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SOMATIC CELL; STEM CELL; UTERUS MYOMA;

MYOMETRIUM; SIDE POPULATION; SOMATIC STEM CELLS; TUMOR-INITIATING CELLS; UTERINE LEIOMYOMAS;

CELL TRANSFORMATION, NEOPLASTIC; FEMALE; HUMANS; LEIOMYOMA; MYOCYTES, SMOOTH MUSCLE; MYOMETRIUM; NEOPLASTIC STEM CELLS; SIDE-POPULATION CELLS; UTERINE NEOPLASMS;

EID: 84906939589     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2014.04.051     Document Type: Review

References (110)

1. E.M. Ramsey Anatomy of the human uterus 1994 Cambridge University Press Cambridge
2. M. Ono, T. Maruyama, H. Masuda, T. Kajitani, T. Nagashima, and T. Arase et al. Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells Proc Natl Acad Sci U S A 104 2007 18700 18705
3. J. Teixeira, B.R. Rueda, and J.K. Pru Uterine stem cells Stembook [internet] 2008 Harvard Stem Cell Institute Cambridge, Massachusetts
4. D.J. Prockop Marrow stromal cells as stem cells for nonhematopoietic tissues Science 276 1997 71 74
5. M.F. Pittenger Mesenchymal stem cells from adult bone marrow Methods Mol Biol 449 2008 27 44
6. M.J. Smalley, and R.B. Clarke The mammary gland "side population": a putative stem/progenitor cell marker? J Mammary Gland Biol Neoplasia 10 2005 37 47
7. G. Larderet, N.O. Fortunel, P. Vaigot, M. Cegalerba, P. Maltere, and O. Zobiri et al. Human side population keratinocytes exhibit long-term proliferative potential and specific gene expression profile and can form a pluristratified epidermis Stem Cells 24 2006 965 974
8. U. Martin Methods for studying stem cells: adult stem cells for lung repair Methods 45 2008 121 132
9. K. Iohara, L. Zheng, H. Wake, M. Ito, H. Nabekura, and H. Wakita et al. A novel stem cell source for vasculogenesis in ischemia: subfraction of side population cells from dental pulp Stem Cells 26 2008 2408 2418
10. I. Cervelló, C. Gil-Sanchis, A. Mas, F. Delgado-Rosas, J.A. Martínez-Conejero, and A. Galán et al. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells PLoS One 5 2010 e10964
11. H. Masuda, Y. Matsuzaki, E. Hiratsu, M. Ono, T. Nagashima, and T. Kajitani et al. Stem cell-like propierties of the endometrial side population: implication in endometrial regeneration PLoS One 5 2010 e10387
12. K.M. Braun, C. Niemann, U.B. Jensen, J.P. Sundberg, V. Silva-Vargas, and F.M. Watt Manipulation of stem cell proliferation and lineage commitment: visualization of label-retaining cells in whole mounts of mouse epidermis Development 130 2003 5241 5255
13. N.A. Arango, P.P. Szotek, T.F. Manganaro, E. Oliva, P.K. Donahoe, and J. Teixeira Conditional deletion of beta-catenin in the mesenchyme of the developing mouse uterus results in a switch to adipogenesis in the myometrium Dev Biol 288 2005 1317 1325
14. P. SzoteK, H.L. Chang, L. Zhang, F. Preffer, D. Dombkowski, and P.K. Donahoe et al. Adult mouse myometrial label-retaining cells divide in response to gonadotropin stimulation Stem Cells 25 2007 1317 1325
15. M. Ono, P. Yin, A. Navarro, M.B. Moravek, J.S. Coon 5th, and S.A. Druschitz et al. Paracrine activation of WNT/β-catenin pathway in uterine leiomyoma stem cells promotes tumor growth Proc Natl Acad Sci U S A 110 2013 17053 17058
