Integrin β1 regulates leiomyoma cytoskeletal integrity and growth

Matrix Biology

Volumn 31, Issue 7-8, 2012, Pages 389-397

  Malik, Minnie ^a   Segars, James ^a,b   Catherino, William H ^a,b  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Cytoskeletal integrity; Extracellular matrix; Integrin 1; Laminins; RhoA; Uterine leiomyoma

Indexed keywords

ALPHA6 INTEGRIN; BETA1 INTEGRIN; LAMININ; LAMININ 5ALPHA; LAMININ 5BETA; LAMININ 5GAMMA; LAMININ RECEPTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MYOMETRIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TUMOR GROWTH; UTERUS MYOMA;

ANALYSIS OF VARIANCE; ANTIGENS, CD29; BLOTTING, WESTERN; CYTOSKELETON; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESIONS; HUMANS; LAMININ; LEIOMYOMA; POLYMERIZATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; UTERINE NEOPLASMS;

EID: 84870389285     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2012.09.005     Document Type: Article

References (87)

1. Arao S., Masumoto A., Otsuki M. Beta1 integrins play an essential role in adhesion and invasion of pancreatic carcinoma cells. Pancreas 2000, 20:129-137.
2. Bagutti C., Wobus A.M., Fassler R., Watt F.M. Differentiation of embryonal stem cells into keratinocytes: comparison of wild-type and β1 integrin-deficient cells. Dev. Biol. 1996, 179:184-196.
3. Belkin A.M., Stepp M.A. Integrins as receptors for laminins. Microsc. Res. Tech. 2000, 51:280-301.
4. Bouvard D., Brakebusch C., Gustafsson E., Aszodi A., Bengtsson T., Berna A., Fassler R. Functional consequences of integrin gene mutations in mice. Circ. Res. 2001, 89:211-223.
5. Cardozo E.R., Clark A.D., Banks N.K., Henne M.B., Stegmann B.J., Segars J.H. The estimated annual cost of uterine leiomyomata in the United States. Am. J. Obstet. Gynecol. 2012, 206. (211.e1-e9).
6. Carroll J.M., Romero M.R., Watt F.M. Suprabasal integrin expression in the epidermis of transgenic mice results in developmental defects and a phenotype resembling psoriasis. Cell 1995, 83:957-968.
7. Catherino W.H., Leppert P.C., Stenmark M.H., Payson M., Potlog-Nahari C., Nieman L.K., Segars J.H. Reduced dermatopontin expression is a molecular link between uterine leiomyomas and keloids. Genes Chromosomes Cancer 2004, 40:204-217.
8. Chai J., Tarnawski A.S. Serum response factor: discovery, biochemistry, biological roles and implications for tissue injury healing. J. Physiol. Pharmacol. 2002, 53:147-157.
9. Chilosi M., Zamò A., Doglioni C., Reghellin D., Lestani M., Montagna L., Pedron S., Ennas M.G., Cancellieri A., Murer B., Poletti V. Migratory marker expression in fibroblast foci of idiopathic pulmonary fibrosis. Respir. Res. 2006, 7:95.
10. Chrzanowska-Wodnicka M., Burridge K. Tyrosine phosphorylation is involved in reorganization of the actin cytoskeleton in response to serum or LPA stimulation. J. Cell Sci. 1994, 107:3643-3654.
11. Dekkers B.G., Bos I.S., Halayko A.J., Zaagsma J., Meurs H. The laminin β1-competing peptide YIGSR induces a hypercontractile, hypoproliferative airway smooth muscle phenotype in an animal model of allergic asthma. Respir. Res. 2010, 11:170.
12. Delcarpio J.B., Claycomb W.C., Moses R.L. Ultrastructural morphometric analysis of cultured neonatal and adult rat ventricular cardiac muscle cells. Am. J. Anat. 1989, 186:335-345.
13. DeMali K.A., Wennerberg K., Burridge K. Integrin signaling to the actin cytoskeleton. Curr. Opin. Cell Biol. 2003, 15:572-582.
14. Enomoto-Iwamoto M., Menko A.S., Philp N., Boettiger D. Evaluation of integrin molecules involved in substrate adhesion. Cell Adhes. Commun. 1993, 1:191-202.
15. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
16. Faraldo M.M., Deugnier M.A., Thiery J.P., Glukhova M.A. Development of mammary gland requires normal beta 1-integrin function. Adv. Exp. Med. Biol. 2000, 480:169-174.
