Matrix metalloproteinase (MMP)-9 induced by Wnt signaling increases the proliferation and migration of embryonic neural stem cells at low O2 levels

Journal of Biological Chemistry

Volumn 286, Issue 20, 2011, Pages 17649-17657

  Ingraham, Christopher A ^a   Park, Gabriel C ^a   Makarenkova, Helen P ^a   Crossin, Kathryn L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX MOLECULES; HYPOXIA-INDUCIBLE TRANSCRIPTION FACTORS; MATRIX METALLOPROTEINASES; MOLECULAR CHANGES; MOLECULAR MECHANISM; NEURAL STEM CELL; QUANTITATIVE RT-PCR; WNT PATHWAY; WNT SIGNALING;

ADHESION; CELL ADHESION; ENZYME ACTIVITY; ENZYME INHIBITION; NUCLEIC ACIDS; SIGNALING; STEM CELLS; TISSUE; TRANSCRIPTION FACTORS;

CELL CULTURE;

BETA CATENIN; GELATINASE B; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELL ADHESION; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MATRIX METALLOPROTEINASE 9; NEURAL STEM CELLS; OXYGEN; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; WNT PROTEINS;

RATTUS;

EID: 79955975393     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.229427     Document Type: Article

References (97)

1. Tuuli, M. G., Longtine, M. S., and Nelson, D. M. (2011) Placenta 32, Suppl. 2, S109-S118
2. Halliwell, B. (2003) FEBS Lett. 540, 3-6
3. Millman, J. R., Tan, J. H., and Colton, C. K. (2009) Curr. Opin. Organ. Transplant. 14, 694-700
4. Dirken, M. N., and Heemstra, H. (1948) Q. J. Exp. Physiol. 34, 193-211
5. Panchision, D. M. (2009) J. Cell. Physiol. 220, 562-568
6. Horng, C. T., Liu, C. C., Wu, D. M., Wu, Y. C., Chen, J. T., Chang, C. J., and Tsai, M. L. (2008) Aviat. Space Environ. Med. 79, 666-669
7. Ereciñska, M., and Silver, I. A. (2001) Respir. Physiol. 128, 263-276
8. Hoffman, C. E., Clark, R. T., Jr., and Brown, E. B., Jr. (1946) Am. J. Physiol. 145, 685-692
9. Vieira, H. L., Alves, P. M., and Vercelli, A. (2011) Prog. Neurobiol. 93, 444-455
10. Simon, M. C., and Keith, B. (2008) Nat. Rev. Mol. Cell Biol. 9, 285-296
11. Lin, Q., Kim, Y., Alarcon, R. M., and Yun, Z. (2008) Gene Regul. Syst. Biol. 2, 43-51
12. Chen, H. L., Pistollato, F., Hoeppner, D. J., Ni, H. T., McKay, R. D., and Panchision, D. M. (2007) Stem Cells 25, 2291-2301
13. Tsatmali, M., Walcott, E. C., Makarenkova, H., and Crossin, K. L. (2006) Mol. Cell. Neurosci. 33, 345-357
14. Studer, L., Csete, M., Lee, S. H., Kabbani, N., Walikonis, J., Wold, B., and McKay, R. (2000) J. Neurosci. 20, 7377-7383
15. Tsatmali, M., Walcott, E. C., and Crossin, K. L. (2005) Brain Res. 1040, 137-150
16. Horie, N., So, K., Moriya, T., Kitagawa, N., Tsutsumi, K., Nagata, I., and Shinohara, K. (2008) Cell Mol. Neurobiol. 28, 833-845
17. Milosevic, J., Adler, I., Manaenko, A., Schwarz, S. C., Walkinshaw, G., Arend, M., Flippin, L. A., Storch, A., and Schwarz, J. (2009) Neurotox. Res. 15, 367-380
18. Pistollato, F., Chen, H. L., Schwartz, P. H., Basso, G., and Panchision, D. M. (2007) Mol. Cell. Neurosci. 35, 424-435
19. Zhao, T., Zhang, C. P., Liu, Z. H., Wu, L. Y., Huang, X., Wu, H. T., Xiong, L., Wang, X., Wang, X. M., Zhu, L. L., and Fan, M. (2008) FEBS J 275, 1824-1834
20. Zhou, L., and Miller, C. A. (2006) Neurodegener. Dis. 3, 50-55
