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Roles of the procollagen C-propeptides in health and disease.

Hulmes DJS.

Essays Biochem. 2019 Sep 13;63(3):313-323. doi: 10.1042/EBC20180049. Print 2019 Sep 13. Review.


COL1A1 C-propeptide mutations cause ER mislocalization of procollagen and impair C-terminal procollagen processing.

Barnes AM, Ashok A, Makareeva EN, Brusel M, Cabral WA, Weis M, Moali C, Bettler E, Eyre DR, Cassella JP, Leikin S, Hulmes DJS, Kessler E, Marini JC.

Biochim Biophys Acta Mol Basis Dis. 2019 Sep 1;1865(9):2210-2223. doi: 10.1016/j.bbadis.2019.04.018. Epub 2019 May 2.


Atypical COL3A1 variants (glutamic acid to lysine) cause vascular Ehlers-Danlos syndrome with a consistent phenotype of tissue fragility and skin hyperextensibility.

Ghali N, Baker D, Brady AF, Burrows N, Cervi E, Cilliers D, Frank M, Germain DP, Hulmes DJS, Jacquemont ML, Kannu P, Lefroy H, Legrand A, Pope FM, Robertson L, Vandersteen A, von Klemperer K, Warburton R, Whiteford M, van Dijk FS.

Genet Med. 2019 Sep;21(9):2081-2091. doi: 10.1038/s41436-019-0470-9. Epub 2019 Mar 6.


Lysyl oxidase-like 2 (LOXL2)-mediated cross-linking of tropoelastin.

Schmelzer CEH, Heinz A, Troilo H, Lockhart-Cairns MP, Jowitt TA, Marchand MF, Bidault L, Bignon M, Hedtke T, Barret A, McConnell JC, Sherratt MJ, Germain S, Hulmes DJS, Baldock C, Muller L.

FASEB J. 2019 Apr;33(4):5468-5481. doi: 10.1096/fj.201801860RR. Epub 2019 Jan 24.


Structural Basis for the Acceleration of Procollagen Processing by Procollagen C-Proteinase Enhancer-1.

Pulido D, Sharma U, Vadon-Le Goff S, Hussain SA, Cordes S, Mariano N, Bettler E, Moali C, Aghajari N, Hohenester E, Hulmes DJS.

Structure. 2018 Oct 2;26(10):1384-1392.e3. doi: 10.1016/j.str.2018.06.011. Epub 2018 Aug 2.


Thrombospondin-1 promotes matrix homeostasis by interacting with collagen and lysyl oxidase precursors and collagen cross-linking sites.

Rosini S, Pugh N, Bonna AM, Hulmes DJS, Farndale RW, Adams JC.

Sci Signal. 2018 May 29;11(532). pii: eaar2566. doi: 10.1126/scisignal.aar2566.


Interaction of Complement Defence Collagens C1q and Mannose-Binding Lectin with BMP-1/Tolloid-like Proteinases.

Lacroix M, Tessier A, Dumestre-Pérard C, Vadon-Le Goff S, Gout E, Bruckner-Tuderman L, Kiritsi D, Nyström A, Ricard-Blum S, Moali C, Hulmes DJS, Thielens NM.

Sci Rep. 2017 Dec 5;7(1):16958. doi: 10.1038/s41598-017-17318-w.


Structural basis of homo- and heterotrimerization of collagen I.

Sharma U, Carrique L, Vadon-Le Goff S, Mariano N, Georges RN, Delolme F, Koivunen P, Myllyharju J, Moali C, Aghajari N, Hulmes DJ.

Nat Commun. 2017 Mar 10;8:14671. doi: 10.1038/ncomms14671.


Fibrillar Collagens.

Bella J, Hulmes DJ.

Subcell Biochem. 2017;82:457-490. doi: 10.1007/978-3-319-49674-0_14. Review.


Determination of the substrate repertoire of ADAMTS2, 3, and 14 significantly broadens their functions and identifies extracellular matrix organization and TGF-β signaling as primary targets.

Bekhouche M, Leduc C, Dupont L, Janssen L, Delolme F, Vadon-Le Goff S, Smargiasso N, Baiwir D, Mazzucchelli G, Zanella-Cleon I, Dubail J, De Pauw E, Nusgens B, Hulmes DJ, Moali C, Colige A.

FASEB J. 2016 May;30(5):1741-56. doi: 10.1096/fj.15-279869. Epub 2016 Jan 6.


Clinical, structural, biochemical and X-ray crystallographic correlates of pathogenicity for variants in the C-propeptide region of the COL3A1 gene.

Stembridge NS, Vandersteen AM, Ghali N, Sawle P, Nesbitt M, Pollitt RC, Ferguson DJ, Holden S, Elmslie F, Henderson A, Hulmes DJ, Pope FM.

