Table of Contents Author Guidelines Submit a Manuscript
Obstetrics and Gynecology International
Volume 2014, Article ID 783289, 12 pages
http://dx.doi.org/10.1155/2014/783289
Review Article

The Extracellular Matrix Contributes to Mechanotransduction in Uterine Fibroids

1Duke University School of Medicine, Durham, NC 27710, USA
2Unit on Reproductive Endocrinology and Infertility, Program on Pediatric and Adult Endocrinology, NICHD, NIH, Bethesda, MD 20892-1109, USA

Received 21 January 2014; Revised 28 May 2014; Accepted 11 June 2014; Published 3 July 2014

Academic Editor: Peter E. Schwartz

Copyright © 2014 Phyllis C. Leppert et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Rogers, J. Norian, M. Malik et al., “Mechanical homeostasis is altered in uterine leiomyoma,” The American Journal of Obstetrics and Gynecology, vol. 198, no. 4, pp. 474.e1–474.e11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. J. M. Norian, C. M. Owen, J. Taboas et al., “Characterization of tissue biomechanics and mechanical signaling in uterine leiomyoma,” Matrix Biology, vol. 31, no. 1, pp. 57–65, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. F. L. Jayes, X. Ma, E. M. Flannery, F. T. Moutos, F. Guilak, and P. C. Leppert, Biomechanical Evaluation of Human Uterine Fibroids after Exposure to Purified Clostridial Collagenase, Society for the Study of Reproduction, Montreal, Canada, 2013.
  4. N. Wang, J. P. Butler, and D. E. Ingber, “Mechanotransduction across the cell surface and through the cytoskeleton,” Science, vol. 260, no. 5111, pp. 1124–1127, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. D. E. Jaalouk and J. Lammerding, “Mechanotransduction gone awry,” Nature Reviews Molecular Cell Biology, vol. 10, no. 1, pp. 63–73, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Boudreau and M. J. Bissell, “Extracellular matrix signaling: integration of form and function in normal and malignant cells,” Current Opinion in Cell Biology, vol. 10, no. 5, pp. 640–646, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Lu, V. M. Weaver, and Z. J. Werb, “The extracellular matrix: a dynamic niche in cancer progression,” The Journal of Cell Biology, vol. 196, no. 4, pp. 395–406, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. J. K, Y. Mouw, L. Damiano et al., “Tissue mechanics modulate microRNA-dependent PTEN expression to regulate malignant progression,” Nature Medicine, vol. 20, no. 4, pp. 360–367, 2014. View at Google Scholar
  9. Z. Jahed, H. Shams, M. Mehrbod, and M. R. K. Mofrad, “Pathways linking the extracellular matrix to the nucleus,” International Review of Cell and Molecular Biology, vol. 310, pp. 171–220, 2014. View at Google Scholar
  10. M. E. Blaauboer, C. L. Emson, L. Verschuren et al., “Novel combination of collagen dynamics analysis and transcriptional profiling reveals fibrosis-relevant genes and pathways,” Matrix Biology, vol. 3215, no. 7-8, pp. 424–431, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Agha, R. Ogawa, G. Pietramaggiori, and D. P. Orgill, “A review of the role of mechanical forces in cutaneous wound healing,” Journal of Surgical Research, vol. 171, no. 2, pp. 700–708, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Amano, K. Chihara, K. Kimura et al., “Formation of actin stress fibers and focal adhesions enhanced by Rho- kinase,” Science, vol. 275, no. 5304, pp. 1308–1311, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. D. E. Ingber, “Mechanobiology and diseases of mechanotransduction,” Annals of Medicine, vol. 35, no. 8, pp. 564–577, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. P. C. Leppert, “Tissue remodeling in the female reproductive tract: a complex process becomes more complex: the Role of Hox genes,” Biology of Reproduction, vol. 86, no. 4, article 98, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. R. C. Bentley, G. L. Mutter, and S. J. Robboy, “Normal structure of the uterus,” in Pathology of the Female Genital Tract, G. S. Mutter, J. Prat, P. Russell, and M. C. Anderson, Eds., p. 297, Elsevier, Churchill Livingstone, London, UK, 2nd edition, 2008. View at Google Scholar
