Procollagen C-proteinase enhancer grasps the stalk of the C-propeptide trimer to boost collagen precursor maturation

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

Volumn 110, Issue 16, 2013, Pages 6394-6399

  Bourhis, Jean Marie ^a,c   Vadon Le Goff, Sandrine ^a   Afrache, Hassnae ^a,d   Mariano, Natacha ^a   Kronenberg, Daniel ^a,e   Thielens, Nicole ^b   Moali, Catherine ^a   Hulmes, David J S ^a  

^a UNIVERSITÉ LYON 1   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c UNIV GRENOBLE ALPES   (France)

^d INSERM   (France)

^e UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1R; PROCOLLAGEN; PROCOLLAGEN C PROTEINASE; PROCOLLAGEN C PROTEINASE ENHANCER PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEMENT ACTIVATION; COMPLEX FORMATION; ENZYME ACTIVITY; ENZYME MECHANISM; KINETICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; RADIATION SCATTERING; SITE DIRECTED MUTAGENESIS; SURFACE PROPERTY;

ANIMALS; BINDING SITES; BONE MORPHOGENETIC PROTEIN 1; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; COLLAGEN TYPE III; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; GLYCOPROTEINS; HEK293 CELLS; HUMANS; KINETICS; MUTAGENESIS, SITE-DIRECTED; POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; SCATTERING, SMALL ANGLE; SURFACE PLASMON RESONANCE;

EID: 84876232536     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300480110     Document Type: Article

References (46)

