Structural changes in intermediate filament networks alter the activity of insulin-degrading enzyme

FASEB Journal

Volumn 23, Issue 11, 2009, Pages 3734-3742

  Chou, Ying Hao ^a   Kuo, Wen Liang ^b   Rosner, Marsha Rich ^c   Tang, Wei Jen ^c   Goldman, Robert D ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b SECTION OF HEMATOLOGY ONCOLOGY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Cytoskeleton; Metalloprotease; Phosphorylation

Indexed keywords

BRADYKININ; INSULINASE; NESTIN; SERINE; VIMENTIN;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; INSULIN DEGRADATION; INTERMEDIATE FILAMENT; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; INSULYSIN; INTERMEDIATE FILAMENT PROTEINS; INTERMEDIATE FILAMENTS; NERVE TISSUE PROTEINS; PHOSPHORYLATION; RATS; VIMENTIN;

EID: 70350532859     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-137455     Document Type: Article

References (56)

1. Omary, M. B., Ku, N. O., Tao, G. Z., Toivola, D. M., and Liao, J. (2006) "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem. Sci. 31, 383-394
2. Eckes, B., Colucci-Guyon, E., Smola, H., Nodder, S., Babinet, C., Krieg, T., and Martin, P. (2000) Impaired wound healing in embryonic and adult mice lacking vimentin. J. Cell Sci. 113, 2455-2462 (Pubitemid 30601362)
3. Nieminen, M., Henttinen, T., Merinen, M., Marttila-Ichihara, F., Eriksson, J. E., and Jalkanen, S. (2006) Vimentin function in lymphocyte adhesion and transcellular migration. Nat. Cell Biol. 8, 156-162
4. Phua, D. C., Humbert, P. O., and Hunziker, W. (2009) Vimentin regulates Scribble activity by protecting it from proteasomal degradation. Mol. Biol. Cell 12, 2841-2855
5. Caulin, C., Ware, C. F., Magin, T. M., and Oshima, R. G. (2000) Keratin-dependent, epithelial resistance to tumor necrosis factor-induced apoptosis. J. Cell Biol. 149, 17-22 (Pubitemid 30196695)
6. Inada, H., Izawa, I., Nishizawa, M., Fujita, E., Kiyono, T., Takahashi, T., Momoi, T., and Inagaki, M. (2001) Keratin attenuates tumor necrosis factor-induced cytotoxicity through association with TRADD. J Cell Biol. 155, 415-426 (Pubitemid 34289332)
7. Kim, S., Wong, P., and Coulombe, P. A. (2006) A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 441, 362-365 (Pubitemid 44050202)
8. Omary, M. B., and Ku, N. O. (2006) Cell biology: skin care by keratins. Nature 441, 296-297
9. Chang, L., and Goldman, R. D. (2004) Intermediate filaments mediate cytoskeletal crosstalk. Nat. Rev. Mol. Cell. Biol. 5, 601-613 (Pubitemid 39025061)
10. Chou, Y. H., Flitney, F. W., Chang, L., Mendez, M., Grin, B., and Goldman, R. D. (2007) The motility and dynamic properties of intermediate filaments and their constituent proteins. Exp. Cell. Res. 313, 2236-2243 (Pubitemid 46842986)
11. Helfand, B. T., Chou, Y. H., Shumaker, D. K., and Goldman, R. D. (2005) Intermediate filament proteins participate in signal transduction. Trends Cell Biol. 15, 568-570 (Pubitemid 41619419)
12. Perlson, E., Hanz, S., Ben-Yaakov, K., Segal-Ruder, Y., Seger, R., and Fainzilber, M. (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45, 715-726 (Pubitemid 40320706)
13. Ivaska, J., Vuoriluoto, K., Huovinen, T., Izawa, I., Inagaki, M., and Parker, P. J. (2005) PKCå-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J. 24, 3834-3845 (Pubitemid 41637991)
14. Lendahl, U., Zimmerman, L. B., and McKay, R. D. (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595 (Pubitemid 20083815)
15. Sejersen, T., and Lendahl, U. (1993) Transient expression of the intermediate filament nestin during skeletal muscle development. J. Cell Sci. 106, 1291-1300 (Pubitemid 24018414)
16. Kawaguchi, A., Miyata, T., Sawamoto, K., Takashita, N., Murayama, A., Akamatsu, W., Ogawa, M., Okabe, M., Tano, Y., Goldman, S. A., and Okano, H. (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol. Cell. Neurosci. 17, 259-273 (Pubitemid 32176484)
17. Mignone, J. L., Kukekov, V., Chiang, A. S., Steindler, D., and Enikolopov, G. (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 469, 311-324 (Pubitemid 38140640)