21. Chen, X., Tian, Y., Yao, L., Zhang, J., and Liu, Y. (2010) Neuroscience 165, 705-714
22. Rodrigues, C. A., Diogo, M. M., da Silva, C. L., and Cabral, J. M. (2010) Biotechnol. Bioeng. 106, 260-270
23. Santilli, G., Lamorte, G., Carlessi, L., Ferrari, D., Rota Nodari, L., Binda, E., Delia, D., Vescovi, A. L., and De Filippis, L. (2010) PLoS one 5, e8575
24. Mazumdar, J., O'Brien, W. T., Johnson, R. S., LaManna, J. C., Chavez, J. C., Klein, P. S., and Simon, M. C. (2010) Nat. Cell Biol. 12, 1007-1013
25. Clarke, L., and van der Kooy, D. (2009) Stem Cells 27, 1879-1886
26. Mohyeldin, A., Garzón-Muvdi, T., and Quiñones-Hinojosa, A. (2010) Cell Stem Cell. 7, 150-161
27. Harrison, J. F., and Haddad, G. G. (2011) Annu. Rev. Physiol. 73, 95-113
28. Jiang, B. H., Semenza, G. L., Bauer, C., and Marti, H. H. (1996) Am. J. Physiol. 271, C1172-C1180
29. Wenger, R. H., and Gassmann, M. (1997) Biol. Chem. 378, 609-616
30. Zádori, A., Agoston, V. A., Demeter, K., Hádinger, N., Várady, L., Köhídi, T., Göbl, A., Nagy, Z., and Madarász, E. (2011) Exp. Neurol. 227, 136-148
31. Harms, K. M., Li, L., and Cunningham, L. A. (2010) PLoS one 5, e9767
32. Giese, A. K., Frahm, J., Hübner, R., Luo, J., Wree, A., Frech, M. J., Rolfs, A., and Ortinau, S. (2010) BMC Cell Biol. 11, 94
33. Zhang, X., Zhou, K., Wang, R., Cui, J., Lipton, S. A., Liao, F. F., Xu, H., and Zhang, Y. W. (2007) J. Biol. Chem. 282, 10873-10880
34. Kim, T. S., Misumi, S., Jung, C. G., Masuda, T., Isobe, Y., Furuyama, F., Nishino, H., and Hida, H. (2008) J. Neurosci. Res. 86, 2353-2362
35. Noles, S. R., and Chenn, A. (2007) Mol. Cell. Neurosci. 35, 549-558
36. Wexler, E. M., Geschwind, D. H., and Palmer, T. D. (2008) Mol. Psychiatry 13, 285-292
37. Zhang, X., Gaspard, J. P., and Chung, D. C. (2001) Cancer Res. 61, 6050-6054
38. Wu, B., Crampton, S. P., and Hughes, C. C. (2007) Immunity 26, 227-239
39. Newby, D., Marks, L., and Lyall, F. (2005) Placenta 26, 353-357
40. Ema, M., Taya, S., Yokotani, N., Sogawa, K., Matsuda, Y., and Fujii- Kuriyama, Y. (1997) Proc. Natl. Acad. Sci. U.S.A. 94, 4273-4278
41. Maxwell, P. H., Dachs, G. U., Gleadle, J. M., Nicholls, L. G., Harris, A. L., Stratford, I. J., Hankinson, O., Pugh, C. W., and Ratcliffe, P. J. (1997) Proc. Natl. Acad. Sci. U.S.A. 94, 8104-8109
42. Millauer, B., Wizigmann-Voos, S., Schnürch, H., Martinez, R., Møller, N. P., Risau, W., and Ullrich, A. (1993) Cell 72, 835-846
43. Carmichael, J., DeGraff, W. G., Gazdar, A. F., Minna, J. D., and Mitchell, J. B. (1987) Cancer Res. 47, 936-942
44. Mosmann, T. (1983) J. Immunol. Methods 65, 55-63
45. Gerlier, D., and Thomasset, N. (1986) J. Immunol. Methods 94, 57-63
46. van de Loosdrecht, A. A., Beelen, R. H., Ossenkoppele, G. J., Broekhoven, M. G., and Langenhuijsen, M. M. (1994) J. Immunol. Methods 174, 311-320
47. Jabbar, S. A., Twentyman, P. R., and Watson, J. V. (1989) Br. J. Cancer 60, 523-528
48. Pagliacci, M. C., Spinozzi, F., Migliorati, G., Fumi, G., Smacchia, M., Grignani, F., Riccardi, C., and Nicoletti, I. (1993) Eur. J. Cancer 29A, 1573-1577
49. York, J. L., Maddox, L. C., Zimniak, P., McHugh, T. E., and Grant, D. F. (1998) BioTechniques 25, 622-624, 626-628
