MCF-7 cells expressing nuclear associated lysyl oxidase-like 2 (LOXL2) exhibit an epithelial-to-Mesenchymal transition (EMT) phenotype and are highly invasive in Vitro

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30000-30008

  Moon, Hee Jung ^a   Finney, Joel ^a   Xu, Li ^a,c   Moore, David ^a   Welch, Danny R ^b   Mure, Minae ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF KANSAS CANCER CENTER   (United States)

^c SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; BREAST CANCER CELLS; IN-VITRO; MCF-7 CELLS;

BIOCHEMISTRY;

BIOLOGY;

LYSYL OXIDASE LIKE 2; PROTEIN LYSINE 6 OXIDASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BREAST CANCER; BREAST METASTASIS; CANCER CELL; CARCINOGENESIS; CATALYSIS; CELL INVASION; CELL NUCLEUS; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME LOCALIZATION; ENZYME RELEASE; ENZYME STABILITY; EPITHELIAL MESENCHYMAL TRANSITION; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BREAST CANCER; CELL INVASION; EPITHELIAL-TO-MESENCHYMAL TRANSITION; LYSYL OXIDASE; LYSYL OXIDASE-LIKE 2; POST-TRANSLATIONAL MODIFICATION; SITE-DIRECTED MUTAGENESIS;

AMINO ACID OXIDOREDUCTASES; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOSYLATION; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS;

EID: 84886912773     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C113.502310     Document Type: Article

References (55)