17. Fassler R., Pfaff M., Murphy J., Noegel A.A., Johansson S., Timpl R., Albrecht R. Lack of β1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J. Cell Biol. 1995, 128:979-988.
18. Fujita M. Histological and biochemical studies on collagen in human uterine leiomyomas. Hokkaido Igaku Zasshi 1985, 60:602-615.
19. Giancotti F.G., Ruoslahti E. Integrin signaling. Science 1999, 285:1028-1032.
20. Giancotti F.G., Tarone G. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu. Rev. Cell Dev. Biol. 2003, 19:173-206.
21. Gressner A.M., Gao C.F., Gressner O.A. Non-invasive biomarkers for monitoring the fibrogenic process in liver: a short survey. World J. Gastroenterol. 2009, 15:2433-2440.
22. Hall A. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 1994, 10:31-54.
23. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
24. Heng E.C., Huang Y., Black S.A., Trackman P.C. CCN2, connective tissue growth factor, stimulates collagen deposition by gingival fibroblasts via module 3 and alpha6- and beta1 integrins. J. Cell. Biochem. 2006, 98:409-420.
25. Herrmann K., Schulze E., Heckmann M., Schubert I., Meurer M., Ziegler V., Haustein U.F., Mehlhorn J., Krieg T. Type III collagen aminopropeptide and laminin P1 levels in serum of patients with silicosis-associated and idiopathic systemic scleroderma. Br. J. Dermatol. 1990, 123:1-7.
26. Howlett A., Bailey N., Damsky C., Petersen O., Bissell M. Cellular growth and survival are mediated by β1 integrins in normal human breast epithelium but not in breast carcinoma. J. Cell Sci. 1995, 108:1945-1957.
27. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
28. Johansson S., Svineng G., Wennerberg K., Armulik A., Lohikangas L. Fibronectin-integrin interactions. Front. Biosci. 1997, 2:d126-d146.
29. Juliano R.L. Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 2002, 42:283-323.
30. Katayama M., Ishizaka A., Sakamoto M., Fujishima S., Sekiguchi K., Asano K., Betsuyaku T., Kotani T., Ware L.B., Matthay M.A., Hashimoto S. Laminin gamma2 fragments are increased in the circulation of patients with early phase acute lung injury. Intensive Care Med. 2010, 36:479-486.
31. Kumar C.C. Signaling by integrin receptors. Oncogene 1998, 17:1365-1373.
32. Lahlou H., Muller W.J. β1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer. Breast Cancer Res. 2011, 13:229.
33. Lau M.T., So W.K., Leung P.C. Integrin β1 mediates epithelial growth factor-induced invasion in human ovarian cancer cells. Cancer Lett. 2012, 320:198-204.
34. Leppert P.C., Baginski T., Prupas C., Catherino W.H., Pletcher S., Segars J.H. Comparative ultrastructure of collagen fibrils in uterine leiomyomas and normal myometrium. Fertil. Steril. 2004, 82:1182-1187.
35. Liu Y., Senger D.R. Matrix-specific activation of Src and Rho initiates capillary morphogenesis of endothelial cells. FASEB J. 2004, 18:457-468.
36. Machesky L.M., Hall A. Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J. Cell Biol. 1997, 138:913-926.
37. Magro G., Fraggetta F., Travali S., Lanzafame S. Immuno-histochemical expression and distribution of alpha2beta1, alpha6beta1, alpha5beta1 integrins and their extracellular ligands, type IV collagen, laminin and fibronectin in palmar fibromatosis. Gen. Diagn. Pathol. 1997, 143:203-208.
38. Malik M., Catherino W.H. Novel method to characterize primary cultures of leiomyoma and myometrium with the use of confirmatory biomarker gene arrays. Fertil. Steril. 2007, 87:1166-1172.
39. Malik M., Catherino W.H. Development and validation of a three-dimensional in vitro model for uterine leiomyoma and patient-matched myometrium. Fertil. Steril. 2012, 97:1287-1293.
40. Malik M., Webb J., Catherino W.H. Retinoic acid treatment of human leiomyoma cells transformed the cell phenotype to one strongly resembling myometrial cells. Clin. Endocrinol. 2008, 69:462-470.
