Matrix metalloproteinase 9/gelatinase B is required for neural crest cell migration

Developmental Biology

Volumn 364, Issue 2, 2012, Pages 162-177

  Monsonego Ornan, Efrat ^a   Kosonovsky, Jenia ^a   Bar, Avi ^a   Roth, Lee ^a   Fraggi Rankis, Veatriki ^a   Simsa, Stav ^a   Kohl, Ayelet ^a   Sela Donenfeld, Dalit ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Cell migration; Delamination; ECM; Epithelial to mesenchymal transition; MMP; Neural tube

Indexed keywords

GELATINASE A; GELATINASE B;

ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BIOTRANSFORMATION; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELLULAR DISTRIBUTION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; NEURAL CREST CELL; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

AVES;

EID: 84858082839     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.01.028     Document Type: Article

References (108)

1. Al Aqeel A., Al Sewairi W., Edress B., Gorlin R.J., Desnick R.J., Martignetti J.A. Inherited multicentric osteolysis with arthritis: a variant resembling Torg syndrome in a Saudi family. Am. J. Med. Genet. 2000, 93:11-18.
2. Al-Aqeel A.I. Al-Aqeel Sewairi syndrome, a new autosomal recessive disorder with multicentric osteolysis, nodulosis and arthropathy. The first genetic defect of matrix metalloproteinase 2 gene. Saudi Med. J. 2005, 26:24-30.
3. Alfandari D., Wolfsberg T.G., White J.M., DeSimone D.W. ADAM 13: a novel ADAM expressed in somitic mesoderm and neural crest cells during Xenopus laevis development. Dev. Biol. 1997, 182:314-330.
4. Al-Mayouf S.M., Majeed M., Hugosson C., Bahabri S. New form of idiopathic osteolysis: nodulosis, arthropathy and osteolysis (NAO) syndrome. Am. J. Med. Genet. 2000, 93:5-10.
5. Anderson R.B. Matrix metalloproteinase-2 is involved in the migration and network formation of enteric neural crest-derived cells. Int. J. Dev. Biol. 2010, 54:63-69.
6. Barembaum M., Bronner-Fraser M. Early steps in neural crest specification. Semin. Cell Dev. Biol. 2005, 16:642-646.
7. Basch M.L., Bronner-Fraser M. Neural crest inducing signals. Adv. Exp. Med. Biol. 2006, 589:24-31.
8. Behrendtsen O., Werb Z. Metalloproteinases regulate parietal endoderm differentiating and migrating in cultured mouse embryos. Dev. Dyn. 1997, 208:255-265.
9. Ben-Zvi T., Yayon A., Gertler A., Monsonego-Ornan E. Suppressors of cytokine signaling (SOCS) 1 and SOCS3 interact with and modulate fibroblast growth factor receptor signaling. J. Cell Sci. 2006, 119:380-387.
10. Burstyn-Cohen T., Kalcheim C. Association between the cell cycle and neural crest delamination through specific regulation of G1/S transition. Dev. Cell 2002, 3:383-395.
11. Burstyn-Cohen T., Stanleigh J., Sela-Donenfeld D., Kalcheim C. Canonical Wnt activity regulates trunk neural crest delamination linking BMP/noggin signaling with G1/S transition. Development 2004, 131:5327-5339.
12. Cai D.H., Brauer P.R. Synthetic matrix metalloproteinase inhibitor decreases early cardiac neural crest migration in chicken embryos. Dev. Dyn. 2002, 224:441-449.
13. Cai D.H., Vollberg T.M., Hahn-Dantona E., Quigley J.P., Brauer P.R. MMP-2 expression during early avian cardiac and neural crest morphogenesis. Anat. Rec. 2000, 259:168-179.
14. Canete-Soler R., Gui Y.H., Linask K.K., Muschel R.J. Developmental expression of MMP-9 (gelatinase B) mRNA in mouse embryos. Dev. Dyn. 1995, 204:30-40.
15. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
16. Cantemir V., Cai D.H., Reedy M.V., Brauer P.R. Tissue inhibitor of metalloproteinase-2 (TIMP-2) expression during cardiac neural crest cell migration and its role in proMMP-2 activation. Dev. Dyn. 2004, 231:709-719.
17. Cheung M., Chaboissier M.C., Mynett A., Hirst E., Schedl A., Briscoe J. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 2005, 8:179-192.