50. Zhang, Z. D., and Cox, G. (1996) Biochem. Mol. Biol. Int. 38, 431-436
51. Fantin, V. R., St-Pierre, J., and Leder, P. (2006) Cancer Cell 9, 425-434
52. Le, A., Cooper, C. R., Gouw, A. M., Dinavahi, R., Maitra, A., Deck, L. M., Royer, R. E., Vander Jagt, D. L., Semenza, G. L., and Dang, C. V. (2010) Proc. Natl. Acad. Sci. U.S.A. 107, 2037-2042
53. Hernández-Guillamon, M., Delgado, P., Ortega, L., Pares, M., Rosell, A., García-Bonilla, L., Fernández-Cadenas, I., Borrell-Pagès, M., Boada, M., and Montaner, J. (2009) J. Neurosci. Res. 87, 2115-2125
54. Kim, D. H., Lilliehook, C., Roides, B., Chen, Z., Chang, M., Mobashery, S., and Goldman, S. A. (2008) J. Neurosci. 28, 208-216
55. Liu, H., Kim, Y., Chattopadhyay, S., Shubayev, I., Dolkas, J., and Shubayev, V. I. (2010) J. Neuropathol. Exp. Neurol. 69, 386-395
56. Zhang, Y., Klassen, H. J., Tucker, B. A., Perez, M. T., and Young, M. J. (2007) J. Neurosci. 27, 4499-4506
57. Levin, J. I., Chen, J., Du, M., Hogan, M., Kincaid, S., Nelson, F. C., Venkatesan, A. M., Wehr, T., Zask, A., DiJoseph, J., Killar, L. M., Skala, S., Sung, A., Sharr, M., Roth, C., Jin, G., Cowling, R., Mohler, K. M., Black, R. A., March, C. J., and Skotnicki, J. S. (2001) Bioorg. Med. Chem. Lett. 11, 2189-2192
58. Fedi, P., Bafico, A., Nieto Soria, A., Burgess, W. H., Miki, T., Bottaro, D. P., Kraus, M. H., and Aaronson, S. A. (1999) J. Biol. Chem. 274, 19465-19472
59. Nelson, W. J., and Nusse, R. (2004) Science 303, 1483-1487
60. Blake, S. M., Strasser, V., Andrade, N., Duit, S., Hofbauer, R., Schneider, W. J., and Nimpf, J. (2008) EMBO J. 27, 3069-3080
61. Lu, Z., and Kipnis, J. (2010) FASEB J. 24, 1925-1934
62. Meng, H., Zhang, X., Hankenson, K. D., and Wang, M. M. (2009) J. Biol. Chem. 284, 7866-7874
63. Brahimi-Horn, M. C., Bellot, G., and Pouyssegur, J. (2011) Curr. Opin. Genet. Dev. 21, 67-72
64. Webster, K. A. (2003) J. Exp. Biol. 206, 2911-2922
65. Kang, S. S., Kook, J. H., Hwang, S., Park, S. H., Nam, S. C., and Kim, J. K. (2008) Brain Res. 1228, 20-26
66. Wang, L., Zhang, Z. G., Zhang, R. L., Gregg, S. R., Hozeska-Solgot, A., LeTourneau, Y., Wang, Y., and Chopp, M. (2006) J. Neurosci. 26, 5996-6003
67. Barkho, B. Z., Munoz, A. E., Li, X., Li, L., Cunningham, L. A., and Zhao, X. (2008) Stem Cells 26, 3139-3149
68. Tonti, G. A., Mannello, F., Cacci, E., and Biagioni, S. (2009) Int. J. Dev. Biol. 53, 1-17
69. Cañete Soler, R., Gui, Y. H., Linask, K. K., and Muschel, R. J. (1995) Brain Res. Dev. Brain Res. 88, 37-52
70. Sternlicht, M. D., and Werb, Z. (2001) Annu. Rev. Cell Dev. Biol. 17, 463-516
71. Björklund, M., and Koivunen, E. (2005) Biochim. Biophys. Acta 1755, 37-69
72. Yong, V. W., Power, C., Forsyth, P., and Edwards, D. R. (2001) Nat. Rev. Neurosci. 2, 502-511
73. Agrawal, S. M., Lau, L., and Yong, V. W. (2008) Semin. Cell Dev. Biol. 19, 42-51
74. Novak, A., and Dedhar, S. (1999) Cell. Mol. Life Sci. 56, 523-537
75. Ethell, I. M., and Ethell, D. W. (2007) J. Neurosci. Res. 85, 2813-2823
76. Michaluk, P., Kolodziej, L., Mioduszewska, B., Wilczynski, G. M., Dzwonek, J., Jaworski, J., Gorecki, D. C., Ottersen, O. P., and Kaczmarek, L. (2007) J. Biol. Chem. 282, 16036-16041
