Alternative splicing of ADAM15 regulates its interactions with cellular SH3 proteins

Journal of Cellular Biochemistry

Volumn 108, Issue 4, 2009, Pages 877-885

  Kleino, Iivari ^a   Ortiz, Rebekka M ^b   Yritys, Miljamartta ^b   Huovila, Ari Pekka J ^b   Saksela, Kalle ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

ADAM15; Nephrocystin; SH3 domain; SNX33; Sorting nexin

Indexed keywords

ADAM PROTEIN; ADAM15; PROTEASE NEXIN; PROTEIN SH3; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; BINDING SITE; CELL LYSATE; EXON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

ADAM PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALTERNATIVE SPLICING; AMINO ACID MOTIFS; CARRIER PROTEINS; CELL LINE; HUMANS; MEMBRANE PROTEINS; PROLINE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; SRC HOMOLOGY DOMAINS; VESICULAR TRANSPORT PROTEINS;

EID: 70350451407     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22317     Document Type: Article

References (54)

1. Abram CL, Seals DF, Pass I, Salinsky D, Maurer L, Roth TM, Courtneidge SA. 2003. The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J Biol Chem 278:16844-16851. (Pubitemid 36799554)
2. Alto NM, Weflen AW, Rardin MJ, Yarar D, Lazar CS, Tonikian R, Koller A, Taylor SS, Boone C, Sidhu SS, Schmid SL, Hecht GA, Dixon JE. 2007. The type III effector EspF coordinates membrane trafficking by the spatiotemporal activation of two eukaryotic signaling pathways. J Cell Biol 178:1265-1278. (Pubitemid 47480231)
3. Benzing T, Gerke P, Hopker K, Hildebrandt F, Kim E, Walz G. 2001. Nephrocystin interacts with Pyk2, p130(Cas), and tensin and triggers phosphorylation of Pyk2. Proc Natl Acad Sci USA 98:9784-9789. (Pubitemid 32769381)
4. Charrier L, Yan Y, Driss A, Laboisse CL, Sitaraman SV, Merlin D. 2005. ADAM-15 inhibits wound healing in human intestinal epithelial cell monolayers. Am J Physiol Gastrointest Liver Physiol 288:G346-G353. (Pubitemid 40129587)
5. Chen Q, Meng LH, Zhu CH, Lin LP, Lu H, Ding J. 2008. ADAM15 suppresses cell motility by driving integrin alpha5beta1 cell surface expression via Erk inactivation. Int J Biochem Cell Biol 40:2164-2173.
6. Donaldson JC, Dempsey PJ, Reddy S, Bouton AH, Coffey RJ, Hanks SK. 2000. Crk-associated substrate p130(Cas) interacts with nephrocystin and both proteins localize to cell-cell contacts of polarized epithelial cells. Exp Cell Res 256:168-178. (Pubitemid 30211179)
7. Edwards DR, Handsley MM, Pennington CJ. 2009. The ADAM metalloproteinases. Mol Aspects Med 29:258-289.
8. Eley L, Moochhala SH, Simms R, Hildebrandt F, Sayer JA. 2008. Nephrocystin-1 interacts directly with Ack1 and is expressed in human collecting duct. Biochem Biophys Res Commun 371:877-882.
9. Foster-Barber A, Bishop JM. 1998. Src interacts with dynamin and synapsin in neuronal cells. Proc Natl Acad Sci USA 95:4673-4677. (Pubitemid 28207972)
10. Haberg K, Lundmark R, Carlsson SR. 2008. SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking. J Cell Sci 121:1495-1505. (Pubitemid 351936314)
11. Ham C, Levkau B, Raines EW, Herren B. 2002. ADAM15 is an adherens junction molecule whose surface expression can be driven by VE-cadherin. Exp Cell Res 279:239-247. (Pubitemid 35217552)
12. Heikkinen LS, Kazlauskas A, Melen K, Wagner R, Ziegler T, Julkunen I, Saksela K. 2008. Avian and 1918 Spanish influenza a virus NS1 proteins bind to Crk/CrkL Src homology 3 domains to activate host cell signaling. J Biol Chem 283:5719-5727.
13. Hiipakka M, Poikonen K, Saksela K. 1999. SH3 domains with high affinity and engineered ligand specificities targeted to HIV-1 Nef. J Mol Biol 293:1097-1106.
14. Hildebrandt F, Attanasio M, Otto E. 2009. Nephronophthisis: Disease mechanisms of a ciliopathy. J Am Soc Nephrol 20:23-35.
15. Horiuchi K, Weskamp G, Lum L, Hammes HP, Cai H, Brodie TA, Ludwig T, Chiusaroli R, Baron R, Preissner KT, Manova K, Blobel CP. 2003. Potential role for ADAM15 in pathological neovascularization in mice. Mol Cell Biol 23:5614-5624. (Pubitemid 36951327)