  16. H. A. Roeder, S. F. Cramer, and P. C. Leppert, “A look at uterine wound healing through a histopathological study of uterine scars,” Reproductive Sciences, vol. 19, no. 5, pp. 463–473, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Schwalm and V. Dubrauszky, “The structure of the musculature of the human uterus—muscles and connective tissue,” American Journal of Obstetrics and Gynecology, vol. 94, no. 3, pp. 391–404, 1966. View at Google Scholar · View at Scopus
  18. P. C. Leppert, T. Baginski, C. Prupas, W. H. Catherino, S. Pletcher, and J. H. Segars, “Comparative ultrastructure of collagen fibrils in uterine leiomyomas and normal myometrium,” Fertility and Sterility, vol. 82, supplement 3, pp. 1182–1187, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Ricard-Blum and F. Ruggiero, “The collagen superfamily: From the extracellular matrix to the cell membrane,” Pathologie Biologie, vol. 53, no. 7, pp. 430–442, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Y. T. Kao and J. G. Leslie, “Polymorphism in human uterine collagen,” Connective Tissue Research, vol. 5, no. 2, pp. 127–129, 1977. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Z. Abedin, S. Ayad, and J. B. Weiss, “Type v collagen: the presence of appreciable amounts of α3(V) chain in uterus,” Biochemical and Biophysical Research Communications, vol. 102, no. 4, pp. 1237–1245, 1981. View at Publisher · View at Google Scholar · View at Scopus
  22. M. O. Pulkkinen, M. Lehto, M. Jalkanen, and K. Näntö-Salonen, “Collagen types and fibronectin in the uterine muscle of normal and hypertensive pregnant patients,” The American Journal of Obstetrics and Gynecology, vol. 149, no. 7, pp. 711–717, 1984. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Trüeb and P. Bornstein, “Characterization of the precursor form of type VI collagen,” Journal of Biological Chemistry, vol. 259, no. 13, pp. 8597–8604, 1984. View at Google Scholar · View at Scopus
  24. J. P. Borel, “Uterine Collagen: general review,” Revue Françoise de Gynécologie et d’ Obstétriques, vol. 86, no. 12, pp. 712–715, 1991. View at Google Scholar
  25. R. Timpl, H. Wiedemann, V. van Delden, H. Furthmayr, and K. Kühn, “A network model for the organization of type IV collagen molecules in basement membranes,” European Journal of Biochemistry, vol. 120, no. 2, pp. 203–211, 1981. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Kokenyesi, “Collagens and proteoglycans,” in The Extracellular Matrix of the Uterus, Cervix and Fetal Membranes: Synthesis, Degradation and Hormonal Regulation, P. C. Leppert and J. F. Woessner, Eds., pp. 15–28, Perinatology Press, Ithaca, NY, USA, 1991. View at Google Scholar
  27. R. Myllyla, J. Koivu, T. Pihlajaniemi, and K. I. Kivirikko, “Protein disulphide-isomerase activity in various cells synthesizing collagen,” European Journal of Biochemistry, vol. 134, no. 1, pp. 7–11, 1983. View at Publisher · View at Google Scholar · View at Scopus
  28. D. J. Prockop, K. I. Kivirikko, L. Tuderman, and N. A. Guzman, “The biosynthesis of collagen and its disorders (first of two parts),” The New England Journal of Medicine, vol. 301, no. 1, pp. 13–23, 1979. View at Publisher · View at Google Scholar · View at Scopus
  29. D. J. Prockop and L. Tuderman, “Posttranslational enzymes in the biosynthesis of collagen: extracellular enzymes,” Methods in Enzymology, vol. 82, pp. 305–319, 1982. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Hofmann, P. P. Fietzek, and K. Kühn, “The role of polar and hydrophobic interactions for the molecular packing of type I collagen: a three-dimensional evaluation of the amino acid sequence,” Journal of Molecular Biology, vol. 125, no. 2, pp. 137–165, 1978. View at Publisher · View at Google Scholar · View at Scopus
  31. D. F. Holmes, C. J. Gilpin, C. Baldock, U. Ziese, A. J. Koster, and K. E. Kadler, “Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 13, pp. 7307–7312, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. R. B. Rücker, N. Romero-Chapman, T. Wong et al., “Modulation of lysyl oxidase by dietary copper in rats,” Journal of Nutrition, vol. 126, no. 1, pp. 51–60, 1996. View at Google Scholar · View at Scopus