18. Chin J.R., Werb Z. Matrix metalloproteinases regulate morphogenesis, migration and remodeling of epithelium, tongue skeletal muscle and cartilage in the mandibular arch. Development 1997, 124:1519-1530.
19. Coles E.G., Taneyhill L.A., Bronner-Fraser M. A critical role for Cadherin6B in regulating avian neural crest emigration. Dev. Biol. 2007, 312:533-544.
20. Cousin H., Abbruzzese G., Kerdavid E., Gaultier A., Alfandari D. Translocation of the cytoplasmic domain of ADAM13 to the nucleus is essential for Calpain8-a expression and cranial neural crest cell migration. Dev Cell 2011, 20:256-263.
21. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
22. Coussens L.M., Tinkle C.L., Hanahan D., Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000, 103:481-490.
23. Dan H., Simsa S., Hisdai A., Sela-Donenfeld D., Monsonego Ornan E. Expression of matrix metalloproteinases during impairment and recovery of the avian growth plate. J. Anim. Sci. 2009, 87:3544-3555.
24. Desban N., Lissitzky J.C., Rousselle P., Duband J.L. Alpha1beta1-integrin engagement to distinct laminin-1 domains orchestrates spreading, migration and survival of neural crest cells through independent signaling pathways. J. Cell Sci. 2006, 119:3206-3218.
25. Dottori M., Gross M.K., Labosky P., Goulding M. The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 2001, 128:4127-4138.
26. Duband J.L., Thiery J.P. Distribution of laminin and collagens during avian neural crest development. Development 1987, 101:461-478.
27. Duong T.D., Erickson C.A. MMP-2 plays an essential role in producing epithelial-mesenchymal transformations in the avian embryo. Dev. Dyn. 2004, 229:42-53.
28. Eisen J.S., Smith J.C. Controlling morpholino experiments: don't stop making antisense. Development 2008, 135:1735-1743.
29. Engsig M.T., Chen Q.J., Vu T.H., Pedersen A.C., Therkidsen B., Lund L.R., Henriksen K., Lenhard T., Foged N.T., Werb Z., et al. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J. Cell Biol. 2000, 151:879-889.
30. Erickson C.A. Morphogenesis of the neural crest. Dev. Biol. (N Y 1985) 1986, 2:481-543.
31. Erickson C.A. Control of pathfinding by the avian trunk neural crest. Development 1988, 103(Suppl):63-80.
32. Erickson C.A., Reedy M.V. Neural crest development: the interplay between morphogenesis and cell differentiation. Curr. Top. Dev. Biol. 1998, 40:177-209.
33. Farlie P.G., Kerr R., Thomas P., Symes T., Minichiello J., Hearn C.J., Newgreen D. A paraxial exclusion zone creates patterned cranial neural crest cell outgrowth adjacent to rhombomeres 3 and 5. Dev. Biol. 1999, 213:70-84.
34. Gammill L.S., Bronner-Fraser M. Neural crest specification: migrating into genomics. Nat. Rev. Neurosci. 2003, 4:795-805.
35. Gammill L.S., Roffers-Agarwal J. Division of labor during trunk neural crest development. Dev. Biol. 2010, 344:555.
36. Giambernardi T.A., Sakaguchi A.Y., Gluhak J., Pavlin D., Troyer D.A., Das G., Rodeck U., Klebe R.J. Neutrophil collagenase (MMP-8) is expressed during early development in neural crest cells as well as in adult melanoma cells. Matrix Biol. 2001, 20:577-587.
37. Graham A., Lumsden A. Patterning the cranial neural crest. Biochem. Soc. Symp. 1996, 62:77-83.
38. Groysman M., Shoval I., Kalcheim C. A negative modulatory role for Rho and Rho-associated kinase signaling in delamination of neural crest cells. Neural Dev. 2008, 3:27.
39. Hahn-Dantona E.A., Aimes R.T., Quigley J.P. The isolation, characterization, and molecular cloning of a 75-kDa gelatinase B-like enzyme, a member of the matrix metalloproteinase (MMP) family. An avian enzyme that is MMP-9-like in its cell expression pattern but diverges from mammalian gelatinase B in sequence and biochemical properties. J. Biol. Chem. 2000, 275:40827-40838.
40. Harrison M., Abu-Elmagd M., Grocott T., Yates C., Gavrilovic J., Wheeler G.N. Matrix metalloproteinase genes in Xenopus development. Dev. Dyn. 2004, 231:214-220.