16. Howard L, Nelson KK, Maciewicz RA, Blobel CP. 1999. Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J Biol Chem 274:31693-31699. (Pubitemid 129501632)
17. Huovila AP, Turner AJ, Pelto-Huikko M, Kärkkäinen I, Ortiz RM. 2005. Shedding light on ADAM metalloproteinases. Trends Biochem Sci 30:413-422.
18. Kang Q, Cao Y, Zolkiewska A. 2000. Metalloprotease-disintegrin ADAM 12 binds to the SH3 domain of Src and activates Src tyrosine kinase in C2C12 cells. Biochem J 352(Pt 3): 883-892. (Pubitemid 32015046)
19. Kärkkäinen S, Hiipakka M, Wang JH, Kleino I, Vähä-Jaakkola M, Renkema GH, Liss M, Wagner R, Saksela K. 2006. Identification of preferred protein interactions by phage-display of the human Src homology-3 proteome. EMBO Rep 7:186-191.
20. Kesti T, Ruppelt A, Wang JH, Liss M, Wagner R, Tasken K, Saksela K. 2007. Reciprocal regulation of SH3 and SH2 domain binding via tyrosine phosphorylation of a common site in CD3epsilon. J Immunol 179:878-885.
21. Kleino I, Ortiz RM, Huovila AP. 2007. ADAM15 gene structure and differential alternative exon use in human tissues. BMC Mol Biol 8:90. (Pubitemid 350286458)
22. Krätzschmar J, Lum L, Blobel CP. 1996. Metargidin, a membrane-anchored metalloprotease-disintegrin protein with an RGD integrin binding sequence. J Biol Chem 271:4593-4596. (Pubitemid 26074933)
23. Le Gall SM, Bobe P, Reiss K, Horiuchi K, Niu XD, Lundell D, Gibb DR, Conrad D, Saftig P, Blobel CP. 2009. ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha. Mol Biol Cell 20:1785-1794.
24. Lundmark R, Carlsson SR. 2009. SNX9-A prelude to vesicle release. J Cell Sci 122:5-11.
25. MaCaulay SL, Stoichevska V, Grusovin J, Gough KH, Castelli LA, Ward CW. 2003. Insulin stimulates movement of sorting nexin 9 between cellular compartments: A putative role mediating cell surface receptor expression and insulin action. Biochem J 376:123-134. (Pubitemid 37487208)
26. Malinin NL, Wright S, Seubert P, Schenk D, Griswold-Prenner I. 2005. Amyloid-beta neurotoxicity is mediated by FISH adapter protein and ADAM12 metalloprotease activity. Proc Natl Acad Sci USA 102:3058-3063. (Pubitemid 40299915)
27. Maretzky T, Yang G, Ouerfelli O, Overall CM, Worpenberg S, Hassiepen U, Eder J, Blobel CP. 2009. Characterization of the catalytic activity of the membrane-anchored metalloproteinase ADAM15 in cell-based assays. Biochem J 420:105-113.
28. Mayer BJ. 2001. SH3 domains: Complexity in moderation. J Cell Sci 114:1253-1263.
29. Mayer BJ, Saksela K. 2005. Modular protein domains. In: "modular protein domains." Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA. pp 37-55.
30. Mizushima S, Nagata S. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res 18:5322. (Pubitemid 20270119)
31. Moarefi I, LaFevre-Bernt M, Sicheri F, Huse M, Lee CH, Kuriyan J, Miller WT. 1997. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385:650-653. (Pubitemid 27087580)
32. Mori S, Tanaka M, Nanba D, Nishiwaki E, Ishiguro H, Higashiyama S, Matsuura N. 2003. PACSIN3 binds ADAM12/meltrin alpha and up-regulates ectodomain shedding of heparin-binding epidermal growth factor-like growth factor. J Biol Chem 278:46029-46034. (Pubitemid 37432752)
33. Najy AJ, Day KC, Day ML. 2008a. ADAM15 supports prostate cancer metastasis by modulating tumor cell-endothelial cell interaction. Cancer Res 68:1092-1099.
34. Najy AJ, Day KC, Day ML. 2008b. The ectodomain shedding of E-cadherin by ADAM15 supports ErbB receptor activation. J Biol Chem 283:18393-18401.
35. Ortiz RM, Kärkkäinen I, Huovila AP. 2004. Aberrant alternative exon use and increased copy number of human metalloprotease-disintegrin ADAM15 gene in breast cancer cells. Genes Chromosomes Cancer 41:366-378. (Pubitemid 39488495)
36. Parkin E, Harris B. 2009. A disintegrin and metalloproteinase (ADAM)-mediated ectodomain shedding of ADAM10. J Neurochem 108:1464-1479.