  33. M. Saito, K. Marumo, K. Fujii, and N. Ishioka, “Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen,” Analytical Biochemistry, vol. 253, no. 1, pp. 26–32, 1997. View at Publisher · View at Google Scholar · View at Scopus
  34. H. A. Lucero and H. M. Kagan, “Lysyl oxidase: an oxidative enzyme and effector of cell function,” Cellular and Molecular Life Sciences, vol. 63, no. 19-20, pp. 2304–2316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. W. Henkel and R. W. Glanville, “Covalent crosslinking between molecules of type I and type III collagen,” European Journal of Biochemistry, vol. 122, no. 1, pp. 205–213, 1982. View at Publisher · View at Google Scholar
  36. K. M. Mak, E. Chu, K. H. V. Lau, and A. J. Kwong, “Liver fibrosis in elderly cadavers: localization of type I, III, and IV, α-smooth muscle actin, and elastic fibers,” The Anatomical Record, vol. 295, no. 7, pp. 1159–1167, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Prydz and K. T. Dalen, “Synthesis and sorting of proteoglycans,” Journal of Cell Science, vol. 113, no. 2, pp. 193–205, 2000. View at Google Scholar · View at Scopus
  38. N. A. Visser, G. P. J. Vankampen, M. H. M. T. Dekoning, and J. K. Vanderkorst, “The effects of loading on the synthesis of biglycan and decorin in intact mature articular cartilage in vitro,” Connective Tissue Research, vol. 30, no. 4, pp. 241–250, 1994. View at Publisher · View at Google Scholar · View at Scopus
  39. J. E. Scott and C. R. Orford, “Dermatan sulphate-rich proteoglycan associates with rat tail-tendon collagen at the d band in the gap region,” Biochemical Journal, vol. 197, no. 1, pp. 213–216, 1981. View at Google Scholar · View at Scopus
  40. E. Schonherr, H. Hausser, L. Beavan, and H. Kresse, “Decorin-type I collagen interaction. Presence of separate core protein-binding domains,” The Journal of Biological Chemistry, vol. 270, no. 15, pp. 8877–8883, 1995. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Kresse, H. Hausser, and E. Schonherr, “Small proteoglycans,” Experientia, vol. 49, no. 5, pp. 403–416, 1993. View at Publisher · View at Google Scholar · View at Scopus
  42. R. V. Iozzo, “The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins,” The Journal of Biological Chemistry, vol. 274, no. 27, pp. 18843–18846, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. A. G. A. Berto, S. M. Oba, Y. M. Michelacci, and L. O. Sampaio, “Galactosaminoglycans from normal myometrium and leiomyoma,” Brazilian Journal of Medical and Biological Research, vol. 34, no. 5, pp. 633–637, 2001. View at Google Scholar · View at Scopus
  44. P. C. Leppert, R. Kokenyesi, C. A. Klemenich, and J. Fisher, “Further evidence of a decorin-collagen interaction in the disruption of cervical collagen fibers during rat gestation,” American Journal of Obstetrics and Gynecology, vol. 182, no. 4, pp. 805–812, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Kokenyesi and J. F. Woessner Jr., “Effects of hormonal perturbations on the small dermatan sulfate proteoglycan and mechanical properties of the uterine cervix of late pregnant rats.,” Connective Tissue Research, vol. 26, no. 3, pp. 199–205, 1991. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Kokenyesi and J. F. Woessner Jr., “Relationship between dilatation of the rat uterine cervix and a small dermatan sulfate proteoglycan,” Biology of Reproduction, vol. 42, no. 1, pp. 87–97, 1990. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Ruscheinsky, C. de la Motte, and M. Mahendroo, “Hyaluronan and its binding proteins during cervical ripening and parturition: dynamic changes in size, distribution and temporal sequence,” Matrix Biology, vol. 27, no. 5, pp. 487–497, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Akgul, R. Holt, M. Mummert, A. Word, and M. Mahendroo, “Dynamic changes in cervical glycosaminoglycan composition during normal pregnancy and preterm birth,” Endocrinology, vol. 153, no. 7, pp. 3493–3503, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. D. A. Carrino, S. Mesiano, N. M. Barker, W. W. Hurd, and A. I. Caplan, “Proteoglycans of uterine fibroids and keloid scars: similarity in their proteoglycan composition,” Biochemical Journal, vol. 443, no. 2, pp. 361–368, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. C. R. de Lima, J. D. A. dos Santos Jr., A. C. P. Nazário, and Y. M. Michelacci, “Changes in glycosaminoglycans and proteoglycans of normal breast and fibroadenoma during the menstrual cycle,” Biochimica et Biophysica Acta: General Subjects, vol. 1820, no. 7, pp. 1009–1019, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. J. T. Cirulis, C. M. Bellingham, E. C. Davis et al., “Fibrillins, fibulins, and matrix-associated glycoprotein modulate the kinetics and morphology of in vitro self-assembly of a recombinant elastin-like polypeptide,” Biochemistry, vol. 47, no. 47, pp. 12601–12613, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. P. C. Leppert and S. Y. Yu, “Three-dimensional structures of uterine elastic fibers: scanning electron microscopic studies,” Connective Tissue Research, vol. 27, no. 1, pp. 15–31, 1991. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Barczyk, A. I. Bolstad, and D. Gullberg, “Role of integrins in the periodontal ligament: organizers and facilitators,” Periodontology 2000, vol. 63, no. 1, pp. 29–47, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Elosegui-Artola, E. Bazellières, M. D. Allen et al., “Rigidity sensing and adaption through regulation of integrin types,” Nature Materials, vol. 13, no. 6, pp. 631–637, 2014. View at Google Scholar
  55. S. Israeli-Rosenberg, A. M. Manso, H. Okada, and R. S. Ross, “Integrins and integrins-associated proteins in the cardiac myoctye,” Circulation Research, vol. 114, no. 3, pp. 572–586, 2014. View at Google Scholar
  56. G. Mechtersheimer, T. Barth, A. Quentmeier, and P. Möller, “Differential expression of β1 integrins in nonneoplastic smooth and striated muscle cells and in tumors derived from these cells,” American Journal of Pathology, vol. 144, no. 6, pp. 1172–1182, 1994. View at Google Scholar · View at Scopus
  57. C. V. Taylor, M. Letarte, and S. J. Lye, “The expression of integrins and cadherins in normal human uterus and uterine leiomyomas,” The American Journal of Obstetrics and Gynecology, vol. 175, no. 2, pp. 411–419, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Peavey, N. Salleh, and P. C. Leppert, “Collagen-binding α11 integrin expression in human myometrium and fibroids utilizing a novel RNA in situ probe,” Reproductive Sciences, 2014. View at Publisher · View at Google Scholar
  59. H. Ji, V. Long, V. Briody, and E. K. Chien, “Progesterone modulates integrin α2 (ITGA2) and α11 (ITGA11) in the pregnant cervix,” Reproductive Sciences, vol. 18, no. 2, pp. 156–163, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Malik, J. Segars, and W. H. Catherino, “Integrin β1 regulates leiomyoma cytoskeletal integrity and growth,” Matrix Biology, vol. 31, no. 7-8, pp. 389–397, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Singh, C. Carraher, and J. E. Schwarzbauer, “Assembly of fibronectin extracellular matrix,” Annual Review of Cell and Developmental Biology, vol. 26, pp. 397–419, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. D. C. Hocking, P. A. Titus, R. Sumagin, and I. H. Sarelius, “Extracellular matrix fibronectin mechanically couples skeletal muscle contraction with local vasodilation,” Circulation Research, vol. 102, no. 3, pp. 372–379, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Lohi, C. L. Wilson, J. D. Roby, and W. C. Parks, “Epilysin, a novel human matrix metalloproteinase (MMP-28) expressed in testis and keratinocytes and in response to injury,” The Journal of Biological Chemistry, vol. 276, no. 13, pp. 10134–10144, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Nagase, R. Visse, and G. Murphy, “Structure and function of matrix metalloproteinases and TIMPs,” Cardiovascular Research, vol. 69, no. 3, pp. 562–573, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Page-McCaw, A. J. Ewald, and Z. Werb, “Matrix metalloproteinases and the regulation of tissue remodelling,” Nature Reviews Molecular Cell Biology, vol. 8, no. 3, pp. 221–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Suzuki, J. J. Enghild, T. Morodomi, G. Salvesen, and H. Nagase, “Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin),” Biochemistry, vol. 29, no. 44, pp. 10261–10270, 1990. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Chung, D. Dinakarpandian, N. Yoshida et al., “Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis,” The EMBO Journal, vol. 23, no. 15, pp. 3020–3030, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. T. E. Curry Jr. and K. G. Osteen, “The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle,” Endocrine Reviews, vol. 24, no. 4, pp. 428–465, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Khalili, A. H. Talasaz, and M. Salarifar, “Serum vitamin D concentration status and its correlation with early biomarkers of remodeling following acute myocardial infarction,” Clinical Research in Cardiology, vol. 101, no. 5, pp. 321–327, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Abramovitch, L. Dahan-Bachar, E. Sharvit et al., “Vitamin D inhibits proliferation and profibrotic marker expression in hepatic stellate cells and decreases thioacetamide-induced liver fibrosis in rats,” Gut, vol. 60, no. 12, pp. 1728–1737, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. E. A. Stewart, A. J. Friedman, K. Peck, and R. A. Nowak, “Relative overexpression of collagen type I and collagen type III messenger ribonucleic acids by uterine leiomyomas during the proliferative phase of the menstrual cycle,” Journal of Clinical Endocrinology and Metabolism, vol. 79, no. 3, pp. 900–906, 1994. View at Publisher · View at Google Scholar · View at Scopus
  72. W. H. Catherino, P. C. Leppert, M. H. Stenmark et al., “Reduced dermatopontin expression is a molecular link between uterine leiomyomas and keloids,” Genes Chromosomes and Cancer, vol. 40, no. 3, pp. 204–217, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Feng, N. Aviles, S. Leikin, and P. Leppert, “Pattern of collagen types in uterine fibroids,” Reproductive Sciences, vol. 17, article 270A, 2010. View at Google Scholar
  74. M. Iwahashi and Y. Muragaki, “Increased type I and V collagen expression in uterine leiomyomas during the menstrual cycle,” Fertility and Sterility, vol. 95, no. 6, pp. 2137–2139, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. L. O. Sampaio, C. P. Dietrich, and O. Giannotti Filho, “Changes in sulfated mucopolysaccharide composition of mammalian tissues during growth and in cancer tissues,” Biochimica et Biophysica Acta, vol. 498, no. 1, pp. 123–131, 1977. View at Publisher · View at Google Scholar · View at Scopus
  76. A. G. Berto, L. O. Sampaio, C. R. Franco, R. M. Cesar Jr., and Y. M. Michelacci, “A comparative analysis of structure and spatial distribution of decorin in human leiomyoma and normal myometrium,” Biochimica et Biophysica Acta: General Subjects, vol. 1619, no. 1, pp. 98–112, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. F. A. Aleem and M. Predanic, “The hemodynamic effect of GnRH agonist therapy on uterine leiomyoma vascularity: a prospective study using transvaginal color Doppler sonography,” Gynecological Endocrinology, vol. 9, no. 3, pp. 253–258, 1995. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Okuda, K. Oshio, H. Shinmoto et al., “Semiquantitative assessment of MR imaging in prediction of efficacy of gonadotropin-releasing hormone agonist for volume reduction of uterine leiomyoma: initial experience,” Radiology, vol. 248, no. 3, pp. 917–924, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. C. P. West, M. A. Lumsden, S. Lawson, J. Williamson, and D. D. Baird, “Shrinkage of uterine fibroids during therapy with goserelin (Zoladex): a luteinizing hormone-releasing hormone agonist administered as a monthly subcutaneous depot,” Fertility and Sterility, vol. 48, no. 1, pp. 45–51, 1987. View at Google Scholar · View at Scopus