77. Haynes, L. W. (1988) Mol. Neurobiol. 2, 263-289
78. Kresse, H., and Schönherr, E. (2001) J. Cell. Physiol. 189, 266-274
79. Vlodavsky, I., Miao, H. Q., Medalion, B., Danagher, P., and Ron, D. (1996) Cancer Metastasis Rev. 15, 177-186
80. Kenagy, R. D., Hart, C. E., Stetler-Stevenson, W. G., and Clowes, A. W. (1997) Circulation 96, 3555-3560
81. Candela, M. E., Geraci, F., Turturici, G., Taverna, S., Albanese, I., and Sconzo, G. (2010) J. Cell. Physiol. 224, 144-151
82. Ardi, V. C., Van den Steen, P. E., Opdenakker, G., Schweighofer, B., Deryugina, E. I., and Quigley, J. P. (2009) J. Biol. Chem. 284, 25854-25866
83. Higgins, S., Wong, S. H., Richner, M., Rowe, C. L., Newgreen, D. F., Werther, G. A., and Russo, V. C. (2009) Endocrinology 150, 4044-4055
84. Cho, A., and Reidy, M. A. (2002) Circ. Res. 91, 845-851
85. Toledo, E. M., Colombres, M., and Inestrosa, N. C. (2008) Prog. Neurobiol. 86, 281-296
86. Li, H. G., Ren, Y. M., Guo, S. C., Cheng, L., Wang, D. P., Yang, J., Chang, Z. J., and Zhao, X. Q. (2009) J. Exp. Zool. A. Ecol. Genet. Physiol. 311, 134-141
87. Yi, X., Liang, Y., Huerta-Sanchez, E., Jin, X., Cuo, Z. X., Pool, J. E., Xu, X., Jiang, H., Vinckenbosch, N., Korneliussen, T. S., Zheng, H., Liu, T., He, W., Li, K., Luo, R., Nie, X., Wu, H., Zhao, M., Cao, H., Zou, J., Shan, Y., Li, S., Yang, Q., Asan, Ni, P., Tian, G., Xu, J., Liu, X., Jiang, T., Wu, R., Zhou, G., Tang, M., Qin, J., Wang, T., Feng, S., Li, G., Huasang, Luosang, J., Wang, W., Chen, F., Wang, Y., Zheng, X., Li, Z., Bianba, Z., Yang, G., Wang, X., Tang, S., Gao, G., Chen, Y., Luo, Z., Gusang, L., Cao, Z., Zhang, Q., Ouyang, W., Ren, X., Liang, H., Zheng, H., Huang, Y., Li, J., Bolund, L., Kristiansen, K., Li, Y., Zhang, Y., Zhang, X., Li, R., Li, S., Yang, H., Nielsen, R., Wang, J., and Wang, J. (2010) Science 329, 75-78
88. Peng, Y., Yang, Z., Zhang, H., Cui, C., Qi, X., Luo, X., Tao, X., Wu, T., Ouzhuluobu, Basang, Ciwangsangbu, Danzengduojie, Chen, H., Shi, H., and Su, B. (2011) Mol. Biol. Evol. 28, 1075-1081
89. Shams, I., Avivi, A., and Nevo, E. (2004) Proc. Natl. Acad. Sci. U.S.A. 101, 9698-9703
90. Shams, I., Nevo, E., and Avivi, A. (2005) FASEB J. 19, 307-309
91. Storz, J. F., Scott, G. R., and Cheviron, Z. A. (2010) J. Exp. Biol. 213, 4125-4136
92. Bigham, A., Bauchet, M., Pinto, D., Mao, X., Akey, J. M., Mei, R., Scherer, S. W., Julian, C. G., Wilson, M. J., Lopez Herraez, D., Brutsaert, T., Parra, E. J., Moore, L. G., and Shriver, M. D. (2010) PLoS Genet. 6, e1001116
93. Simonson, T. S., Yang, Y., Huff, C. D., Yun, H., Qin, G., Witherspoon, D. J., Bai, Z., Lorenzo, F. R., Xing, J., Jorde, L. B., Prchal, J. T., and Ge, R. (2010) Science 329, 72-75
94. Zhou, D., Xue, J., Chen, J., Morcillo, P., Lambert, J. D., White, K. P., and Haddad, G. G. (2007) PLoS One 2, e490
95. Zhou, D., Visk, D. W., and Haddad, G. G. (2009) Pediatr. Res. 66, 239-247
96. Loenarz, C., Coleman, M. L., Boleininger, A., Schierwater, B., Holland, P. W., Ratcliffe, P. J., and Schofield, C. J. (2011) EMBO Rep. 12, 63-70
97. Rytkönen, K. T., and Storz, J. F. (2011) EMBO Rep. 12, 3-4