Am J Med Genet A. 2015 Aug;167A(8):1763-72. doi: 10.1002/ajmg.a.37081. Epub 2015 Apr 5.


BMP-1/tolloid-like proteinases synchronize matrix assembly with growth factor activation to promote morphogenesis and tissue remodeling.

Vadon-Le Goff S, Hulmes DJ, Moali C.

Matrix Biol. 2015 May-Jul;44-46:14-23. doi: 10.1016/j.matbio.2015.02.006. Epub 2015 Feb 18. Review.


Proteolytic control of TGF-β co-receptor activity by BMP-1/tolloid-like proteases revealed by quantitative iTRAQ proteomics.

Delolme F, Anastasi C, Alcaraz LB, Mendoza V, Vadon-Le Goff S, Talantikite M, Capomaccio R, Mevaere J, Fortin L, Mazzocut D, Damour O, Zanella-Cléon I, Hulmes DJ, Overall CM, Valcourt U, Lopez-Casillas F, Moali C.

Cell Mol Life Sci. 2015 Mar;72(5):1009-27. doi: 10.1007/s00018-014-1733-x. Epub 2014 Sep 27.


Upregulation of bone morphogenetic protein-1/mammalian tolloid and procollagen C-proteinase enhancer-1 in corneal scarring.

Malecaze F, Massoudi D, Fournié P, Tricoire C, Cassagne M, Malbouyres M, Hulmes DJ, Moali C, Galiacy SD.

Invest Ophthalmol Vis Sci. 2014 Sep 23;55(10):6712-21. doi: 10.1167/iovs.13-13800.


Type I procollagen C-propeptide defects: study of genotype-phenotype correlation and predictive role of crystal structure.

Symoens S, Hulmes DJ, Bourhis JM, Coucke PJ, De Paepe A, Malfait F.

Hum Mutat. 2014 Nov;35(11):1330-41. doi: 10.1002/humu.22677. Epub 2014 Oct 18.


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

Broder C, Arnold P, Vadon-Le Goff S, Konerding MA, Bahr K, Müller S, Overall CM, Bond JS, Koudelka T, Tholey A, Hulmes DJ, Moali C, Becker-Pauly C.

Proc Natl Acad Sci U S A. 2013 Aug 27;110(35):14219-24. doi: 10.1073/pnas.1305464110. Epub 2013 Aug 12.


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

Bourhis JM, Vadon-Le Goff S, Afrache H, Mariano N, Kronenberg D, Thielens N, Moali C, Hulmes DJ.

Proc Natl Acad Sci U S A. 2013 Apr 16;110(16):6394-9. doi: 10.1073/pnas.1300480110. Epub 2013 Apr 2.


Development of ex vivo organ culture models to mimic human corneal scarring.

Janin-Manificat H, Rovère MR, Galiacy SD, Malecaze F, Hulmes DJ, Moali C, Damour O.

Mol Vis. 2012;18:2896-908. Epub 2012 Dec 1.


Production and crystallization of the C-propeptide trimer from human procollagen III.

Bourhis JM, Mariano N, Zhao Y, Walter TS, El Omari K, Delolme F, Moali C, Hulmes DJ, Aghajari N.

Acta Crystallogr Sect F Struct Biol Cryst Commun. 2012 Oct 1;68(Pt 10):1209-13. doi: 10.1107/S1744309112035294. Epub 2012 Sep 26.


Structural basis of fibrillar collagen trimerization and related genetic disorders.

Bourhis JM, Mariano N, Zhao Y, Harlos K, Exposito JY, Jones EY, Moali C, Aghajari N, Hulmes DJ.

Nat Struct Mol Biol. 2012 Oct;19(10):1031-6. doi: 10.1038/nsmb.2389. Epub 2012 Sep 23.


Sizzled is unique among secreted frizzled-related proteins for its ability to specifically inhibit bone morphogenetic protein-1 (BMP-1)/tolloid-like proteinases.

Bijakowski C, Vadon-Le Goff S, Delolme F, Bourhis JM, Lécorché P, Ruggiero F, Becker-Pauly C, Yiallouros I, Stöcker W, Dive V, Hulmes DJ, Moali C.

J Biol Chem. 2012 Sep 28;287(40):33581-93. Epub 2012 Jul 23.


Procollagen C-proteinase enhancer stimulates procollagen processing by binding to the C-propeptide region only.

Vadon-Le Goff S, Kronenberg D, Bourhis JM, Bijakowski C, Raynal N, Ruggiero F, Farndale RW, Stöcker W, Hulmes DJ, Moali C.