37. Poghosyan Z, Robbins SM, Houslay MD, Webster A, Murphy G, Edwards DR. 2002. Phosphorylation-dependent interactions between ADAM15 cytoplasmic domain and Src family protein-tyrosine kinases. J Biol Chem 277:4999-5007. (Pubitemid 34968539)
38. Resch A, Xing Y, Modrek B, Gorlick M, Riley R, Lee C. 2004. Assessing the impact of alternative splicing on domain interactions in the human proteome. J Proteome Res 3:76-83. (Pubitemid 38233453)
39. Sambrook J, Russell DE. 2001. Molecular cloning: A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
40. Saunders WB, Bohnsack BL, Faske JB, Anthis NJ, Bayless KJ, Hirschi KK, Davis GE. 2006. Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol 175:179-191.
41. Schermer B, Hopker K, Omran H, Ghenoiu C, Fliegauf M, Fekete A, Horvath J, Kottgen M, Hackl M, Zschiedrich S, Huber TB, Kramer-Zucker A, Zentgraf H, Blaukat A, Walz G, Benzing T. 2005. Phosphorylation by casein kinase 2 induces PACS-1 binding of nephrocystin and targeting to cilia. EMBO J 24:4415-4424. (Pubitemid 41828915)
42. Schobel S, Neumann S, Hertweck M, Dislich B, Kuhn PH, Kremmer E, Seed B, Baumeister R, Haass C, Lichtenthaler SF. 2008. A novel sorting nexin modulates endocytic trafficking and alpha-secretase cleavage of the amyloid precursor protein. J Biol Chem 283:14257-14268.
43. Seet LF, Hong W. 2006. The Phox (PX) domain proteins and membrane traffic. Biochim Biophys Acta 1761:878-896. (Pubitemid 44348964)
44. Shimizu E, Yasui A, Matsuura K, Hijiya N, Higuchi Y, Yamamoto S. 2003. Structure and expression of the murine ADAM15 gene and its splice variants, and difference of interaction between their cytoplasmic domains and Src family proteins. Biochem Biophys Res Commun 309:779-785. (Pubitemid 37122596)
45. Stamm S, Ben-Ari S, Rafalska I, Tang Y, Zhang Z, Toiber D, Thanaraj TA, Soreq H. 2005. Function of alternative splicing. Gene 344:1-20.
46. Tanaka M, Nanba D, Mori S, Shiba F, Ishiguro H, Yoshino K, Matsuura N, Higashiyama S. 2004. ADAM binding protein Eve-1 is required for ectodomain shedding of epidermal growth factor receptor ligands. J Biol Chem 279:41950-41959. (Pubitemid 39313645)
47. Tousseyn T, Thathiah A, Jorissen E, Raemaekers T, Konietzko U, Reiss K, Maes E, Snellinx A, Serneels L, Nyabi O, Annaert W, Saftig P, Hartmann D, De Strooper B. 2009. ADAM10, the rate-limiting protease of regulated intramembrane proteolysis of Notch and other proteins, is processed by ADAMS-9, ADAMS-15, and the gamma-secretase. J Biol Chem 284:11738-11747.
48. Tsyba L, Gryaznova T, Dergai O, Dergai M, Skrypkina I, Kropyvko S, Boldyryev O, Nikolaienko O, Novokhatska O, Rynditch A. 2008. Alternative splicing affecting the SH3A domain controls the binding properties of intersectin 1 in neurons. Biochem Biophys Res Commun 372:929-934.
49. Ushio-Fukai M. 2006a. Localizing NADPH oxidase-derived ROS. Sci STKE 2006:re8.
50. Ushio-Fukai M. 2006b. Redox signaling in angiogenesis: Role of NADPH oxidase. Cardiovasc Res 71:226-235. (Pubitemid 43913733)
51. Xie B, Shen J, Dong A, Swaim M, Hackett SF, Wyder L, Worpenberg S, Barbieri S, Campochiaro PA. 2008. An Adam15 amplification loop promotes vascular endothelial growth factor-induced ocular neovascularization. FASEB J 22:2775-2783.
52. Yarar D, Waterman-Storer CM, Schmid SL. 2007. SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev Cell 13:43-56. (Pubitemid 46972030)
53. Yasui A, Matsuura K, Shimizu E, Hijiya N, Higuchi Y, Yamamoto S. 2004. Expression of splice variants of the human ADAM15 gene and strong interaction between the cytoplasmic domain of one variant and Src family proteins Lck and Hck. Pathobiology 71:185-192. (Pubitemid 38969876)
54. Zhong JL, Poghosyan Z, Pennington CJ, Scott X, Handsley MM, Warn A, Gavrilovic J, Honert K, Kruger A, Span PN, Sweep FC, Edwards DR. 2008. Distinct functions of natural ADAM-15 cytoplasmic domain variants in human mammary carcinoma. Mol Cancer Res 6:383-394.