Metalloproteases meprin α and meprin β are C- and N-procollagen proteinases important for collagen assembly and tensile strength

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 35, 2013, Pages 14219-14224

  Broder, Claudia ^a   Arnold, Philipp ^b   Goff, Sandrine Vadon Le ^c   Konerding, Moritz A ^b   Bahr, Kerstin ^b   Müller, Stefan ^d   Overall, Christopher M ^e   Bond, Judith S ^f   Koudelka, Tomas ^a   Tholey, Andreas ^a   Hulmes, David J S ^c   Moali, Catherine ^c   Becker Pauly, Christoph ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c CNRS   (France)

^d UNIVERSITY OF BERN   (Switzerland)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Connective tissue; Ehlers Danlos syndrome; Fibrosis; Proteolysis; Proteomics

Indexed keywords

COLLAGEN; COLLAGEN FIBRIL; COLLAGENASE 3; FIBRILLAR COLLAGEN; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; MEPRIN; MEPRIN ALPHA; MEPRIN BETA; NEUTROPHIL COLLAGENASE; PROCOLLAGEN C PROTEINASE; PROCOLLAGENASE; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE; UNCLASSIFIED DRUG; COLLAGEN TYPE 1; MEPRIN B; METALLOPROTEINASE; PROCOLLAGEN N PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TENSILE STRENGTH; ANIMAL; CHO CELL LINE; CRICETULUS; GENETICS; HAMSTER; HEK293 CELL LINE; KNOCKOUT MOUSE; METABOLISM; PROTEIN DEGRADATION; SKIN;

MUS;

ANIMALS; CHO CELLS; COLLAGEN TYPE I; CRICETINAE; CRICETULUS; HEK293 CELLS; HUMANS; METALLOENDOPEPTIDASES; MICE; MICE, KNOCKOUT; PROCOLLAGEN N-ENDOPEPTIDASE; PROTEOLYSIS; SKIN; TENSILE STRENGTH;

EID: 84883386538     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305464110     Document Type: Article

References (53)