J Biol Chem. 2011 Nov 11;286(45):38932-8. doi: 10.1074/jbc.M111.274944. Epub 2011 Sep 22.


Use of magnetically oriented orthogonal collagen scaffolds for hemi-corneal reconstruction and regeneration.

Builles N, Janin-Manificat H, Malbouyres M, Justin V, Rovère MR, Pellegrini G, Torbet J, Hulmes DJ, Burillon C, Damour O, Ruggiero F.

Biomaterials. 2010 Nov;31(32):8313-22. doi: 10.1016/j.biomaterials.2010.07.066. Epub 2010 Aug 13.


Processing of procollagen III by meprins: new players in extracellular matrix assembly?

Kronenberg D, Bruns BC, Moali C, Vadon-Le Goff S, Sterchi EE, Traupe H, Böhm M, Hulmes DJ, Stöcker W, Becker-Pauly C.

J Invest Dermatol. 2010 Dec;130(12):2727-35. doi: 10.1038/jid.2010.202. Epub 2010 Jul 15.


Role of the netrin-like domain of procollagen C-proteinase enhancer-1 in the control of metalloproteinase activity.

Bekhouche M, Kronenberg D, Vadon-Le Goff S, Bijakowski C, Lim NH, Font B, Kessler E, Colige A, Nagase H, Murphy G, Hulmes DJ, Moali C.

J Biol Chem. 2010 May 21;285(21):15950-9. doi: 10.1074/jbc.M109.086447. Epub 2010 Mar 5.


Strong cooperativity and loose geometry between CUB domains are the basis for procollagen c-proteinase enhancer activity.

Kronenberg D, Vadon-Le Goff S, Bourhis JM, Font B, Eichenberger D, Hulmes DJ, Moali C.

J Biol Chem. 2009 Nov 27;284(48):33437-46. doi: 10.1074/jbc.M109.046128. Epub 2009 Oct 1.


Extracellular and cell surface proteases in wound healing: new players are still emerging.

Moali C, Hulmes DJ.

Eur J Dermatol. 2009 Nov-Dec;19(6):552-64. doi: 10.1684/ejd.2009.0770. Epub 2009 Jul 22. Review.


Development of a reconstructed cornea from collagen-chondroitin sulfate foams and human cell cultures.

Vrana NE, Builles N, Justin V, Bednarz J, Pellegrini G, Ferrari B, Damour O, Hulmes DJ, Hasirci V.

Invest Ophthalmol Vis Sci. 2008 Dec;49(12):5325-31. doi: 10.1167/iovs.07-1599. Epub 2008 Aug 15.


Procollagen C-proteinase enhancer-1 (PCPE-1) interacts with beta2-microglobulin (beta2-m) and may help initiate beta2-m amyloid fibril formation in connective tissues.

Morimoto H, Wada J, Font B, Mott JD, Hulmes DJ, Ookoshi T, Naiki H, Yasuhara A, Nakatsuka A, Fukuoka K, Takatori Y, Ichikawa H, Akagi S, Nakao K, Makino H.

Matrix Biol. 2008 Apr;27(3):211-9. doi: 10.1016/j.matbio.2007.11.005. Epub 2007 Nov 28.


Tissue engineering of the cornea: orthogonal scaffold of magnetically aligned collagen lamellae for corneal stroma reconstruction.

Torbet J, Malbouyres M, Builles N, Justin V, Roulet M, Damour O, Oldberg A, Ruggiero F, Hulmes DJ.

Conf Proc IEEE Eng Med Biol Soc. 2007;2007:6400. No abstract available.


Trimerization of collagen IX alpha-chains does not require the presence of the COL1 and NC1 domains.

Jäälinoja J, Ylöstalo J, Beckett W, Hulmes DJ, Ala-Kokko L.

Biochem J. 2008 Jan 15;409(2):545-54.


Orthogonal scaffold of magnetically aligned collagen lamellae for corneal stroma reconstruction.

Torbet J, Malbouyres M, Builles N, Justin V, Roulet M, Damour O, Oldberg A, Ruggiero F, Hulmes DJ.

Biomaterials. 2007 Oct;28(29):4268-76. Epub 2007 Jul 5.


Enzymatic cleavage specificity of the proalpha1(V) chain processing analysed by site-directed mutagenesis.

Bonod-Bidaud C, Beraud M, Vaganay E, Delacoux F, Font B, Hulmes DJ, Ruggiero F.

Biochem J. 2007 Jul 15;405(2):299-306.


Development of a hemicornea from human primary cell cultures for pharmacotoxicology testing.

Builles N, Bechetoille N, Justin V, André V, Barbaro V, Di Iorio E, Auxenfans C, Hulmes DJ, Damour O.

Cell Biol Toxicol. 2007 Jul;23(4):279-92. Epub 2007 Feb 13.