41. Malik M., Norian J., McCarthy-Keith D., Britten J., Catherino W.H. Why leiomyomas are called fibroids: the central role of extracellular matrix in symptomatic women. Semin. Reprod. Med. 2010, 28:169-179.
42. Margadant C., Monsuur H.N., Norman J.C., Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 2011, 23:607-614.
43. Mechtersheimer G., Barth T., Quentmeier A., Möller P. Differential expression of beta 1 integrins in nonneoplastic smooth and striated muscle cells and in tumors derived from these cells. Am. J. Pathol. 1994, 144:1172-1182.
44. Meredith J.E., Fazeli B., Schwartz M.A. The extracellular matrix as a cell survival factor. Mol. Biol. Cell 1993, 4:953-961.
45. Miano J.M. Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 2003, 35:577-593.
46. Miranti C.K., Brugge J.S. Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 2002, 4:E83-E90.
47. Mitropoulou T.N., Theocharis A.D., Stagiannis K.D., Karamanos N.K. Identification, quantification and fine structural characterization of glycosaminoglycans from uterine leiomyoma and normal myometrium. Biochimie 2001, 83:529-536.
48. Mizejewski G. Role of integrins in cancer: survey of expression patterns. Proc. Soc. Exp. Biol. Med. 1999, 222:124-138.
49. Mukhopadhyay N.K., Gilchrist D., Gordon G.J., Chen C.J., Bueno R., Lu M.L., Salgia R., Sugarbaker D.J., Jaklitsch M.T. Integrin-dependent protein tyrosine phosphorylation is a key regulatory event in collagen-IV-mediated adhesion and proliferation of human lung tumor cell line, Calu-1. Ann. Thorac. Surg. 2004, 78:450-457.
50. Nakanuma Y., Harada K., Sato Y., Ikeda H. Recent progress in the etiopathogenesis of pediatric biliary disease, particularly Caroli's disease with congenital hepatic fibrosis and biliary atresia. Histol. Histopathol. 2010, 25:223-235.
51. Neubauer K., Saile B., Ramadori G. Liver fibrosis and altered matrix synthesis. Can. J. Gastroenterol. 2001, 15:187-193.
52. Norian J.M., Owen C.M., Taboas J., Korecki C., Tuan R., Malik M., Catherino W.H., Segars J.H. Characterization of tissue biomechanics and mechanical signaling in uterine leiomyoma. Matrix Biol. 2012, 31:57-65.
53. Nowak R.A. Identifications of new therapies: what in vitro studies can tell us. Clin. Obstet. Gynecol. 2001, 44:327-334.
54. Paszek M.J., Weaver V.M. The tension mounts: mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia 2004, 9:325-342.
55. Pattabiraman P.P., Rao P.V. Mechanistic basis of Rho GTPase-induced extracellular matrix synthesis in trabecular meshwork cells. Am. J. Physiol. Cell Physiol. 2010, 298:C749-C763.
56. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
57. Plebani M., Burlina A. Biochemical markers of hepatic fibrosis. Clin. Biochem. 1991, 24:219-239.
58. Reilly J.T. Idiopathic myelofibrosis: pathogenesis, natural history and management. Blood Rev. 1997, 11:233-242.
59. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992, 70:389-399.
60. Rogers R., Norian J., Malik M., Christman G., Abu-Asab M., Chen F., Korecki C., Latridis J., Catherino W.H., Tuan R.S., Dhillon N., Leppert P., Segars J.H. Mechanical homeostasis is altered in uterine leiomyoma. Am. J. Obstet. Gynecol. 2008, 198. (474.e1-11).
61. Rosa H., Parise E.R. Is there a place for serum laminin determination in patients with liver disease and cancer?. World J. Gastroenterol. 2008, 14:3628-3632.
62. Sabry M., Al-Hendy A. Medical treatment of uterine leiomyoma. Reprod. Sci. 2012, 19:339-353.
63. Sawai H., Okada Y., Funahashi H., Matsuo Y., Takahashi H., Takeyama H., Manabe T. Activation of focal adhesion kinase enhances the adhesion and invasion of pancreatic cancer cells via extracellular signal-regulated kinase-1/2 signaling pathway activation. Mol. Cancer 2005, 4:37.
