Prodomain-dependent tissue targeting of an ADAMTS protease controls cell migration in Caenorhabditis elegans

EMBO Journal

Volumn 26, Issue 11, 2007, Pages 2607-2620

  Ihara, Shinji ^a   Nishiwaki, Kiyoji ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

ADAMTS protease; Cell migration; Glycosylation; MIG 17; Prodomain

Indexed keywords

POLYPEPTIDE; PROTEASE ADAMTS; PROTEIN; PROTEIN ADAMTS; PROTEIN MIG 17; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL CULTURE; CELL MIGRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECRETION; TRANSGENIC ANIMAL; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASEMENT MEMBRANE; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MOVEMENT; DISINTEGRINS; ENZYME ACTIVATION; GONADS; METALLOENDOPEPTIDASES; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PROTEIN STRUCTURE, TERTIARY;

ANIMALIA; CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 34249986093     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601718     Document Type: Article

References (38)

1. Baum PD, Garriga G (1997) Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19: 51-62
2. Blelloch R, Anna-Arriola SS, Gao D, Li Y, Hodgkin J, Kimble J (1999) The gon-1 gene is required for gonadal morphogenesis in Caenorhabditis elegans. Dev Biol 216: 382-393
3. Blelloch R, Kimble J (1999) Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans. Nature 399: 586-590
4. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94
5. Cal S, Arguelles JM, Fernandez PL, Lopez-Otin C (2001) Identification, characterization, and intracellular processing of ADAM-TS12, a novel human disintegrin with a complex structural organization involving multiple thrombospondin-1 repeats. J Biol Chem 276: 17932-17940
6. Christensen M, Estevez A, Yin X, Fox R, Morrison R, McDonnell M, Gleason C, Miller III DM, Strange K (2002) A primary culture system for functional analysis of C. elegans neurons and muscle cells. Neuron 33: 503-514
7. Colige A, Li SW, Sieron AL, Nusgens BV, Prockop DJ, Lapiere CM (1997) cDNA cloning and expression of bovine procollagen I N-proteinase: a new member of the superfamily of zinc-metalloproteinases with binding sites for cells and other matrix components. Proc Natl Acad Sci USA 94: 2374-2379
8. Colige A, Nuytinck L, Hausser I, van Essen AJ, Thiry M, Herens C, Ades LC, Malfait F, Paepe AD, Franck P, Wolff G, Oosterwijk JC, Smitt JH, Lapiere CM, Nusgens BV (2004) Novel types of mutation responsible for the dermatosparactic type of Ehlers-Danlos syndrome (type VIIC) and common polymorphisms in the ADAMTS2 gene. J Invest Dermatol 123: 656-663
9. Dagoneau N, Benoist-Lasselin C, Huber C, Faivre L, Megarbane A, Alswaid A, Dollfus H, Alembik Y, Munnich A, Legeai-Mallet L, Cormier-Daire V (2004) ADAMTS10 mutations in autosomal recessive Weill-Marchesani syndrome. Am J Hum Genet 75: 801-806
10. Fares H, Greenwald I (2001a) Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159: 133-145
11. Fares H, Greenwald I (2001b) Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 28: 64-68
12. Fernandes RJ, Hirohata S, Engle JM, Colige A, Cohn DH, Eyre DR, Apte SS (2001) Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J Biol Chem 276: 31502-31509
13. Henderson ST, Gao D, Lambie EJ, Kimble J (1994) lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120: 2913-2924
14. Ihara S, Miyoshi E, Nakahara S, Sakiyama H, Ihara H, Akinaga A, Honke K, Dickson RB, Lin CY, Taniguchi N (2004) Addition of β1-6 GlcNAc branching to the oligosaccharide attached to Asn 772 in the serine protease domain of matriptase plays a pivotal role in its stability and resistance against trypsin. Glycobiology 14: 139-146
15. Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81: 208-219
16. Koo BH, Longpre JM, Somerville RP, Alexander JP, Leduc R, Apte SS (2006) Cell-surface processing of pro-ADAMTS9 by furin. J Biol Chem 281: 12485-12494
17. Kubota Y, Sano M, Goda S, Suzuki N, Nishiwaki K (2006) The conserved oligomeric Golgi complex acts in organ morphogenesis via glycosylation of an ADAM protease in C. elegans. Development 133: 263-273
18. Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K (1997) Molecular cloning of a gene encoding a new type of metalloproteinase-disintegrin family protein with thrombospondin motifs as an inflammation associated gene. J Biol Chem 272: 556-562
19. Kuno K, Okada Y, Kawashima H, Nakamura H, Miyasaka M, Ohno H, Matsushima K (2000) ADAMTS-1 cleaves a cartilage proteoglycan, aggrecan. FEBS Lett 478: 241-245
20. Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, Yang AY, Siemieniak DR, Stark KR, Gruppo R, Sarode R, Shurin SB, Chandrasekaran V, Stabler SP, Sabio H, Bouhassira EE, Upshaw Jr JD, Ginsburg D, Tsai HM (2001) Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 413: 488-494
21. Longpre JM, Leduc R (2004) Identification of prodomain determinants involved in ADAMTS-1 biosynthesis. J Biol Chem 279: 33237-33245
22. Maduro M, Pilgrim D (1995) Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141: 977-988
23. Matthews RT, Gary SC, Zerillo C, Pratta M, Solomon K, Arner EC, Hockfield S (2000) Brain-enriched hyaluronan binding (BEHAB)/ brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J Biol Chem 275: 22695-22703
24. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970
25. Nishiwaki K (1999) Mutations affecting symmetrical migration of distal tip cells in Caenorhabditis elegans. Genetics 152: 985-997
26. Nishiwaki K, Hisamoto N, Matsumoto K (2000) A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans. Science 288: 2205-2208
27. Nishiwaki K, Kubota Y, Chigira Y, Roy SK, Suzuki M, Schvarzstein M, Jigami Y, Hisamoto N, Matsumoto K (2004) An NDPase links ADAM protease glycosylation with organ morphogenesis in C. elegans. Nat Cell Biol 6: 31-37
28. Porter S, Clark IM, Kevorkian L, Edwards DR (2005) The ADAMTS metalloproteinases. Biochem J 386: 15-27
29. Rodriguez-Manzaneque JC, Milchanowski AB, Dufour EK, Leduc R, Iruela-Arispe ML (2000) Characterization of METH-1/ADAMTS1 processing reveals two distinct active forms. J Biol Chem 275: 33471-33479
30. Sandy JD, Westling J, Kenagy RD, Iruela-Arispe ML, Verscharen C, Rodriguez-Mazaneque JC, Zimmermann DR, Lemire JM, Fischer JW, Wight TN, Clowes AW (2001) Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 276: 13372-13378
31. Schlomann U, Wildeboer D, Webster A, Antropova O, Zeuschner D, Knight CG, Docherty AJ, Lambert M, Skelton L, Jockusch H, Bartsch JW (2002) The metalloprotease disintegrin ADAM8. Processing by autocatalysis is required for proteolytic activity and cell adhesion. J Biol Chem 277: 48210-48219
32. Somerville RP, Jungers KA, Apte SS (2004a) Discovery and characterization of a novel, widely expressed metalloprotease, ADAMTS10, and its proteolytic activation. J Biol Chem 279: 51208-51217
33. Somerville RP, Longpre JM, Apel ED, Lewis RM, Wang LW, Sanes JR, Leduc R, Apte SS (2004b) ADAMTS7B, the full-length product of the ADAMTS7 gene, is a chondroitin sulfate proteoglycan containing a mucin domain. J Biol Chem 279: 35159-35175
34. Somerville RP, Longpre JM, Jungers KA, Engle JM, Ross M, Evanko S, Wight TN, Leduc R, Apte SS (2003) Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem 278: 9503-9513
35. Tortorella M, Pratta M, Liu RQ, Abbaszade I, Ross H, Burn T, Arner E (2000) The thrombospondin motif of aggrecanase-1 (ADAMTS-4) is critical for aggrecan substrate recognition and cleavage. J Biol Chem 275: 25791-25797
36. Tortorella MD, Arner EC, Hills R, Gormley J, Fok K, Pegg L, Munie G, Malfait AM (2005) ADAMTS-4 (aggrecanase-1): N-terminal activation mechanisms. Arch Biochem Biophys 444: 34-44
37. Tortorella MD, Burn TC, Pratta MA, Abbaszade I, Hollis JM, Liu R, Rosenfeld SA, Copeland RA, Decicco CP, Wynn R, Rockwell A, Yang F, Duke JL, Solomon K, George H, Bruckner R, Nagase H, Itoh Y, Ellis DM, Ross H, Wiswall BH, Murphy K, Hillman Jr MC, Hollis GF, Newton RC, Magolda RL, Trzaskos JM, Arner EC (1999) Purification and cloning of aggrecanase-1: a member of the ADAMTS family of proteins. Science 284: 1664-1666
38. Wang WM, Lee S, Steiglitz BM, Scott IC, Lebares CC, Allen ML, Brenner MC, Takahara K, Greenspan DS (2003) Transforming growth factor-b induces secretion of activated ADAMTS-2. A procollagen III N-proteinase. J Biol Chem 278: 19549-19557