  80. J. L. Britten, M. Malik, G. Levy, M. Mendoza, and W. H. Catherino, “Gonadotropin-releasing hormone (GnRH) agonist leuprolide acetate and GnRH antagonist cetrorelix acetate directly inhibit leiomyoma extracellular matrix production,” Fertility and Sterility, vol. 98, no. 5, pp. 1299–1307, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. J. D. Parker, M. Malik, and W. H. Catherino, “Human myometrium and leiomyomas express gonadotropin-releasing hormone 2 and gonadotropin-releasing hormone 2 receptor,” Fertility and Sterility, vol. 88, no. 1, pp. 39–46, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. D. M. McCarthy-Keith, M. Malik, J. Britten, J. Segars, and W. H. Catherino, “Gonadotropin-releasing hormone agonist increases expression of osmotic response genes in leiomyoma cells,” Fertility and Sterility, vol. 95, no. 7, pp. 2383–2387, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. S. F. Cramer, J. Horiszny, A. Patel, and S. Sigrist, “The relation of fibrous degeneration to menopausal status in small uterine leiomyomas with evidence for postmenopausal origin of seedling myomas,” Modern Pathology, vol. 9, no. 7, pp. 774–780, 1996. View at Google Scholar · View at Scopus
  84. S. F. Cramer, C. Marchetti, J. Freedman, and A. Padela, “Relationship of myoma cell size and menopausal status in small uterine leiomyomas,” Archives of Pathology & Laboratory Medicine, vol. 124, no. 10, pp. 1448–1453, 2000. View at Google Scholar · View at Scopus
  85. I. Konishi, S. Fujii, C. Ban, Y. Okuda, H. Okamura, and S. Tojo, “Ultrastructural study of minute uterine leiomyomas,” International Journal of Gynecological Pathology, vol. 2, no. 2, pp. 113–120, 1983. View at Publisher · View at Google Scholar · View at Scopus
  86. J. T. Holdsworth-Carson, M. Zaitseva, B. J. Vollenhoven, and P. A. Rogers, “Clonality of smooth muscle and fibroid cells populations isolated from human fibroid and myometrial tissues,” Molecular Human Reproduction, vol. 20, no. 3, pp. 250–259, 2014. View at Publisher · View at Google Scholar
  87. R. Tal and J. H. Segars, “The role of angiogenic factors in fibroid pathogenesis: potential implications for future therapy,” Human Reproduction Update, vol. 20, no. 2, pp. 149–216, 2014. View at Publisher · View at Google Scholar
  88. T. Maruyama, M. Ono, and Y. Yoshimura, “Somatic stem cells in the myometrium and in myomas,” Seminars in Reproductive Medicine, vol. 31, no. 1, pp. 77–81, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. J. C. M. Tsibris, J. Segars, D. Coppola et al., “Insights from gene arrays on the development and growth regulation of uterine leiomyomata,” Fertility and Sterility, vol. 78, no. 1, pp. 114–121, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Ono, P. Yin, A. Navarro et al., “Paracrine activation of WNT/β catenin pathway in uterine leiomyoma stem cells promotes tumor growth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 24, pp. 17053–17058, 2013. View at Google Scholar
  91. M. Ono, T. Maruyama, H. Masuda et al., “Side population in human uterine myometrium displays phenotypic and functional characteristics of myometrial stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 47, pp. 18700–18705, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. S. F. Cramer and A. Patel, “The nonrandom regional distribution of uterine leiomyomas: a clue to histogenesis?” Human Pathology, vol. 23, no. 6, pp. 635–638, 1992. View at Publisher · View at Google Scholar · View at Scopus
  93. D. E. Ingber, “Can cancer be reversed by engineering the tumor microenvironment?” Seminars in Cancer Biology, vol. 18, no. 5, pp. 356–364, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nature Reviews Cancer, vol. 9, no. 2, pp. 108–122, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. M. J. Paszek and V. M. Weaver, “The tension mounts: mechanics meets morphogenesis and malignancy,” Journal of Mammary Gland Biology and Neoplasia, vol. 9, no. 4, pp. 325–342, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. M. J. Paszek, N. Zahir, K. R. Johnson et al., “Tensional homeostasis and the malignant phenotype,” Cancer Cell, vol. 8, no. 3, pp. 