41. Hasky-Negev M., Simsa S., Tong A., Genina O., Monsonego Ornan E. Expression of matrix metalloproteinases during vascularization and ossification of normal and impaired avian growth plate. J. Anim. Sci. 2008, 86:1306-1315.
42. Holmbeck K., Bianco P., Caterina J., Yamada S., Kromer M., Kuznetsov S.A., Mankani M., Robey P.G., Poole A.R., Pidoux I., et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92.
43. Itasaki N., Bel-Vialar S., Krumlauf R. 'Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1999, 1:E203-E207.
44. Itoh T., Ikeda T., Gomi H., Nakao S., Suzuki T., Itohara S. Unaltered secretion of beta-amyloid precursor protein in gelatinase A (matrix metalloproteinase 2)-deficient mice. J. Biol. Chem. 1997, 272:22389-22392.
45. Itoh T., Tanioka M., Matsuda H., Nishimoto H., Yoshioka T., Suzuki R., Uehira M. Experimental metastasis is suppressed in MMP-9-deficient mice. Clin. Exp. Metastasis 1999, 17:177-181.
46. Jhingory S., Wu C.Y., Taneyhill L.A. Novel insight into the function and regulation of [alpha]N-catenin by Snail2 during chick neural crest cell migration. Developmental Biology 2010, 344:896.
47. Kalcheim C. Mechanisms of early neural crest development: from cell specification to migration. Int. Rev. Cytol. 2000, 200:143-196.
48. Kalcheim C., Burstyn-Cohen T. Early stages of neural crest ontogeny: formation and regulation of cell delamination. Int. J. Dev. Biol. 2005, 49:105-116.
49. Kinoh H., Sato H., Tsunezuka Y., Takino T., Kawashima A., Okada Y., Seiki M. MT-MMP, the cell surface activator of proMMP-2 (pro-gelatinase A), is expressed with its substrate in mouse tissue during embryogenesis. J. Cell Sci. 1996, 109(Pt 5):953-959.
50. Kulesa P.M., Gammill L.S. Neural crest migration: patterns, phases and signals. Dev. Biol. 2010, 344:566.
51. Leach R.M., Monsonego-Ornan E. Tibial dyschondroplasia 40years later. Poult. Sci. 2007, 86:2053-2058.
52. Le-Douarin N.M., Kalcheim C. The Neural Crest 1999, Cambridge University Press. 2nd edn.
53. Lelongt B., Trugnan G., Murphy G., Ronco P.M. Matrix metalloproteinases MMP2 and MMP9 are produced in early stages of kidney morphogenesis but only MMP9 is required for renal organogenesis in vitro. J. Cell Biol. 1997, 136:1363-1373.
54. Levin J.I., Chen J., Du M., Hogan M., Kincaid S., Nelson F.C., Venkatesan A.M., Wehr T., Zask A., DiJoseph J., et al. The discovery of anthranilic acid-based MMP inhibitors. Part 2: SAR of the 5-position and P1(1) groups. Bioorg. Med. Chem. Lett. 2001, 11:2189-2192.
55. Lohi J., Wilson C.L., Roby J.D., Parks W.C. Epilysin, a novel human matrix metalloproteinase (MMP-28) expressed in testis and keratinocytes and in response to injury. J. Biol. Chem. 2001, 276:10134-10144.
56. Malemud C.J. Matrix metalloproteinases (MMPs) in health and disease: an overview. Front. Biosci. 2006, 11:1696-1701.
57. Malemud C.J. Matrix metalloproteinases: role in skeletal development and growth plate disorders. Front. Biosci. 2006, 11:1702-1715.
58. Martignetti J.A., Aqeel A.A., Sewairi W.A., Boumah C.E., Kambouris M., Mayouf S.A., Sheth K.V., Eid W.A., Dowling O., Harris J., et al. Mutation of the matrix metalloproteinase 2 gene (MMP2) causes a multicentric osteolysis and arthritis syndrome. Nat. Genet. 2001, 28:261-265.
59. Martinez-Morales P.L., Diez del Corral R., Olivera-Martinez I., Quiroga A.C., Das R.M., Barbas J.A., Storey K.G., Morales A.V. FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. J. Cell Biol. 2011, 194:489-503.
60. McCawley L.J., Matrisian L.M. Matrix metalloproteinases: multifunctional contributors to tumor progression. Mol. Med. Today 2000, 6:149-156.
61. Miettinen P.J., Chin J.R., Shum L., Slavkin H.C., Shuler C.F., Derynck R., Werb Z. Epidermal growth factor receptor function is necessary for normal craniofacial development and palate closure. Nat. Genet. 1999, 22:69-73.
62. Monsonego-Ornan E., Adar R., Feferman T., Segev O., Yayon A. The transmembrane mutation G380R in fibroblast growth factor receptor 3 uncouples ligand-mediated receptor activation from down-regulation. Mol. Cell. Biol. 2000, 20:516-522.