18. Dahlstrand, J., Collins, V. P., and Lendahl, U. (1992) Expression of the class VI intermediate filament nestin in human central nervous system tumors. Cancer Res. 52, 5334-5341
19. Rutka, J. T., Ivanchuk, S., Mondal, S., Taylor, M., Sakai, K., Dirks, P., Jun, P., Jung, S., Becker, L. E., and Ackerley, C. (1999) Co-expression of nestin and vimentin intermediate filaments in invasive human astrocytoma cells. Int. J. Dev. Neurosci. 17, 503-515 (Pubitemid 29421837)
20. Sultana, S., Zhou, R., Sadagopan, M. S., and Skalli, O. (1998) Effects of growth factors and basement membrane proteins on the phenotype of U-373 MG glioblastoma cells as determined by the expression of intermediate filament proteins. Am. J. Pathol. 153, 1157-1168 (Pubitemid 28465839)
21. Thomas, S. K., Messam, C. A., Spengler, B. A., Biedler, J. L., and Ross, R. A. (2004) Nestin is a potential mediator of malignancy in human neuroblastoma cells. J. Biol. Chem. 279, 27994-27999
22. Tohyama, T., Lee, V. M., Rorke, L. B., Marvin, M., McKay, R. D., and Trojanowski, J. Q. (1992) Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab. Invest. J. Tech. Methods Pathol. 66, 303-313
23. Duckworth, W. C., Bennett, R. G., and Hamel, F. G. (1998) Insulin degradation: progress and potential. Endocrine Rev. 19, 608-624
24. Farris, W., Mansourian, S., Chang, Y., Lindsley, L., Eckman, E. A., Frosch, M. P., Eckman, C. B., Tanzi, R. E., Selkoe, D. J., and Guenette, S. (2003) Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proc. Natl. Acad. Sci. U. S. A. 100, 4162-4167 (Pubitemid 36418174)
25. Miller, B. C., Eckman, E. A., Sambamurti, K., Dobbs, N., Chow, K. M., Eckman, C. B., Hersh, L. B., and Thiele, D. L. (2003) Amyloid-beta peptide levels in brain are inversely correlated with insulysin activity levels in vivo. Proc. Natl. Acad. Sci. U. S. A. 100, 6221-6226 (Pubitemid 36576957)
26. Li, Q., Ali, M. A., and Cohen, J. I. (2006) Insulin degrading enzyme is a cellular receptor mediating varicella-zoster virus infection and cell-to-cell spread. Cell 127, 305-316 (Pubitemid 44572380)
27. Kurochkin, I. V. (2001) Insulin-degrading enzyme: embarking on amyloid destruction. Trends Biochem. Sci. 26, 421-425
28. Malito, E., Hulse, R. E., and Tang, W. J. (2008) Amyloid beta-degrading cryptidases: insulin degrading enzyme, presequence peptidase, and neprilysin. Cell. Mol. Life Sci. 65, 2574-2585
29. Shen, Y., Joachimiak, A., Rosner, M. R., and Tang, W. J. (2006) Structures of human insulin-degrading enzyme reveal a new substrate recognition mechanism. Nature 443, 870-874 (Pubitemid 44622699)
30. Inagaki, M., Inagaki, N., Takahashi, T., and Takai, Y. (1997) Phosphorylation-dependent control of structures of intermediate filaments: a novel approach using site- and phosphorylation state-specific antibodies. J. Biochem. (Tokyo) 121, 407-414 (Pubitemid 27145892)
31. Chou, Y. H., Khuon, S., Herrmann, H., and Goldman, R. D. (2003) Nestin promotes the phosphorylation-dependent disassembly of vimentin intermediate filaments during mitosis. Mol. Biol. Cell 14, 1468-1478 (Pubitemid 36547415)
32. Sahlgren, C. M., Pallari, H. M., He, T., Chou, Y. H., Goldman, R. D., and Eriksson, J. E. (2006) A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death. EMBO J. 25, 4808-4819 (Pubitemid 44607026)
33. Newport, J., and Spann, T. (1987) Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes. Cell 48, 219-230
34. Prahlad, V., Yoon, M., Moir, R. D., Vale, R. D., and Goldman, R. D. (1998) Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J. Cell Biol. 143, 159-170 (Pubitemid 28480525)
35. Chou, Y. H., Rosevear, E., and Goldman, R. D. (1989) Phosphorylation and disassembly of intermediate filaments in mitotic cells. Proc. Natl. Acad. Sci. U. S. A. 86, 1885-1889 (Pubitemid 19087036)
36. Goldman, R. D., Khuon, S., Chou, Y. H., Opal, P., and Steinert, P. M. (1996) The function of intermediate filaments in cell shape and cytoskeletal integrity. J. Cell Biol. 134, 971-983 (Pubitemid 26278222)
37. Chou, Y. H., Opal, P., Quinlan, R. A., and Goldman, R. D. (1996) The relative roles of specific N- and C-terminal phosphorylation sites in the disassembly of intermediate filament in mitotic BHK-21 cells. J. Cell Sci. 109, 817-826 (Pubitemid 26134384)
