Lysine 63-linked ubiquitination is important for arachidonic acid-induced cellular adhesion and migration

Biochemistry and Cell Biology

Volumn 88, Issue 6, 2010, Pages 947-956

  Ray, Denise M ^a   Rogers, Brian A ^a,b   Sunman, Jeffrey A ^a   Akiyama, Steven K ^a   Olden, Kenneth ^a   Roberts, John D ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

Author keywords

Adhesion; Arachidonic acid; Metastasis; Signal transduction; Ubiquitin

Indexed keywords

ARACHIDONIC ACIDS; CELL MIGRATION; CELLULAR ADHESION; EXTRACELLULAR MATRICES; FUNCTIONAL INFORMATION; HUMAN CANCER CELLS; INTRACELLULAR SIGNALING PATHWAYS; LYSINE RESIDUES; METASTASIS; NULL MUTANT; P38 MAPK; POLYUBIQUITIN; POLYUNSATURATED FATTY ACIDS; UBIQUITIN; UBIQUITINATION;

ADHESION; AMINO ACIDS; BACTERIOPHAGES; CELL ADHESION; CHEMICAL ACTIVATION; COLLAGEN; ENZYME ACTIVITY; ENZYME INHIBITION; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

FATTY ACIDS;

ARACHIDONIC ACID; COLLAGEN TYPE 4; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE P38; P21 ACTIVATED KINASE 1; PYR 431; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL MIGRATION; DRUG INHIBITION; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTRACELLULAR SIGNALING; OUTCOME ASSESSMENT; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR CELL; UBIQUITINATION;

ARACHIDONIC ACID; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; COLLAGEN TYPE IV; ENZYME INHIBITORS; EXTRACELLULAR MATRIX; HUMANS; LYSINE; NEOPLASM METASTASIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; UBIQUITIN; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITINATION;

EID: 78650382466     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O10-148     Document Type: Article

References (38)