16. M. Ono, P. Yin, A. Navarro, M.B. Moravek, J.S. Coon V, and S.A. Druschitz et al. Inhibition of canonical WNT signaling attenuates human leiomyoma cell growth Fertil Steril 101 2014 1441 1449
17. C. Liu, Y. Li, M. Semenov, C. Han, G.H. Baeg, and Y. Tan et al. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism Cell 108 2002 837 847
18. S. Ikeda, S. Kishida, H. Yamamoto, H. Murai, S. Koyama, and A. Kikuchi Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin EMBO J 17 1998 1371 1384
19. M.D. Gordon, and R. Nusse Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors J Biol Chem 281 2006 22429 22433
20. M.A. Goodell, K. Brose, G. Paradis, A.S. Conner, and R.C. Mulligan Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo J Exp Med 183 1996 1797 1806
21. G.A. Challen, and M.H. Little A side order of stem cells: the SP phenotype Stem Cells 24 2006 3 12
22. A. Golebiewska, N.H. Brons, R. Bjerkvig, and S.P. Niclou Critical appraisal of the side population assay in stem cell and cancer stem research Cell Stem Cell 8 2011 136 147
23. T. Maruyama, H. Masuda, M. Ono, T. Kajitani, and Y. Yoshimura Human uterine stem/progenitor cells: their possible role in uterine physiology and pathology Reproduction 140 2010 11 22
24. M. Ono, W. Qiang, V.A. Serna, P. Yin, J.S. Coon, and A. Navarro et al. Role of stem cells in human uterine leiomyoma growth PLoS One 7 2012 e36935
25. A. Mas, I. Cervelló, C. Gil-Sanchis, A. Faus, J. Ferro, and A. Pellicer et al. Identification and characterization of the human leiomyoma side population as putative tumor-initiating cells Fertil Steril 98 2012 741 751
26. T. Maruyama, M. Ono, and Y. Yoshimura Somatic stem cells in the myometrium and in myomas Semin Reprod Med 31 2013 77 81
27. T. Maruyama, K. Miyazaki, H. Masuda, M. Ono, H. Uchida, and Y. Yoshimura Review: human uterine stem/progenitor cells: implications for uterine physiology and pathology Placenta 34 Suppl 2013 S68 S72
28. K.D. Burroughs, R. Fuchs-Young, B. Davis, and C.L. Walker Altered hormonal responsiveness of proliferation and apoptosis during myometrial maturation and the development of uterine leiomyomas in the rat Biol Reprod 63 2000 1322 1330
29. O. Shynlova, A. Oldenhof, A. Dorogin, Q. Xu, J. Mu, and N. Nashman et al. Myometrial apoptosis: activation of the caspase cascade in the pregnant rat myometrium at midgestation Biol Reprod 74 2006 839 849
30. O. Shynlova, P. Tsui, S. Jaffer, and S.J. Lye Integration of endocrine and mechanical signals in the regulation of myometrial functions during pregnancy and labour Eur J Obstet Gynecol Reprod Biol 144 Suppl 1 2009 S2 S10
31. H. Matsuo, O. Kurachi, Y. Shimomura, T. Samoto, and T. Maruo Molecular bases for the actions of ovarian sex steroids in the regulation of proliferation and apoptosis of human uterine leiomyoma Oncology 57 Suppl 2 1999 49 58
32. E.A. Stewart Uterine fibroids Lancet 357 2001 293 298
33. C.L. Walker, and E.A. Stewart Uterine fibroids: the elephant in the room Science 308 2005 1589 1592
34. W.H. Parker Etiology, symptomatology, and diagnosis of uterine myomas Fertil Steril 87 2007 725 736