38. Chesneau, V., and Rosner, M. R. (2000) Functional human insulin-degrading enzyme can be expressed in bacteria. Protein Expr. Purif. 19, 91-98 (Pubitemid 30387899)
39. Chou, Y. H., Bischoff, J. R., Beach, D., and Goldman, R. D. (1990) Intermediate filament reorganization during mitosis is mediated by p34cdc2 phosphorylation of vimentin. Cell 62, 1063-1071 (Pubitemid 20333767)
40. Johnson, G. D., and Ahn, K. (2000) Development of an internally quenched fluorescent substrate selective for endothelin-converting enzyme-1. Anal. Biochem. 286, 112-118
41. Schagger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379 (Pubitemid 18004907)
42. Dahlstrand, J., Zimmerman, L. B., McKay, R. D., and Lendahl, U. (1992) Characterization of the human nestin gene reveals a close evolutionary relationship to neurofilaments. J. Cell Sci. 103, 589-597
43. Weirich, G., Mengele, K., Yfanti, C., Gkazepis, A., Hellmann, D., Welk, A., Giersig, C., Kuo, W. L., Rosner, M. R., Tang, W. J., and Schmitt, M. (2008) Immunohistochemical evidence of ubiquitous distribution of the metalloendoprotease insulin-degrading enzyme (IDE; insulysin) in human non-malignant tissues and tumor cell lines. Biol. Chem. 389, 1441-1445
44. Sahlgren, C. M., Mikhailov, A., Hellman, J., Chou, Y. H., Lendahl, U., Goldman, R. D., and Eriksson, J. E. (2001) Mitotic reorganization of the intermediate filament protein nestin involves phosphorylation by cdc2 kinase. J. Biol. Chem. 276, 16456-16463 (Pubitemid 37391694)
45. Eriksson, J. E., He, T., Trejo-Skalli, A. V., Harmala-Brasken, A. S., Hellman, J., Chou, Y. H., and Goldman, R. D. (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell Sci. 117, 919-932 (Pubitemid 38386949)
46. Jones, J. C., Goldman, A. E., Yang, H. Y., and Goldman, R. D. (1985) The organizational fate of intermediate filament networks in two epithelial cell types during mitosis. J. Cell Biol. 100, 93-102
47. Tzivion, G., Luo, Z. J., and Avruch, J. (2000) Calyculin A-induced vimentin phosphorylation sequesters 14-3-3 and displaces other 14-3-3 partners in vivo. J. Biol. Chem. 275, 29,772-29,778 (Pubitemid 32043861)
48. Ku, N. O., Michie, S., Resurreccion, E. Z., Broome, R. L., and Omary, M. B. (2002) Keratin binding to 14-3-3 proteins modulates keratin filaments and hepatocyte mitotic progression. Proc. Natl. Acad. Sci. U. S. A. 99, 4373-4378 (Pubitemid 34285992)
49. Liao, J., and Omary, M. B. (1996) 14-3-3 proteins associate with phosphorylated simple epithelial keratins during cell cycle progression and act as a solubility cofactor. J. Cell Biol. 133, 345-357 (Pubitemid 26132533)
50. Malito, E., Ralat, L. A., Manolopoulou, M., Tsay, J. L., Wadlington, N. L., and Tang, W. J. (2008) Molecular bases for the recognition of short peptide substrates and cysteine-directed modifications of human insulin-degrading enzyme. Biochemistry 47, 12822-12834
51. Safavi, A., Miller, B. C., Cottam, L., and Hersh, L. B. (1996) Identification of γ-endorphin-generating enzyme as insulin-degrading enzyme. Biochemistry 35, 14318-14325
52. Song, E. S., Daily, A., Fried, M. G., Juliano, M. A., Juliano, L., and Hersh, L. B. (2005) Mutation of active site residues of insulin-degrading enzyme alters allosteric interactions. J. Biol. Chem. 280, 17701-17706 (Pubitemid 41389007)
53. Fawcett, J., Permana, P. A., Levy, J. L., and Duckworth, W. C. (2007) Regulation of protein degradation by insulin-degrading enzyme: analysis by small interfering RNA-mediated gene silencing. Arch. Biochem. Biophys. 468, 128-133 (Pubitemid 350103692)
54. Johnston, J. A., Ward, C. L., and Kopito, R. R. (1998) Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898
55. Bieberich, E., MacKinnon, S., Silva, J., Noggle, S., and Condie, B. G. (2003) Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J. Cell Biol. 162, 469-479 (Pubitemid 36988555)
56. Wakamatsu, Y., Nakamura, N., Lee, J. A., Cole, G. J., and Osumi, N. (2007) Transitin, a nestin-like intermediate filament protein, mediates cortical localization and the lateral transport of Numb in mitotic avian neuroepithelial cells. Development 134, 2425-2433 (Pubitemid 47074137)