64. Schoenwaelder S.M., Burridge K. Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 1999, 11:274-286.
65. Schwartz M.A., Ginsberg M.H. Networks and crosstalk: integrin signalling spreads. Nat. Cell Biol. 2002, 4:E65-E68.
66. Schwartz M.A., Shattil S.J. Signaling networks linking integrins and rho family GTPases. Trends Biochem. Sci. 2000, 25:388-391.
67. Segarra A., Simó R., Masmiquel L., Segura R.M., Fonollosa V., Huguet P., Majo J., Piera L., Schwartz S. Serum concentrations of laminin-P1 in thrombotic microangiopathy: usefulness as an index of activity and prognostic value. J. Am. Soc. Nephrol. 2000, 11:434-443.
68. Shimaoka M., Takagi J., Springer T.A. Conformational regulation of integrin structure and function. Annu. Rev. Biophys. Biomol. Struct. 2002, 31:485-516.
69. Streuli C.H., Bissell M.J. Mammary epithelial cells, extracellular matrix, and gene expression. Cancer Treat. Res. 1991, 53:365-381.
70. Streuli C.H., Bailey N., Bissell M.J. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J. Cell Biol. 1991, 115:1383-1395.
71. Stupack D.G. Integrins as a distinct subtype of dependence receptors. Cell Death Differ. 2005, 12:1021-1030.
72. Stupack D.G. The biology of integrins. Oncology 2007, 21:6-12.
73. Stupack D.G., Puente X.S., Boutsaboualoy S., Storgard C.M., Cheresh D.A. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J. Cell Biol. 2001, 155:59-70.
74. Taylor C.V., Letarte M., Lye S.J. The expression of integrins and cadherins in normal human uterus and uterine leiomyomas. Am. J. Obstet. Gynecol. 1996, 175:411-419.
75. Tian B., Lessan K., Kahm J., Kleidon J., Henke C. beta 1 integrin regulates fibroblast viability during collagen matrix contraction through a phosphatidylinositol 3-kinase/Akt/protein kinase B signaling pathway. J. Biol. Chem. 2002, 277:24667-24675.
76. Wagrowska-Danilewicz M., Danilewicz M. Expression of alpha5beta1 and alpha6beta1 integrins in IgA nephropathy (IgAN) with mild and severe proteinuria. An immunohistochemical study. Int. Urol. Nephrol. 2004, 36:81-87.
77. Walker C.L., Stewart E.A. Uterine fibroids: the elephant in the room. Science 2005, 308:1589-1592.
78. Wang J.C. Importance of plasma matrix metalloproteinases (MMP) and tissue inhibitors of metalloproteinase (TIMP) in development of fibrosis in agnogenic myeloid metaplasia. Leuk. Lymphoma 2005, 46:1261-1268.
79. Wang D.Z., Olson E.N. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr. Opin. Genet. Dev. 2004, 14:558-566.
80. Wang R., Li J., Lyte K., Yashpal N.K., Fellows F., Goodyer C.G. Role for beta1 integrin and its associated alpha3, alpha5, and alpha6 subunits in development of the human fetal pancreas. Diabetes 2005, 54:2080-2089.
81. Weaver V.M., Petersen O.W., Wang F., Larabell C.A., Briand P., Damsky C., Bissell M.J. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 1997, 137:231-245.
82. Wei L., Wang L., Carson J.A., Agan J.E., Imanaka-Yoshida K., Schwartz R.J. beta1 integrin and organized actin filaments facilitate cardiomyocyte-specific RhoA-dependent activation of the skeletal alpha-actin promoter. FASEB J. 2001, 15:785-796.
83. Wettschureck N., Offermanns S. Rho/Rho-kinase mediated signaling in physiology and pathophysiology. J. Mol. Med. 2002, 80:629-638.
84. Whittard J.D., Akiyama S.K. Activation of beta1 integrins induces cell-cell adhesion. Exp. Cell Res. 2001, 263:65-76.
85. Wickström S.A., Lange A., Montanez E., Fässler R. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase!. EMBO J. 2010, 29:281-291.
86. Wolańska M., Sobolewski K., Drozdzewicz M., Bankowski E. Extracellular matrix components in uterine leiomyoma and their alteration during the tumour growth. Mol. Cell. Biochem. 1998, 189:145-152.
87. Wolańska M., Sobolewski K., Drozdzewicz M. Integrins and prolidase activity in uterine leiomyoma during tumor growth. Ginekol. Pol. 2001, 72:121-126.