The crystal structure of the Bacillus anthracis spore surface protein BclA shows remarkable similarity to mammalian proteins.

Réty S, Salamitou S, Garcia-Verdugo I, Hulmes DJ, Le Hégarat F, Chaby R, Lewit-Bentley A.

J Biol Chem. 2005 Dec 30;280(52):43073-8. Epub 2005 Oct 25.


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.

Moali C, Font B, Ruggiero F, Eichenberger D, Rousselle P, François V, Oldberg A, Bruckner-Tuderman L, Hulmes DJ.

J Biol Chem. 2005 Jun 24;280(25):24188-94. Epub 2005 Apr 15.


Inhibition of lysyl oxidase activity can delay phenotypic modulation of chondrocytes in two-dimensional culture.

Farjanel J, Sève S, Borel A, Sommer P, Hulmes DJ.

Osteoarthritis Cartilage. 2005 Feb;13(2):120-8.


Intra-articular hyaluronate in experimental rabbit osteoarthritis can prevent changes in cartilage proteoglycan content.

Hulmes DJ, Marsden ME, Strachan RK, Harvey RE, McInnes N, Gardner DL.

Osteoarthritis Cartilage. 2004 Mar;12(3):232-8.


Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily.

McAlinden A, Smith TA, Sandell LJ, Ficheux D, Parry DA, Hulmes DJ.

J Biol Chem. 2003 Oct 24;278(43):42200-7. Epub 2003 Aug 14.


Low resolution structure determination shows procollagen C-proteinase enhancer to be an elongated multidomain glycoprotein.

Bernocco S, Steiglitz BM, Svergun DI, Petoukhov MV, Ruggiero F, Ricard-Blum S, Ebel C, Geourjon C, Deleage G, Font B, Eichenberger D, Greenspan DS, Hulmes DJ.

J Biol Chem. 2003 Feb 28;278(9):7199-205. Epub 2002 Dec 15.


Interaction properties of the procollagen C-proteinase enhancer protein shed light on the mechanism of stimulation of BMP-1.

Ricard-Blum S, Bernocco S, Font B, Moali C, Eichenberger D, Farjanel J, Burchardt ER, van der Rest M, Kessler E, Hulmes DJ.

J Biol Chem. 2002 Sep 13;277(37):33864-9. Epub 2002 Jul 8.


Building collagen molecules, fibrils, and suprafibrillar structures.

Hulmes DJ.

J Struct Biol. 2002 Jan-Feb;137(1-2):2-10. Review.


Lysyl oxidase-like protein from bovine aorta. Isolation and maturation to an active form by bone morphogenetic protein-1.

Borel A, Eichenberger D, Farjanel J, Kessler E, Gleyzal C, Hulmes DJ, Sommer P, Font B.

J Biol Chem. 2001 Dec 28;276(52):48944-9. Epub 2001 Oct 29.


Biophysical characterization of the C-propeptide trimer from human procollagen III reveals a tri-lobed structure.

Bernocco S, Finet S, Ebel C, Eichenberger D, Mazzorana M, Farjanel J, Hulmes DJ.

J Biol Chem. 2001 Dec 28;276(52):48930-6. Epub 2001 Oct 29.


Unhydroxylated triple helical collagen I produced in transgenic plants provides new clues on the role of hydroxyproline in collagen folding and fibril formation.

Perret S, Merle C, Bernocco S, Berland P, Garrone R, Hulmes DJ, Theisen M, Ruggiero F.

J Biol Chem. 2001 Nov 23;276(47):43693-8. Epub 2001 Sep 13.


Control of heterotypic fibril formation by collagen V is determined by chain stoichiometry.

Chanut-Delalande H, Fichard A, Bernocco S, Garrone R, Hulmes DJ, Ruggiero F.

J Biol Chem. 2001 Jun 29;276(26):24352-9.


Folding and activity of recombinant human procollagen C-proteinase enhancer.

Moschcovich L, Bernocco S, Font B, Rivkin H, Eichenberger D, Chejanovsky N, Hulmes DJ, Kessler E.

Eur J Biochem. 2001 May;268(10):2991-6.


Changes in proteoglycan content of articular cartilage during avian degenerative joint disease.

Anderson-MacKenzie JM, Robins SP, Thorp BH, Hulmes DJ.

Clin Exp Rheumatol. 2001 Mar-Apr;19(2):159-64.


Liquid crystalline ordering of procollagen as a determinant of three-dimensional extracellular matrix architecture.

Martin R, Farjanel J, Eichenberger D, Colige A, Kessler E, Hulmes DJ, Giraud-Guille MM.

J Mol Biol. 2000 Aug 4;301(1):11-7.


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