1. Moali C, Hulmes DJS (2012) Extracellular Matrix: Pathobiology and Signaling. Roles and Regulation of BMP-1/Tolloid-Like Proteinases: Collagen/Matrix Assembly, Growth Factor Activation and Beyond, ed Karamanos M (De Gruyter, Berlin).
2. Hulmes DJS (2008) Collagen diversity, synthesis and assembly. Collagen: Structure and Mechanics, ed Fratzl P (Springer, New York), pp 15-74.
3. Hulmes DJ (2002) Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 137(1-2):2-10.
4. Kadler KE, Holmes DF, Graham H, Starborg T (2000) Tip-mediated fusion involving unipolar collagen fibrils accounts for rapid fibril elongation, the occurrence of fibrillar branched networks in skin and the paucity of collagen fibril ends in vertebrates. Matrix Biol 19(4):359-365.
5. Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118(Pt 7):1341-1353.
6. Widmer C, et al. (2012) Molecular basis for the action of the collagen-specific chaperone Hsp47/SERPINH1 and its structure-specific client recognition. Proc Natl Acad Sci USA 109(33):13243-13247.
7. Colige A, et al. (2002) Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem 277(8): 5756-5766.
8. Hopkins DR, Keles S, Greenspan DS (2007) The bone morphogenetic protein 1/Tolloidlike metalloproteinases. Matrix Biol 26(7):508-523.
9. Moali C, et al. (2005) Substrate-specific modulation of a multisubstrate proteinase: Cterminal processing of fibrillar procollagens is the only BMP-1-dependent activity to be enhanced by PCPE-1. J Biol Chem 280(25):24188-24194.
10. Bourhis JM, et al. (2012) Structural basis of fibrillar collagen trimerization and related genetic disorders. Nat Struct Mol Biol 19(10):1031-1036.
11. Sarras MP, Jr. (1996) BMP-1 and the astacin family of metalloproteinases: A potential link between the extracellular matrix, growth factors and pattern formation. Bioessays 18(6):439-442.
12. Schechter I (2005) Mapping of the active site of proteases in the 1960s and rational design of inhibitors/drugs in the 1990s. Curr Protein Pept Sci 6(6):501-512.
13. Becker-Pauly C, et al. (2011) Proteomic analyses reveal an acidic prime side specificity for the astacin metalloprotease family reflected by physiological substrates. Mol Cell Proteomics 10(9):009233.
14. Vazeille E, et al. (2011) Role of meprins to protect ileal mucosa of Crohn's disease patients from colonization by adherent-invasive E. coli. PLoS ONE 6(6):e21199.
15. Schütte A, Hedrich J, Stöcker W, Becker-Pauly C (2010) Let it flow: Morpholino knockdown in zebrafish embryos reveals a pro-angiogenic effect of the metalloprotease meprin alpha2. PLoS ONE 5(1):e8835.
16. Banerjee S, et al. (2011) Balance of meprin A and B in mice affects the progression of experimental inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 300(2):G273-G282.
17. Herzog C, et al. (2009) Meprin A and meprin alpha generate biologically functional IL-1beta from pro-IL-1beta. Biochem Biophys Res Commun 379(4):904-908.
18. Kruse MN, et al. (2004) Human meprin alpha and beta homo-oligomers: Cleavage of basement membrane proteins and sensitivity to metalloprotease inhibitors. Biochem J 378(Pt 2):383-389.
19. Jefferson T, et al. (2011) Metalloprotease meprin beta generates nontoxic N-terminal amyloid precursor protein fragments in vivo. J Biol Chem 286(31):27741-27750.
20. Broder C, Becker-Pauly C (2013) The metalloproteases meprin α and meprin β: Unique enzymes in inflammation, neurodegeneration, cancer and fibrosis. Biochem J 450(2): 253-264.
21. Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ; Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK) (1998) Ehlers-Danlos syndromes: Revised nosology, Villefranche, 1997. Am J Med Genet 77(1):31-37.
22. Lenaers A, Ansay M, Nusgens BV, Lapière CM (1971) Collagen made of extended chains, procollagen, in genetically-defective dermatosparaxic calves. Eur J Biochem 23(3):533-543.
23. Spinale FG (2002) Matrix metalloproteinases: Regulation and dysregulation in the failing heart. Circ Res 90(5):520-530.
24. Newby AC (2005) Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 85(1):1-31.
25. Brinckerhoff CE, Matrisian LM (2002) Matrix metalloproteinases: A tail of a frog that became a prince. Nat Rev Mol Cell Biol 3(3):207-214.
26. Kadoglou NP, Liapis CD (2004) Matrix metalloproteinases: Contribution to pathogenesis, diagnosis, surveillance and treatment of abdominal aortic aneurysms. Curr Med Res Opin 20(4):419-432.
27. Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69(3):562-573.
28. Nagase H, Brew K (2002) Engineering of tissue inhibitor of metalloproteinases mutants as potential therapeutics. Arthritis Res 4(Suppl 3):S51-S61.
29. Wynn TA, Ramalingam TR (2012) Mechanisms of fibrosis: Therapeutic translation for fibrotic disease. Nat Med 18(7):1028-1040.
30. LeBleu VS, et al. (2013) Identification of human epididymis protein-4 as a fibroblastderived mediator of fibrosis. Nat Med 19(2):227-231.
31. Iyer S, Visse R, Nagase H, Acharya KR (2006) Crystal structure of an active form of human MMP-1. J Mol Biol 362(1):78-88.
32. Tam EM, Moore TR, Butler GS, Overall CM (2004) Characterization of the distinct collagen binding, helicase and cleavage mechanisms of matrix metalloproteinase 2 and 14 (gelatinase A and MT1-MMP): The differential roles of the MMP hemopexin c domains and the MMP-2 fibronectin type II modules in collagen triple helicase activities. J Biol Chem 279(41):43336-43344.
33. Manka SW, et al. (2012) Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci USA 109(31):12461-12466.
34. Eckhard U, Schönauer E, Nüss D, Brandstetter H (2011) Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis. Nat Struct Mol Biol 18(10):1109-1114.
35. Kronenberg D, et al. (2010) Processing of procollagen III by meprins: New players in extracellular matrix assembly? J Invest Dermatol 130(12):2727-2735.
36. Jefferson T, et al. (2013) The substrate degradome of meprin metalloproteases reveals an unexpected proteolytic link between meprin β and ADAM10. Cell Mol Life Sci 70(2):309-333.
37. Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221-233.
38. Van Wart HE, Birkedal-Hansen H (1990) The cysteine switch: A principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc Natl Acad Sci USA 87(14):5578-5582.
39. Kessler E, Takahara K, Biniaminov L, Brusel M, Greenspan DS (1996) Bone morphogenetic protein-1: The type I procollagen C-proteinase. Science 271(5247):360-362.
40. Van der Rest M, Rosenberg LC, Olsen BR, Poole AR (1986) Chondrocalcin is identical with the C-propeptide of type II procollagen. Biochem J 237(3):923-925.
41. Pappano WN, Steiglitz BM, Scott IC, Keene DR, Greenspan DS (2003) Use of Bmp1/Tll1 doubly homozygous null mice and proteomics to identify and validate in vivo substrates of bone morphogenetic protein 1/tolloid-like metalloproteinases. Mol Cell Biol 23(13):4428-4438.
42. Suzuki N, et al. (1996) Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 122(11):3587-3595.
43. Norman LP, Jiang W, Han X, Saunders TL, Bond JS (2003) Targeted disruption of the meprin beta gene in mice leads to underrepresentation of knockout mice and changes in renal gene expression profiles. Mol Cell Biol 23(4):1221-1230.
44. Kang AH, Bornstein P, Piez KA (1967) The amino acid sequence of peptides from the cross-linking region of rat skin collagen. Biochemistry 6(3):788-795.
45. Hanson DA, et al. (1992) A specific immunoassay for monitoring human bone resorption: Quantitation of type I collagen cross-linked N-telopeptides in urine. J Bone Miner Res 7(11):1251-1258.
46. Moradi-Améli M, et al. (1994) Diversity in the processing events at the N-terminus of type-V collagen. Eur J Biochem 221(3):987-995.
47. Pope FM, Burrows NP (1997) Ehlers-Danlos syndrome has varied molecular mechanisms. J Med Genet 34(5):400-410.
48. Hulmes DJ, et al. (1989) Pleomorphism in type I collagen fibrils produced by persistence of the procollagen N-propeptide. J Mol Biol 210(2):337-345.
49. Watson RB, et al. (1992) Ehlers-Danlos syndrome type VIIB: Incomplete cleavage of abnormal type I procollagen by N-proteinase in vitro results in the formation of copolymers of collagen and partially cleaved pNcollagen that are near circular in crosssection. J Biol Chem 267(13):9093-9100.
50. Colige A, et al. (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(4):656-663.
51. Holmes DF, Watson RB, Steinmann B, Kadler KE (1993) Ehlers-Danlos syndrome type VIIB: Morphology of type I collagen fibrils formed in vivo and in vitro is determined by the conformation of the retained N-propeptide. J Biol Chem 268(21):15758-15765.
52. Giunta C, Chambaz C, Pedemonte M, Scapolan S, Steinmann B (2008) The arthrochalasia type of Ehlers-Danlos syndrome (EDS VIIA and VIIB): The diagnostic value of collagen fibril ultrastructure. Am J Med Genet A 146A(10):1341-1346.
53. Pettersen EF, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.