241–254, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. J. S. Crabtree, S. A. Jelinsky, H. A. Harris et al., “Comparison of human and rat uterine leiomyomata: identification of a dysregulated mammalian target of rapamycin pathway,” Cancer Research, vol. 69, no. 15, pp. 6171–6178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. B. V. Varghese, F. Koohestani, M. McWilliams et al., “Loss of the repressor REST in uterine fibroids promotes aberrant G protein-coupled receptor 10 expression and activates mammalian target of rapamycin pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 6, pp. 2187–2192, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. N. E. Zanchi and A. H. Lancha Jr., “Mechanical stimuli of skeletal muscle: Implications on mTOR/p70s6k and protein synthesis,” European Journal of Applied Physiology, vol. 102, no. 3, pp. 253–263, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. I. Mandl, J. D. MacLennan, and E. L. Howes, “Isolation and characteristics of proteinase and collagenase from Cl histolyticum,” Journal of Clinical Investigation, vol. 32, no. 12, pp. 1323–1329, 1953. View at Publisher · View at Google Scholar · View at Scopus
  101. T. Toyoshima, O. Matsushita, J. Minami, N. Nishi, A. Okabe, and T. Itano, “Collagen-binding domain of a Clostridium histolyticum collagenase exhibits a broad substrate spectrum both in vitro and in vivo,” Connective Tissue Research, vol. 42, no. 4, pp. 281–290, 2001. View at Publisher · View at Google Scholar · View at Scopus
  102. W. Borth, E. J. Menzel, M. Salzer, and C. Steffen, “Human serum inhibitors of collagenase as revealed by preparative isoelectric focusing,” Clinica Chimica Acta, vol. 117, no. 2, pp. 219–225, 1981. View at Publisher · View at Google Scholar · View at Scopus
  103. S. K. Halder, K. G. Osteen, and A. Al-Hendy, “Vitamin D3 inhibits expression and activities of matrix metalloproteinase-2 and -9 in human uterine fibroid cells,” Human Reproduction, vol. 28, no. 9, pp. 2407–2416, 2013. View at Publisher · View at Google Scholar · View at Scopus
  104. B. R. Heaps, M. House, S. Socrate, P. Leppert, and J. F. Strauss III, “Matrix biology and preterm birth,” in Preterm Birth Mechanisms, Mediators, Prediction, Prevention and Interventions, F. Petraglia, J. F. Strauss III, S. G. Gabbe, and G. Weiss, Eds., chapter 8, pp. 70–93, Oxon, Informa Healthcare, Abington, Ill, USA, 2007. View at Google Scholar
  105. D. D. Baird, M. C. Hill, J. M. Schectman, and B. W. Hollis, “Vitamin D and the risk of uterine fibroids,” Epidemiology, vol. 24, no. 3, pp. 447–453, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. 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,” American Journal of Obstetrics and Gynecology, vol. 188, no. 1, pp. 100–107, 2003. View at Publisher · View at Google Scholar · View at Scopus
  107. S. D. Peddada, S. K. Laughlin, K. Miner et al., “Growth of uterine leiomyomata among premenopausal black and white women,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 50, pp. 19887–19892, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. B. J. Davis, J. I. Risinger, G. V. R. Chandramouli, P. R. Bushel, D. D. Baird, and S. D. Peddada, “Gene Expression in Uterine Leiomyoma from Tumors Likely to Be Growing (from Black Women over 35) and Tumors Likely to Be Non-Growing (from White Women over 35),” PLoS ONE, vol. 8, no. 6, Article ID e63909, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. F. Koohestani, A. G. Braudmeier, A. Mahdian et al., “Extracellular matrix collagen alters cell proliferation and cell cycle progression of human uterine smooth muscle cells,” PLoS ONE, vol. 10, Article ID 0075844, 2013. View at Publisher · View at Google Scholar
  110. E. A. Stewart, F. A. Taran, J. Chen et al., “Magnetic resonance elastography of uterine leiomyomas: a feasibility study,” Fertility and Sterility, vol. 95, no. 1, pp. 281–284, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. D. Gullberg, “Shift happens—a paradigm shift for the role of integrins in fibrosis,” Matrix Biology, vol. 28, no. 7, p. 383, 2009. View at Publisher · View at Google Scholar · View at Scopus