1. Akiyama, S.K. 2002. Functional analysis of cell adhesion: quantitation of cell-matrix attachment. Methods Cell Biol. 69: 281-296. 10.1016/S0091-679X(02) 69018-1 12070999 (Pubitemid 44245298)
2. Akiyama, S.K., Yamada, S.S., Chen, W.T., and Yamada, K.M. 1989. Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J. Cell Biol. 109 (2): 863-875. 10.1083/jcb.109.2.863 2527241
3. Didier, C., Broday, L., Bhoumik, A., Israeli, S., Takahashi, S., Nakayama, K., et al. 2003. RNF5, a RING finger protein that regulates cell motility by targeting paxillin ubiquitination and altered localization. Mol. Cell. Biol. 23 (15): 5331-5345. 10.1128/MCB.23.15.5331-5345.2003 12861019 (Pubitemid 36950888)
4. Erickson, K.L., and Hubbard, N.E. 1990. Dietary fat and tumor metastasis. Nutr. Rev. 48 (1): 6-14. 10.1111/j.1753-4887.1990.tb02871.x 2186315
5. Fan, Y., Yu, Y., Shi, Y., Sun, W., Xie, M., Ge, N., et al. 2010. Lysine 63-linked polyubiquitination of TAK1 at lysine 158 is required for tumor necrosis factor -and interleukin-1-induced IKK/NF-B and JNK/AP-1 activation. J. Biol. Chem. 285 (8): 5347-5360. 10.1074/jbc.M109.076976 20038579
6. Garcia, M.C., Ray, D.M., Lackford, B., Rubino, M., Olden, K., and Roberts, J.D. 2009. Arachidonic acid stimulates cell adhesion through a novel p38 MAPK-RhoA signaling pathway that involves heat shock protein 27. J. Biol. Chem. 284 (31): 20936-20945. 10.1074/jbc.M109.020271 19506078
7. Herrmann, J., Lerman, L.O., and Lerman, A. 2007. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ. Res. 100 (9): 1276-1291. 10.1161/01.RES.0000264500.11888.f0 17495234 (Pubitemid 46742918)
8. Hershko, A., and Ciechanover, A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67 (1): 425-479. 10.1146/annurev.biochem.67.1.425 9759494 (Pubitemid 28411135)
9. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. 1983. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258 (13): 8206-8214. 6305978
10. Huang, C., Rajfur, Z., Yousefi, N., Chen, Z., Jacobson, K., and Ginsberg, M.H. 2009. Talin phosphorylation by Cdk5 regulates Smurf1-mediated talin head ubiquitylation and cell migration. Nat. Cell Biol. 11 (5): 624-630. 10.1038/ncb1868 19363486
11. Jiang, W.G., Hiscox, S., Hallett, M.B., Scott, C., Horrobin, D.F., and Puntis, M.C. 1995. Inhibition of hepatocyte growth factor-induced motility and in vitro invasion of human colon cancer cells by gamma-linolenic acid. Br. J. Cancer, 71 (4): 744-752. 7710939
12. Jin, J., Li, X., Gygi, S.P., and Harper, J.W. 2007. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature, 447 (7148): 1135-1138. 10.1038/nature05902 17597759 (Pubitemid 47014428)
13. Jin, C., Yang, Y.A., Anver, M.R., Morris, N., Wang, X., and Zhang, Y.E. 2009. Smad ubiquitination regulatory factor 2 promotes metastasis of breast cancer cells by enhancing migration and invasiveness. Cancer Res. 69 (3): 735-740. 10.1158/0008-5472.CAN-08-1463 19155312
14. Johanning, G.L., and Lin, T.Y. 1995. Unsaturated fatty acid effects on human breast cancer cell adhesion. Nutr. Cancer, 24 (1): 57-66. 10.1080/01635589509514393 7491298
15. Kaabeche, K., Guenou, H., Bouvard, D., Didelot, N., Listrat, A., and Marie, P.J. 2005. Cbl-mediated ubiquitination of 5 integrin subunit mediates fibronectin-dependent osteoblast detachment and apoptosis induced by FGFR2 activation. J. Cell Sci. 118 (6): 1223-1232. 10.1242/jcs.01679 15728256 (Pubitemid 40528692)
16. Kanayama, A., Seth, R.B., Sun, L., Ea, C.K., Hong, M., Shaito, A., et al. 2004. TAB2 and TAB3 activate the NF-B pathway through binding to polyubiquitin chains. Mol. Cell, 15 (4): 535-548. 10.1016/j.molcel.2004.08.008 15327770 (Pubitemid 39141781)
17. Khanapure, S.P., Garvey, D.S., Janero, D.R., and Letts, L.G. 2007. Eicosanoids in inflammation: biosynthesis, pharmacology, and therapeutic frontiers. Curr. Top. Med. Chem. 7 (3): 311-340. 10.2174/156802607779941314 17305573 (Pubitemid 46358664)
18. Kishida, S., Sanjo, H., Akira, S., Matsumoto, K., and Ninomiya-Tsuji, J. 2005. TAK1-binding protein 2 facilitates ubiquitination of TRAF6 and assembly of TRAF6 with IKK in the IL-1 signaling pathway. Genes Cells, 10 (5): 447-454. 10.1111/j.1365-2443.2005.00852.x 15836773 (Pubitemid 40590362)
19. Mack, G.S., and Marshall, A. 2010. Lost in migration. Nat. Biotechnol. 28 (3): 214-229. 10.1038/nbt0310-214 20212481