63. Morrison C.J., Butler G.S., Rodriguez D., Overall C.M. Matrix metalloproteinase proteomics: substrates, targets, and therapy. Curr. Opin. Cell Biol. 2009, 21:645-653.
64. Mosig R.A., Dowling O., DiFeo A., Ramirez M.C., Parker I.C., Abe E., Diouri J., Aqeel A.A., Wylie J.D., Oblander S.A., et al. Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Hum. Mol. Genet. 2007, 16:1113-1123.
65. Mott J.D., Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 2004, 16:558-564.
66. Nagase H., Woessner J.F. Matrix metalloproteinases. J. Biol. Chem. 1999, 274:21491-21494.
67. Nakagawa S., Takeichi M. Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 1995, 121:1321-1332.
68. Nakagawa S., Takeichi M. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 1998, 125:2963-2971.
69. Nelson A.R., Fingleton B., Rothenberg M.L., Matrisian L.M. Matrix metalloproteinases: biologic activity and clinical implications. J. Clin. Oncol. 2000, 18:1135-1149.
70. Newgreen D.F., Minichiello J. Control of epitheliomesenchymal transformation. I. Events in the onset of neural crest cell migration are separable and inducible by protein kinase inhibitors. Dev. Biol. 1995, 170:91-101.
71. Nieto M.A., Bradley L.C., Wilkinson D.G. Conserved segmental expression of Krox-20 in the vertebrate hindbrain and its relationship to lineage restriction. Development 1991, (Suppl. 2):59-62.
72. Perez S.E., Cano D.A., Dao-Pick T., Rougier J.P., Werb Z., Hebrok M. Matrix metalloproteinases 2 and 9 are dispensable for pancreatic islet formation and function in vivo. Diabetes 2005, 54:694-701.
73. Perris R., Paulsson M., Bronner-Fraser M. Molecular mechanisms of avian neural crest cell migration on fibronectin and laminin. Dev. Biol. 1989, 136:222.
74. Radisky D.C. Epithelial-mesenchymal transition. J. Cell Sci. 2005, 118:4325-4326.
75. Raible D.W. Development of the neural crest: achieving specificity in regulatory pathways. Curr. Opin. Cell Biol. 2006, 18:698-703.
76. Randall L.E., Hall R.C. Temperospatial expression of matrix metalloproteinases 1, 2, 3, and 9 during early tooth development. Connect. Tissue Res. 2002, 43:205-211.
77. Reich A., Jaffe N., Tong A., Lavelin I., Genina O., Pines M., Sklan D., Nussinovitch A., Monsonego-Ornan E. Weight loading young chicks inhibits bone elongation and promotes growth plate ossification and vascularization. J. Appl. Physiol. 2005, 98:2381-2389.
78. Reponen P., Sahlberg C., Huhtala P., Hurskainen T., Thesleff I., Tryggvason K. Molecular cloning of murine 72-kDa type IV collagenase and its expression during mouse development. J. Biol. Chem. 1992, 267:7856-7862.
79. Rodriguez D., Morrison C.J., Overall C.M. Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim Biophys Acta 2010, 1803:39-54.
80. Sela-Donenfeld D., Kalcheim C. Regulation of the onset of neural crest migration by coordinated activity of BMP4 and Noggin in the dorsal neural tube. Development 1999, 126:4749-4762.
81. Sela-Donenfeld D., Kalcheim C. Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Development 2000, 127:4845-4854.
82. Sela-Donenfeld D., Kalcheim C. Localized BMP4-noggin interactions generate the dynamic patterning of noggin expression in somites. Dev. Biol. 2002, 246:311-328.
83. Sela-Donenfeld D., Kayam G., Wilkinson D. Boundary cells regulate a switch in the expression of FGF3 in hindbrain rhombomeres. BMC Dev. Biol. 2009, 9:16.
84. Shelton E.L., Yutzey K.E. Tbx20 regulation of endocardial cushion cell proliferation and extracellular matrix gene expression. Dev. Biol. 2007, 302:376-388.
85. Shimo T., Kanyama M., Wu C., Sugito H., Billings P.C., Abrams W.R., Rosenbloom J., Iwamoto M., Pacifici M., Koyama E. Expression and roles of connective tissue growth factor in Meckel's cartilage development. Dev. Dyn. 2004, 231:136-147.