35. J.H. Segars, E.C. Parrott, J.D. Nagel, X.C. Guo, X. Gao, and L.S. Birnbaum et al. Proceedings from the Third National Institutes of Health International Congress on Advances in Uterine Leiomyoma Research: comprehensive review, conference summary and future recommendations Hum Reprod Update 20 2014 309 333
36. E.R. Cardozo, A.D. Clark, N.K. Banks, M.B. Henne, B.J. Stegmann, and J.H. Segars The estimated annual cost of uterine leiomyomata in the United States Am J Obstet Gynecol 206 2012 211.e1 211.e9
37. D.D. Baird, D.B. Dunson, M.C. Hill, D. Cousins, and J.M. Schectman High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence Am J Obstet Gynecol 188 2003 100 107
38. S. Bulun Uterine fibroids N Engl J Med 369 2013 1344 1355
39. Y. Yamagata, R. Maekawa, H. Asada, T. Taketani, I. Tamura, and H. Tamura et al. Aberrant DNA methylation status in human uterine leiomyoma Mol Hum Reprod 15 2009 259 267
40. A. Navarro, P. Yin, D. Monsivais, S.M. Lin, P. Du, and J.J. Wei et al. Genome-wide DNA methylation indicates silencing of tumor suppressor genes in uterine leiomyoma PLoS One 7 2012 e33284
41. L.H. Wei, P.L. Torng, S.M. Hsiao, Y.M. Jeng, M.W. Chen, and C.A. Chen Histone deacetylase-6 regulates estrogen receptor a in uterine leiomyoma Reprod Sci 18 2011 755 762
42. J. Zavadil, H. Ye, Z. Liu, J.J. Wu, P. Lee, and E. Hernando et al. Profiling and functional analyses of microRNAs and their target gene products in human uterine leiomyomas PLoS One 5 2010 e12362
43. B. Georgieva, I. Milev, I. Minkov, I. Dimitrova, A.P. Bradford, and V. Baev Characterization of the uterine leiomyoma microRNAome by deep sequencing Genomics 93 2012 275 281
44. I.P. Tomlinson, N.A. Alam, A.J. Rowan, E. Barclay, E.E. Jaeger, and D. Kelsell et al. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer Nat Genet 30 2002 406 410
45. N. Mäkinen, M. Mehine, J. Tolvaven, E. Kaasinen, Y. Li, and H.J. Lehtonen et al. MED12, the mediator complex subunit 12 gene, is mutated at high frequency in uterine leiomyomas Science 334 2011 252 255
46. M.M. McGuire, A. Yatsenko, L. Hoffner, M. Jones, U. Surti, and A. Rajkovic Whole exome sequencing in a random sample of North American women with leiomyomas identifies MED12 mutations in majority of uterine leiomyomas PLoS One 7 2012 e33251
47. G. Pérot, S. Croce, A. Ribeiro, P. Lagarde, V. Velasco, and A. Neuville et al. MED12 alterations in both human benign and malignant uterine soft tissue tumors PLoS One 7 2012 e40015
48. I. Brosens, J. Deprest, P. Dal Cin, and H. Van den Berghe Clinical significance of cytogenetic abnormalities in uterine myomas Fertil Steril 69 1998 232 235
49. M.S. Rein, W.L. Powell, F.C. Walters, S. Weremowicz, R.M. Cantor, and R.L. Barbieri et al. Cytogenetic abnormalities in uterine myomas are associated with myoma size Mol Hum Reprod 4 1998 83 86
50. M. Mehine, E. Kaasinen, N. Mäkinen, R. Katainen, K. Kämpjärvi, and E. Pitkänen et al. Characterization of uterine leiomyomas by whole-genome sequencing N Engl J Med 369 2013 43 53
51. S.E. Ingraham, R.A. Lynch, S. Kathiresan, A.J. Buckler, and A.G. Menon hREC2, a RAD51-like gene, is disrupted by t(12;14)(q15;q24.1) in a uterine leiomyoma Cancer Genet Cytogenet 115 1999 56 61
52. J. Thacker The RAD51 gene family, genetic instability and cancer Cancer Lett 219 2005 125 135