20. McGrath, J.P., Jentsch, S., and Varshavsky, A. 1991. UBA1: an essential yeast gene encoding ubiquitin-activating enzyme. EMBO J. 10 (1): 227-236. 1989885
21. Nony, P.A., Kennett, S.B., Glasgow, W.C., Olden, K., and Roberts, J.D. 2005. 15(S)-Lipoxygenase-2 mediates arachidonic acid-stimulated adhesion of human breast carcinoma cells through the activation of TAK1, MKK6, and p38 MAPK. J. Biol. Chem. 280 (36): 31413-31419. 10.1074/jbc.M500418200 16000313 (Pubitemid 41291882)
22. Paine, E., Palmantier, R., Akiyama, S.K., Olden, K., and Roberts, J.D. 2000. Arachidonic acid activates mitogen-activated protein (MAP) kinase-activated protein kinase 2 and mediates adhesion of a human breast carcinoma cell line to collagen type IV through a p38 MAP kinase-dependent pathway. J. Biol. Chem. 275 (15): 11284-11290. 10.1074/jbc.275.15.11284 10753939 (Pubitemid 30212776)
23. Palmantier, R., Roberts, J.D., Glasgow, W.C., Eling, T., and Olden, K. 1996. Regulation of the adhesion of a human breast carcinoma cell line to type IV collagen and vitronectin: roles for lipoxygenase and protein kinase C. Cancer Res. 56 (9): 2206-2212. 8616873
24. 1 integrin-mediated adhesion of human breast carcinoma cells to type IV collagen by activating protein kinases C- and-. Cancer Res. 61 (6): 2445-2452. 11289113
25. Pickart, C.M., and Eddins, M.J. 2004. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta, 1695 (1-3): 55-72. 10.1016/j.bbamcr.2004.09. 019 15571809 (Pubitemid 39585154)
26. Rose, D.P., and Connolly, J.M. 1997. Dietary fat and breast cancer metastasis by human tumor xenografts. Breast Cancer Res. Treat. 46 (2-3): 225-237. 10.1023/A:1005971317978 9478277 (Pubitemid 28029525)
27. Rose, D.P., Connolly, J.M., and Liu, X.H. 1994. Dietary fatty acids and human breast cancer cell growth, invasion, and metastasis. Adv. Exp. Med. Biol. 364: 83-91. 7725962
28. Shekhar, M.P., Gerard, B., Pauley, R.J., Williams, B.O., and Tait, L. 2008. Rad6B is a positive regulator of -catenin stabilization. Cancer Res. 68 (6): 1741-1750. 10.1158/0008-5472.CAN-07-2111 18339854 (Pubitemid 351416559)
29. Shi, C.S., and Kehrl, J.H. 2003. Tumor necrosis factor (TNF)-induced germinal center kinase-related (GCKR) and stress-activated protein kinase (SAPK) activation depends upon the E2/E3 complex Ubc13-Uev1A/TNF receptor-associated factor 2 (TRAF2). J. Biol. Chem. 278 (17): 15429-15434. 10.1074/jbc.M211796200 12591926 (Pubitemid 36799883)
30. Sorrentino, A., Thakur, N., Grimsby, S., Marcusson, A., von Bulow, V., Schuster, N., et al. 2008. The type I TGF- receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat. Cell Biol. 10 (10): 1199-1207. 10.1038/ncb1780 18758450
31. Tan, J.M., Wong, E.S., Kirkpatrick, D.S., Pletnikova, O., Ko, H.S., Tay, S.P., et al. 2008. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum. Mol. Genet. 17 (3): 431-439. 10.1093/hmg/ddm320 17981811
32. Wang, C., Deng, L., Hong, M., Akkaraju, G.R., Inoue, J., and Chen, Z.J. 2001. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature, 412 (6844): 346-351. 10.1038/35085597 11460167 (Pubitemid 32694385)
33. Welchman, R.L., Gordon, C., and Mayer, R.J. 2005. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6 (8): 599-609. 10.1038/nrm1700 16064136 (Pubitemid 41081264)
34. Yamamoto, M., Okamoto, T., Takeda, K., Sato, S., Sanjo, H., Uematsu, S., et al. 2006. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat. Immunol. 7 (9): 962-970. 10.1038/ni1367 16862162 (Pubitemid 44263910)
35. Yang, Y., Kitagaki, J., Dai, R.M., Tsai, Y.C., Lorick, K.L., Ludwig, R.L., et al. 2007. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 67 (19): 9472-9481. 10.1158/0008-5472.CAN-07-0568 17909057 (Pubitemid 47535937)
36. Yang, W.L., Wang, J., Chan, C.H., Lee, S.W., Campos, A.D., Lamothe, B., et al. 2009. The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science, 325 (5944): 1134-1138. 10.1126/science.1175065 19713527
37. Yilmaz, M., and Christofori, G. 2010. Mechanisms of motility in metastasizing cells. Mol. Cancer Res. 8 (5): 629-642. 10.1158/1541-7786.MCR-10- 0139 20460404
38. Zacksenhaus, E., and Sheinin, R. 1990. Molecular cloning, primary structure and expression of the human X linked A1S9 gene cDNA which complements the ts A1S9 mouse L cell defect in DNA replication. EMBO J. 9 (9): 2923-2929. 2390975