86. Shoval I., Ludwig A., Kalcheim C. Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 2007, 134:491-501.
87. Simsa S., Genina O., Ornan E.M. Matrix metalloproteinase expression and localization in turkey (Meleagris gallopavo) during the endochondral ossification process. J. Anim. Sci. 2007, 85:1393-1401.
88. Simsa S., Hasdai A., Dan H., Ornan E.M. Differential regulation of MMPs and matrix assembly in chicken and turkey growth-plate chondrocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R2216-R2224.
89. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 2001, 17:463-516.
90. Taneyhill L.A. To adhere or not to adhere: the role of cadherins in neural crest development. Cell Adh. Migr. 2008, 2:223-230.
91. Taylor K.M., LaBonne C. Modulating the activity of neural crest regulatory factors. Curr. Opin. Genet. Dev. 2007, 17:326-331.
92. Thiery J.P., Boyer B., Tucker G., Gavrilovic J., Valles A.M. Adhesion mechanisms in embryogenesis and in cancer invasion and metastasis. CIBA Found. Symp. 1988, 141:48-74.
93. Tomlinson M.L., Garcia-Morales C., Abu-Elmagd M., Wheeler G.N. Three matrix metalloproteinases are required in vivo for macrophage migration during embryonic development. Mech Dev 2008.
94. Tomlinson M.L., Guan P., Morris R.J., Fidock M.D., Rejzek M., Garcia-Morales C., Field R.A., Wheeler G.N. A chemical genomic approach identifies matrix metalloproteinases as playing an essential and specific role in Xenopus melanophore migration. Chem. Biol. 2009, 16:93-104.
95. Tong A., Reich A., Genin O., Pines M., Monsonego-Ornan E. Expression of chicken 75-kDa gelatinase B-like enzyme in perivascular chondrocytes suggests its role in vascularization of the growth plate. J. Bone Miner. Res. 2003, 18:1443-1452.
96. Trainor P.A. Specification of neural crest cell formation and migration in mouse embryos. Semin. Cell Dev. Biol. 2005, 16:683-693.
97. Tzu J., Marinkovich M.P. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int. J. Biochem. Cell Biol. 2008, 40:199-214.
98. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 2003, 92:827-839.
99. Vu T.H., Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 2000, 14:2123-2133.
100. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., Shapiro S.D., Senior R.M., Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998, 93:411-422.
101. Wei S., Xu G., Bridges L.C., Williams P., White J.M., DeSimone D.W. ADAM13 induces cranial neural crest by cleaving class B ephrins and regulating Wnt signaling. Developmental Cell 2010, 19:345.
102. Weisinger K., Wilkinson G.D., Sela-Donenfeld D. Inhibition of BMPs by follistatin is required for FGF3 expression and segmental patterning of the hindbrain 2008, Developmental Biology.
103. Weizmann S., Tong A., Reich A., Genina O., Yayon A., Monsonego-Ornan E. FGF upregulates osteopontin in epiphyseal growth plate chondrocytes: implications for endochondral ossification. Matrix Biol 2005, 24:520-529.
104. Wright J., Cooley B., Duwell J., Sieber-Blum M. Migration-related changes in the cytoskeleton of cultured neural crest cells visualized by the monoclonal antibody I-5G9. J. Neurosci. Res. 1988, 21:148-154.
105. Yu Q., Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000, 14:163-176.
106. Zheng G., Lyons J.G., Tan T.K., Wang Y., Hsu T.-T., Min D., Succar L., Rangan G.K., Hu M., Henderson B.R., et al. Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-β1 in renal tubular epithelial cells. Am. J. Pathol. 2009, 175:580-591.
107. Zhou Z., Apte S.S., Soininen R., Cao R., Baaklini G.Y., Rauser R.W., Wang J., Cao Y., Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4052-4057.
108. Zuo J.-H., Zhu W., Li M.-Y., Li X.-H., Yi H., Zeng G.-Q., Wan X.-X., He Q.-Y., Li J.-H., Qu J.-Q., et al. Activation of EGFR promotes squamous carcinoma SCC10A cell migration and invasion via inducing EMT-like phenotype change and MMP-9-mediated degradation of E-cadherin. J. Cell. Biochem. 2011, 112:2508-2517.