1. Csiszar, K. (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog. Nucleic Acid Res. Mol. Biol. 70, 1-32
2. Smith-Mungo, L. I., and Kagan, H. M. (1998) Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol. 16, 387-398
3. Wang, S. X., Mure, M., Medzihradszky, K. F., Burlingame, A. L., Brown, D. E., Dooley, D. M., Smith, A. J., Kagan, H. M., and Klinman, J. P. (1996) A crosslinked cofactor in lysyl oxidase: redox function for amino acid side chains. Science 273, 1078-1084
4. Akiri, G., Sabo, E., Dafni, H., Vadasz, Z., Kartvelishvily, Y., Gan, N., Kessler, O., Cohen, T., Resnick, M., Neeman, M., and Neufeld, G. (2003) Lysyl oxidase-related protein-1 promotes tumor fibrosis and tumor progression in vivo. Cancer Res. 63, 1657-1666
5. Kirschmann, D. A., Seftor, E. A., Fong, S. F., Nieva, D. R., Sullivan, C. M., Edwards, E. M., Sommer, P., Csiszar, K., and Hendrix, M. J. (2002) A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res. 62, 4478-4483
6. Baker, A. M., Bird, D., Lang, G., Cox, T. R., and Erler, J. T. (2013) Lysyl oxidase enzymatic function increases stiffness to drive colorectal cancer progression through FAK. Oncogene 32, 1863-1868
7. Erler, J. T., Bennewith, K. L., Cox, T. R., Lang, G., Bird, D., Koong, A., Le, Q. T., and Giaccia, A. J. (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15, 35-44
8. Kass, L., Erler, J. T., Dembo, M., and Weaver, V. M. (2007) Mammary epithelial cell: influence of extracellular matrix composition and organization during development and tumorigenesis. Int. J. Biochem. Cell Biol. 39, 1987-1994
9. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W., Yamauchi, M., Gasser, D. L., and Weaver, V. M. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906
10. Barker, H. E., Chang, J., Cox, T. R., Lang, G., Bird, D., Nicolau, M., Evans, H. R., Gartland, A., and Erler, J. T. (2011) LOXL2-mediated matrix remodeling in metastasis and mammary gland involution. Cancer Res. 71, 1561-1572
11. Payne, S. L., Fogelgren, B., Hess, A. R., Seftor, E. A., Wiley, E. L., Fong, S. F., Csiszar, K., Hendrix, M. J., and Kirschmann, D. A. (2005) Lysyl oxidase regulates breast cancer cell migration and adhesion through a hydrogen peroxide-mediated mechanism. Cancer Res. 65, 11429-11436
12. Peng, L., Ran, Y. L., Hu, H., Yu, L., Liu, Q., Zhou, Z., Sun, Y. M., Sun, L. C., Pan, J., Sun, L. X., Zhao, P., and Yang, Z. H. (2009) Secreted LOXL2 is a novel therapeutic target that promotes gastric cancer metastasis via the Src/FAK pathway. Carcinogenesis 30, 1660-1669
13. Barry-Hamilton, V., Spangler, R., Marshall, D., McCauley, S., Rodriguez, H. M., Oyasu, M., Mikels, A., Vaysberg, M., Ghermazien, H., Wai, C., Garcia, C. A., Velayo, A. C., Jorgensen, B., Biermann, D., Tsai, D., Green, J., Zaffryar-Eilot, S., Holzer, A., Ogg, S., Thai, D., Neufeld, G., Van Vlasselaer, P., and Smith, V. (2010) Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat. Med. 16, 1009-1017
14. Cano, A., Santamaría, P. G., and Moreno-Bueno, G. (2012) LOXL2 in epithelial cell plasticity and tumor progression. Future Oncol. 8, 1095-1108
15. Moreno-Bueno, G., Salvador, F., Martín, A., Florist́n, A., Cuevas, E. P., Santos, V., Montes, A., Morales, S., Castilla, M. A., Rojo-Sebastín, A., Martínez, A., Hardisson, D., Csiszar, K., Portillo, F., Peinado, H., Palacios, J., and Cano, A. (2011) Lysyl oxidase-like 2 (LOXL2), a new regulator of cell polarity required for metastatic dissemination of basal-like breast carcinomas. EMBO Mol. Med. 3, 528-544
16. Peinado, H., Moreno-Bueno, G., Hardisson, D., Pérez-Gómez, E., Santos, V., Mendiola, M., de Diego, J. I., Nistal, M., Quintanilla, M., Portillo, F., and Cano, A. (2008) Lysyl oxidase-like 2 as a new poor prognosis marker of squamous cell carcinomas. Cancer Res. 68, 4541-4550
17. Peinado, H., Del Carmen Iglesias-de la Cruz, M., Olmeda, D., Csiszar, K., Fong, K. S., Vega, S., Nieto, M. A., Cano, A., and Portillo, F. (2005) A molecular role for lysyl oxidase-like 2 enzyme in Snail regulation and tumor progression. EMBO J. 24, 3446-3458
18. Herranz, N., Dave, N., Millanes-Romero, A., Morey, L., Díaz, V. M., Lórenz-Fonfría, V., Gutierrez-Gallego, R., Jerónimo, C., Di Croce, L., García de Herreros, A., and Peiró, S. (2012) Lysyl oxidase-like 2 deaminates lysine 4 in histone H3. Mol. Cell 46, 369-376
19. Xu, L., Go, E. P., Finney, J., Moon, H., Lantz, M., Rebecchi, K., Desaire, H., and Mure, M. (2013) Post-translational modifications of recombinant human lysyl oxidase-like 2 (rhLOXL2) secreted from Drosophila S2 cells. J. Biol. Chem. 288, 5357-5363
20. Palamakumbura, A. H., and Trackman, P. C. (2002) A fluorometric assay for detection of lysyl oxidase enzyme activity in biological samples. Anal. Biochem. 300, 245-251
21. Hollosi, P., Yakushiji, J. K., Fong, K. S., Csiszar, K., and Fong, S. F. (2009) Lysyl oxidase-like 2 promotes migration in noninvasive breast cancer cells but not in normal breast epithelial cells. Int. J. Cancer 125, 318-327
22. Rebecchi, K. R., Go, E. P., Xu, L., Woodin, C. L., Mure, M., and Desaire, H. (2011) A general protease digestion procedure for optimal protein sequence coverage and post-translational modifications analysis of recombinant glycoproteins: application to the characterization of human lysyl oxidase-like 2 glycosylation. Anal. Chem. 83, 8484-8491
23. Bence, M., and Sahin-Tóth, M. (2011) Asparagine-linked glycosylation of human chymotrypsin C is required for folding and secretion but not for enzyme activity. FEBS J. 278, 4338-4350
24. Petrecca, K., Atanasiu, R., Akhavan, A., and Shrier, A. (1999) N-Linked glycosylation sites determine HERG channel surface membrane expression. J. Physiol. 515, 41-48