53. G. Tallini, and P. Dal Cin HMGI(Y) and HMGI-C dysregulation: a common occurrence in human tumors Adv Anat Pathol 6 1999 237 246
54. A.H. Ligon, and C.C. Morton Genetics of uterine leiomyomata Genes Chromosomes Cancer 3 2000 235 245
55. M.S. Islam, O. Protic, P. Stortoni, G. Grechi, P. Lamanna, and F. Petraglia et al. Complex networks of multiple factors in the pathogenesis of uterine leiomyoma Fertil Steril 100 2013 178 193
56. T. Maruo, N. Ohara, J. Wang, and H. Matsuo Sex steroidal regulation of uterine leiomyoma growth and apoptosis Hum Reprod Update 10 2004 207 220 Review
57. E.E. Marsh, and S.E. Bulun Steroid hormones and leiomyomas Obstet Gynecol Clin North Am 33 2006 59 67
58. M. Sabry, and A. Al-Hendy Medical treatment of uterine fibroids Reprod Sci 19 2012 339 353
59. H. Ishikawa, K. Ishi, V.A. Serna, R. Kakazu, S.E. Bulun, and T. Kurita Progesterone is essential for maintenance and growth of uterine leiomyoma Endocrinology 151 2010 2433 2442
60. K. Fiscella, S.H. Eisinger, S. Meldrum, C. Feng, S.G. Fisher, and D.S. Guzick Effect of mifepristone for symptomatic leiomyomata on quality of life and uterine size: a randomized controlled trial Obstet Gynecol 108 Suppl 6 2006 1381 1387
61. J.L. Carbonell Esteve, R. Acosta, B. Heredia, Y. Perez, M.C. Castaneda, and A.V. Hernandez Mifepristone for the treatment of uterine leiomyomas: a randomized controlled trial Obstet Gynecol 112 Suppl 5 2008 1029 1036
62. M. Engman, S. Granberg, A.R. Williams, C.X. Meng, P.G. Lalitkumar, and K. Gemzell-Danielsson Mifepristone for treatment of uterine leiomyoma. A prospective randomized placebo controlled trial Hum Reprod 24 Suppl 8 2009 1870 1879
63. G. Marelli, A.M. Codegoni, and A. Bizzi Estrogen and progesterone receptors in leiomyomas and normal uterine tissues during reproductive life Acta Eur Fertil 20 1989 19 22
64. B. Viville, D.S. Charnock-Jones, A.M. Sharkey, B. Wetzka, and S.K. Smith Distribution of the A and B forms of the progesterone receptor messenger ribonucleic acid and protein in uterine leiomyomata and adjacent myometrium Hum Reprod 12 1997 815 822
65. J.J. Kim, and E.C. Sefton The role of progesterone signaling in the pathogenesis of uterine leiomyoma Mol Cell Endocrinol 358 2011 223 231
66. I. Sozen, and A. Arici Interactions of cytokines, growth factors, and the extracellular matrix in the cellular biology of uterine leiomyomata Fertil Steril 78 2002 1 12
67. G.P. Flake, J. Andersen, and D. Dixon Etiology and pathogenesis of uterine leiomyomas: a review Environ Health Perspect 111 2003 1037 1054
68. Y.Y. Hsieh, C.C. Chang, C.H. Tsai, C.C. Lin, and F.J. Tsai Interleukin (IL)-12 receptorb1 codon 378 G homozygote and allele, but not IL-1 (b-511 promoter, 3953 exon 5, receptor antagonist), IL-2 114, IL-4-590 intron 3, IL-8 30-UTR 2767, and IL-18 105, are associated with higher susceptibility to leiomyoma Fertil Steril 87 2007 886 895
69. S. Nair, and A. Al-Hendy Adipocytes enhance the proliferation of human leiomyoma cells via TNF-α proinflammatory cytokine Reprod Sci 18 2011 1186 1192
70. B. Mehrad, M.P. Keane, and R.M. Strieter Chemokines as mediators of angiogenesis Thromb Haemost 97 2007 755 762