1. Kisseleva T, Brenner DA (2008) Mechanisms of fibrogenesis. Exp Biol Med (Maywood) 233(2):109-122.
2. Wynn TA, Ramalingam TR (2012) Mechanisms of fibrosis: Therapeutic translation for fibrotic disease. Nat Med 18(7):1028-1040.
3. Moali C, Hulmes DJS (2009) Extracellular and cell surface proteases in wound healing: new players are still emerging. Eur J Dermatol 19(6):552-564.
4. Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118(Pt 7):1341-1353.
5. Kadler KE, Hill A, Canty-Laird EG (2008) Collagen fibrillogenesis: Fibronectin, in-tegrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20(5): 495-501.
6. Kessler E, Takahara K, Biniaminov L, Brusel M, Greenspan DS (1996) Bone morpho-genetic protein-1: The type I procollagen C-proteinase. Science 271(5247):360-362.
7. Li SW, et al. (1996) The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenic protein-1. Proc Natl Acad Sci USA 93(10):5127-5130.
8. Muir A, Greenspan DS (2011) Metalloproteinases in Drosophila to humans that are central players in developmental processes. J Biol Chem 286(49):41905-41911.
9. Moali C, Hulmes DJS (2012) Extracellular Matrix: Pathobiology and Signaling, ed Karamanos NK (De Gruyter, Berlin), pp 539-561.
10. Adar R, Kessler E, Goldberg B (1986) Evidence for a protein that enhances the activity of type I procollagen C-proteinase. Coll Relat Res 6(3):267-277.
11. Steiglitz BM, Keene DR, Greenspan DS (2002) PCOLCE2 encodes a functional procollagen C-proteinase enhancer (PCPE2) that is a collagen-binding protein differing in distribution of expression and post-translational modification from the previously described PCPE1. J Biol Chem 277(51):49820-49830.
12. Moali C, et al. (2005) Substrate-specific modulation of a multisubstrate proteinase. C-terminal processing of fibrillar procollagens is the only BMP-1-dependent activity to be enhanced by PCPE-1. J Biol Chem 280(25):24188-24194.
13. Petropoulou V, Garrigue-Antar L, Kadler KE (2005) Identification of the minimal domain structure of bone morphogenetic protein-1 (BMP-1) for chordinase activity: Chordinase activity is not enhanced by procollagen C-proteinase enhancer-1 (PCPE-1). J Biol Chem 280(24):22616-22623.
14. Ogata I, et al. (1997) Up-regulation of type I procollagen C-proteinase enhancer protein messenger RNA in rats with CCl4-induced liver fibrosis. Hepatology 26(3): 611-617.
15. Kessler-Icekson G, Schlesinger H, Freimann S, Kessler E (2006) Expression of procollagen C-proteinase enhancer-1 in the remodeling rat heart is stimulated by aldo-sterone. Int J Biochem Cell Biol 38(3):358-365.
16. Baicu CF, et al. (2012) Effects of the absence of procollagen C-endopeptidase enhancer-2 on myocardial collagen accumulation in chronic pressure overload. Am J Physiol Heart Circ Physiol 303(2):H234-H240.
17. Kronenberg D, et al. (2009) Strong cooperativity and loose geometry between CUB domains are the basis for procollagen c-proteinase enhancer activity. J Biol Chem 284(48):33437-33446.
18. Vadon-Le Goff S, et al. (2011) Procollagen C-proteinase enhancer stimulates procollagen processing by binding to the C-propeptide region only. J Biol Chem 286(45): 38932-38938.
19. Moschcovich L, et al. (2001) Folding and activity of recombinant human procollagen C-proteinase enhancer. Eur J Biochem 268(10):2991-2996.
20. Bourhis JM, et al. (2012) Structural basis of fibrillar collagen trimerization and related genetic disorders. Nat Struct Mol Biol 19(10):1031-1036.
21. David G, Perez J (2009) Combined sampler robot and high-performance liquid chro-matography: A fully automated system for biological small angle X-ray scattering experiments at the synchrotron SOLEIL SWING beamline. J Appl Cryst 42:892-900.
22. Franke D, Svergun DI (2009) DAMMIF, a program for rapid ab initio shape determination in small-angle scattering. J Appl Cryst 42:342-346.
23. Volkov VV, Svergun DI (2003) Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36:860-864.
24. Petoukhov MV, Svergun DI (2006) Joint use of small-angle X-ray and neutron scattering to study biological macromolecules in solution. Eur Biophys J 35(7):567-576.
25. Andersen CBF, Madsen M, Storm T, Moestrup SK, Andersen GR (2010) Structural basis for receptor recognition of vitamin-B(12)-intrinsic factor complexes. Nature 464(7287):445-448.
26. Gaboriaud C, et al. (2011) Structure and properties of the Ca(2+)-binding CUB domain, a widespread ligand-recognition unit involved in major biological functions. Biochem J 439(2):185-193.
27. Gingras AR, et al. (2011) Structural basis of mannan-binding lectin recognition by its associated serine protease MASP-1: Implications for complement activation. Structure 19(11):1635-1643.
28. Blanc G, et al. (2007) Insights into how CUB domains can exert specific functions while sharing a common fold: Conserved and specific features of the CUB1 domain contribute to the molecular basis of procollagen C-proteinase enhancer-1 activity. J Biol Chem 282(23):16924-16933.
29. Steiglitz BM, et al. (2006) Procollagen C proteinase enhancer 1 genes are important determinants of the mechanical properties and geometry of bone and the ultrastructure of connective tissues. Mol Cell Biol 26(1):238-249.
30. Gregory LA, Thielens NM, Arlaud GJ, Fontecilla-Camps JC, Gaboriaud C (2003) X-ray structure of the Ca2+-binding interaction domain of C1s. Insights into the assembly of the C1 complex of complement. J Biol Chem 278(34):32157-32164.
31. Gregory LA, et al. (2004) The X-ray structure of human mannan-binding lectin-associated protein 19 (MAp19) and its interaction site with mannan-binding lectin and L-ficolin. J Biol Chem 279(28):29391-29397.
32. Teillet F, et al. (2008) Crystal structure of the CUB1-EGF-CUB2 domain of human MASP-1/3 and identification of its interaction sites with mannan-binding lectin and ficolins. J Biol Chem 283(37):25715-25724.
33. Teillet F, et al. (2007) Identification of the site of human mannan-binding lectin involved in the interaction with its partner serine proteases: The essential role of Lys55. J Immunol 178(9):5710-5716.
34. Wallis R, et al. (2004) Localization of the serine protease-binding sites in the collagenlike domain of mannose-binding protein: Indirect effects of naturally occurring mutations on protease binding and activation. J Biol Chem 279(14):14065-14073.
35. Girija UV, Dodds AW, Roscher S, Reid KB, Wallis R (2007) Localization and characterization of the mannose-binding lectin (MBL)-associated-serine protease-2 binding site in rat ficolin-A: Equivalent binding sites within the collagenous domains of MBLs and ficolins. J Immunol 179(1):455-462.
36. Lacroix M, et al. (2009) Residue Lys57 in the collagen-like region of human L-ficolin and its counterpart Lys47 in H-ficolin play a key role in the interaction with the mannan-binding lectin-associated serine proteases and the collectin receptor calreticulin. J Immunol 182(1):456-465.
37. Bally I, et al. (2009) Identification of the C1q-binding Sites of Human C1r and C1s: A refined three-dimensional model of the C1 complex of complement. J Biol Chem 284(29):19340-19348.
38. Chung L, et al. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23(15):3020-3030.
39. 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.
40. Nerenberg PS, Salsas-Escat R, Stultz CM (2008) Do collagenases unwind triple-helical collagen before peptide bond hydrolysis? Reinterpreting experimental observations with mathematical models. Proteins 70(4):1154-1161.
41. 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.
42. Berry R, et al. (2009) Role of dimerization and substrate exclusion in the regulation of bone morphogenetic protein-1 and mammalian tolloid. Proc Natl Acad Sci USA 106(21):8561-8566.
43. Berry R, Jowitt TA, Garrigue-Antar L, Kadler KE, Baldock C (2010) Structural and functional evidence for a substrate exclusion mechanism in mammalian tolloid like-1 (TLL-1) proteinase. FEBS Lett 584(4):657-661.
44. Bernocco S, et al. (2001) Biophysical characterization of the C-propeptide trimer from human procollagen III reveals a tri-lobed structure. J Biol Chem 276(52):48930-48936.
45. Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76(6):2879-2886.
46. Svergun DI, Petoukhov MV, Koch MH (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80(6):2946-2953.