25. Stanley, P., Schachter, H., and Taniguchi, N. (2009) Chapter 8, N-Glycans. in Essentials of Glycobiology (Varki, A., Cummings, R., Esko, J., Freeze, H. H., Stanley, P., Bertozzi, C., Hart, G., and Etzler, M. eds), Second Ed., pp. 101-114, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
26. Polevoda, B., and Sherman, F. (2003) N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J. Mol. Biol. 325, 595-622
27. Rodriguez, H. M., Vaysberg, M., Mikels, A., McCauley, S., Velayo, A. C., Garcia, C., and Smith, V. (2010) Modulation of lysyl oxidase-like 2 enzymatic activity by an allosteric antibody inhibitor. J. Biol. Chem. 285, 20964-20974
28. Tang, S. S., Trackman, P. C., and Kagan, H. M. (1983) Reaction of aortic lysyl oxidase with β-aminopropionitrile. J. Biol. Chem. 258, 4331-4338
29. Bollinger, J. A., Brown, D. E., and Dooley, D. M. (2005) The formation of lysine tyrosylquinone (LTQ) is a self-processing reaction. Expression and characterization of a Drosophila lysyl oxidase. Biochemistry 44, 11708-11714
30. Tu, B. P., and Weissman, J. S. (2004) Oxidative protein folding in eukaryotes: mechanisms and consequences. J. Cell Biol. 164, 341-346
31. Moore, R. H., Spies, M. A., Culpepper, M. B., Murakawa, T., Hirota, S., Okajima, T., Tanizawa, K., and Mure, M. (2007) Trapping of a dopaquinone intermediate in the TPQ cofactor biogenesis in a copper-containing amine oxidase from Arthrobacter globiformis. J. Am. Chem. Soc. 129, 11524-11534
32. Mure, M., Wang, S. X., and Klinman, J. P. (2003) Synthesis and characterization of model compounds of the lysine tyrosyl quinone cofactor of lysyl oxidase. J. Am. Chem. Soc. 125, 6113-6125
33. Tang, C., and Klinman, J. P. (2001) The catalytic function of bovine lysyl oxidase in the absence of copper. J. Biol. Chem. 276, 30575-30578
34. Martin-Belmonte, F., and Perez-Moreno, M. (2012) Epithelial cell polarity, stem cells and cancer. Nat. Rev. Cancer 12, 23-38
35. Batlle, E., Sancho, E., Francí, C., Domínguez, D., Monfar, M., Baulida, J., and García De Herreros, A. (2000) The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89
36. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000) The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83
37. Dhasarathy, A., Kajita, M., and Wade, P. A. (2007) The transcription factor Snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-α. Mol. Endocrinol. 21, 2907-2918
38. Martínez-Estrada, O. M., Cullerés, A., Soriano, F. X., Peinado, H., Bolós, V., Martínez, F. O., Reina, M., Cano, A., Fabre, M., and Vilaró, S. (2006) The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 394, 449-457
39. Stanisavljevic, J., Porta-de-la-Riva, M., Batlle, R., de Herreros, A. G., and Baulida, J. (2011) The p65 subunit of NF-k B and PARP1 assist Snail1 in activating fibronectin transcription. J. Cell Sci. 124, 4161-4171
40. Lin, C. Y., Tsai, P. H., Kandaswami, C. C., Lee, P. P., Huang, C. J., Hwang, J. J., and Lee, M. T. (2011) Matrix metalloproteinase-9 cooperates with transcription factor Snail to induce epithelial-mesenchymal transition. Cancer Sci. 102, 815-827
41. Mendez, M. G., Kojima, S., and Goldman, R. D. (2010) Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J. 24, 1838-1851
42. Olmeda, D., Jord́, M., Peinado, H., Fabra, A., and Cano, A. (2007) Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene 26, 1862-1874
43. Peinado, H., Portillo, F., and Cano, A. (2005) Switching on-off Snail: LOXL2 versus GSK3β. Cell Cycle 4, 1749-1752
44. Kim, E. S., Kim, J. S., Kim, S. G., Hwang, S., Lee, C. H., and Moon, A. (2011) Sphingosine 1-phosphate regulates matrix metalloproteinase-9 expression and breast cell invasion through S1P3-Gαq coupling. J. Cell Sci. 124, 2220-2230
45. Miyazawa, Y., Uekita, T., Ito, Y., Seiki, M., Yamaguchi, H., and Sakai, R. (2013) CDCP1 regulates the function of MT1-MMP and invadopodiamediated invasion of cancer cells. Mol. Cancer Res. 11, 628-637
46. Toth, M., Chvyrkova, I., Bernardo, M. M., Hernandez-Barrantes, S., and Fridman, R. (2003) Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes. Biochem. Biophys. Res. Commun. 308, 386-395
47. Miyoshi, A., Kitajima, Y., Sumi, K., Sato, K., Hagiwara, A., Koga, Y., and Miyazaki, K. (2004) Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br. J. Cancer 90, 1265-1273
48. Shields, M. A., Dangi-Garimella, S., Krantz, S. B., Bentrem, D. J., and Munshi, H. G. (2011) Pancreatic cancer cells respond to type I collagen by inducing Snail expression to promote membrane type 1 matrix metalloproteinase- dependent collagen invasion. J. Biol. Chem. 286, 10495-10504
49. Saad, S., Gottlieb, D. J., Bradstock, K. F., Overall, C. M., and Bendall, L. J. (2002) Cancer cell-associated fibronectin induces release of matrix metalloproteinase- 2 from normal fibroblasts. Cancer Res. 62, 283-289
50. Welm, B., Mott, J., and Werb, Z. (2002) Developmental biology: vasculogenesis is a wreck without RECK. Curr. Biol. 12, R209-211
51. Sodek, K. L., Ringuette, M. J., and Brown, T. J. (2007) MT1-MMP is the critical determinant of matrix degradation and invasion by ovarian cancer cells. Br. J. Cancer 97, 358-367
52. Sanz-Moreno, V., and Marshall, C. J. (2010) The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr. Opin. Cell Biol. 22, 690-696
53. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Bröcker, E. B., and Friedl, P. (2003) Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160, 267-277
54. Poincloux, R., Collin, O., Liźrraga, F., Romao, M., Debray, M., Piel, M., and Chavrier, P. (2011) Contractility of the cell rear drives invasion of breast tumor cells in 3D Matrigel. Proc. Natl. Acad. Sci. U.S.A. 108, 1943-1948
55. Terry, S. J., Elbediwy, A., Zihni, C., Harris, A. R., Bailly, M., Charras, G. T., Balda, M. S., and Matter, K. (2012) Stimulation of cortical myosin phosphorylation by p114RhoGEF drives cell migration and tumor cell invasion. PLoS One 7, e50188