71. N. Chegini Proinflammatory and profibrotic mediators: principal effectorsof leiomyoma development as a fibrotic disorder Semin Reprod Med 28 2010 180 203
72. D.T. Scadden The stem-cell niche as an entity of action Nature 441 2006 1075 1079
73. L. Li, and H. Clevers Coexistence of quiescent and active adult stem cells in mammals Science 327 2010 542 545
74. I.L. Weissman Translating stem and progenitor cell biology to the clinic: barriers and opportunities Science 287 2000 1442 1446
75. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, and J.D. Mosca et al. Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
76. D. Bonnet Haematopoietic stem cells J Pathol 197 2002 430 440
77. F.H. Gage Mammalian neural stem cells Science 287 2000 1433 1438
78. B.A. Reynolds, and S. Weiss Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science 255 1992 1707 1710
79. S. Forbes, P. Vig, R. Poulsom, H. Thomas, and M. Alison Hepatic stem cells J Pathol 197 2002 510 518
80. S. Bonner-Weir, and A. Sharma Pancreatic stem cells J Pathol 197 2002 519 526
81. V. Tropepe, B.L. Coles, B.J. Chiasson, D.J. Horsford, A.J. Elia, and R.R. McInnes et al. Retinal stem cells in the adult mammalian eye Science 287 2000 2032 2036
82. S.M. Hughes, and H.M. Blau Migration of myoblasts across basal lamina during skeletal muscle development Nature 345 1990 350 353
83. K.A. Jackson, T. Mi, and M.A. Goodell Hematopoietic potential of stem cells isolated from murine skeletal muscle Proc Natl Acad Sci U S A 96 1999 14482 14486
84. W.R. Otto Lung epithelial stem cells J Pathol 197 2002 527 535
85. I. Cervelló, A. Mas, C. Gil-Sanchis, L. Peris, A. Faus, and P.T. Saunders et al. Reconstruction of endometrium from human endometrial side population cell lines PLoS One 6 2011 e21221
86. I. Cervelló, C. Gil-Sanchis, A. Mas, A. Faus, J. Sanz, and F. Moscardó et al. Bone marrow-derived cells from male donors do not contribute to the endometrial side population of the recipient PLoS One 7 2012 e30260
87. M. Ono, T. Maruyama, and Y. Yoshimura Regeneration and adult stem cells in the human female reproductive tract Stem Cells Cloning Adv Appl 1 2008 23 29
88. M. Ono, T. Kajitani, H. Uchida, T. Arase, H. Oda, and S. Nishikawa-Uchida et al. OCT4 expression in human uterine myometrial stem/progenitor cells Hum Reprod 25 2010 2059 2067
89. J. Teixeira, S. Maheswaran, and P.K. Donahoe Müllerian inhibiting substance: an instructive developmental hormone with diagnostic and possible therapeutic applications Endocr Rev 22 2001 657 674
90. J. Hu, and T.E. Spencer Carbonic anhydrase regulate endometrial gland development in the neonatal uterus Biol Reprod 73 2005 131 138
91. S. Fujii, I. Konishi, A. Horiuchi, A. Orii, and T. Nikaido Mesenchymal cell differentiation: speculation about the histogenesis of uterine leiomyomas 1999 Parthenon New York
92. T. Kurita, P.S. Cooke, and G.R. Cunha Epithelial-stromal tissue interaction in paramesonephric (müllerian) epithelial differentiation Dev Biol 240 2001 194 211
93. D. Dixon, G.P. Flake, A.B. Moore, H. He, J.K. Haseman, and J.I. Risinger et al. Cell proliferation and apoptosis in human uterine leiomyomas and myometria Virchows Arch 441 2002 53 62
94. H.L. Chang, T.N. Senaratne, L. Zhang, P.P. Szotek, E. Stewart, and D. Dombkowski et al. Uterine leiomyomas exhibit fewer stem/progenitor cell characteristics when compared with corresponding normal myometrium Reprod Sci 17 2010 158 167
95. D. Linder, and S.M. Gartler Glucose-6-phosphate dehydrogenase mosaicism: utilization as a cell marker in the study of leiomyomas Science 150 1965 67 69
96. E. Fuchs, T. Tumbar, and G. Guasch Socializing with the neighbors: stem cells and their niche Cell 116 2004 769 778
97. C.P. Pavlovich, and L.S. Schmidt Searching for the hereditary causes of renal-cell carcinoma Nat Rev Cancer 4 2004 381 393
98. A. Mohyeldin, T. Garzón-Muvdi, and A. Quiñones-Hinojosa Oxygen in stem cell biology: a critical component of the stem cell niche Cell Stem Cell 7 2010 150 161
99. A. Mayer, M. Hoeckel, A. von Wallbrunn, L.C. Horn, and A. Wree HIF-mediated hypoxic response is missing in several hyoxic uterine leiomyomas Adv Exp Med Biol 662 2010 399 405
100. K. Fukuhara, M. Kariya, M. Kita, H. Shime, T. Kanamori, and C. Kosaka et al. Secreted frizzled related protein 1 is overexpressed in uterine leiomyomas, associated with a high estrogenic environment and unrelated to proliferative activity J Clin Endocrinol Metab 87 2002 1729 1736
101. S. Zhou, T. Yi, K. Shen, B. Zhang, F. Huang, and X. Zhao Hypoxia: the driving force of uterine myometrial stem cells differentiation into leiomyoma cells Med Hypotheses 77 2011 985 986
102. T.C. Dale, S.J. Weber-Hall, K. Smith, E.L. Huguet, H. Jayatilake, and B.A. Gusterson et al. Compartment switching of WNT-2 expression in human breast tumors Cancer Res 56 1996 4320 4323
103. G. Abu-Jawdeh, N. Comella, Y. Tomita, L.F. Brown, K. Tognazzi, and S.Y. Sokol et al. Differential expression of frpHE: a novel human stromal protein of the secreted frizzled gene family, during the endometrial cycle and malignancy Lab Invest 79 1999 439 447
104. E. Bertsch, W. Qiang, Q. Zhang, M. Espona-Fiedler, S. Druschitz, and Y. Liu et al. MED12 and HMGA2 mutations: two independent genetic events in uterine leiomyoma and leiomyosarcoma Mod Pathol 2014 [Epub ahead of print.] http://dx.doi.org/10.1038/modpathol.2013.243.
105. D.N. Markowski, I. von Ahsen, M.H. Nezhad, W. Wosniok, B.M. Helmke, and J. Bullerdiek HMGA2 and the p19Arf-TP53-CDKN1A axis: a delicate balance in the growth of uterine leiomyomas Genes Chromosomes Cancer 49 2010 661 668
106. D.N. Markowski, N. Winter, F. Meyer, I. von Ahsen, H. Wenk, and I. Nolte et al. p14Arf acts as an antagonist of HMGA2 in senescence of mesenchymal stem cells-implications for benign tumorigenesis Genes Chromosomes Cancer 50 2011 489 498
107. P. Bouchard, N. Chabbert-Buffet, and B.C. Fauser Selective progesterone receptor modulators in reproductive medicine: pharmacology, clinical efficacy and safety Fertil Steril 96 2011 1175 1189
108. D.D. Baird, J.S. Kesner, and D.B. Dunson Luteinizing hormone in premenopausal women may stimulate uterine leiomyomata development J Soc Gynecol Investig 13 2006 130 135
109. E.A. Stewart Gonadotropins and the uterus: is there a gonad-independent pathway? J Soc Gynecol Investig 8 2001 319 326
110. E.A. Stewart New science will move fibroid therapies into the 21st century Fertil Steril 98 2012 604 605