Literature DB >> 31346034

C-terminal proteolysis of the collagen VI α3 chain by BMP-1 and proprotein convertase(s) releases endotrophin in fragments of different sizes.

Stefanie Elisabeth Heumüller1, Maya Talantikite2, Manon Napoli2, Jean Armengaud3, Matthias Mörgelin4, Ursula Hartmann1, Gerhard Sengle1,5,6,7, Mats Paulsson1,5,6,8, Catherine Moali9, Raimund Wagener10,5,6.   

Abstract

The assembly of collagen VI microfibrils is a multistep process in which proteolytic processing within the C-terminal globular region of the collagen VI α3 chain plays a major role. However, the mechanisms involved remain elusive. Moreover, C5, the short and most C-terminal domain of the α3 chain, recently has been proposed to be released as an adipokine that enhances tumor progression, fibrosis, inflammation, and insulin resistance and has been named "endotrophin." Serum endotrophin could be a useful biomarker to monitor the progression of such disorders as chronic obstructive pulmonary disease, systemic sclerosis, and kidney diseases. Here, using biochemical and isotopic MS-based analyses, we found that the extracellular metalloproteinase bone morphogenetic protein 1 (BMP-1) is involved in endotrophin release and determined the exact BMP-1 cleavage site. Moreover, we provide evidence that several endotrophin-containing fragments are present in various tissues and body fluids. Among these, a large C2-C5 fragment, which contained endotrophin, was released by furin-like proprotein convertase cleavage. By using immunofluorescence microscopy and EM, we also demonstrate that these proteolytic maturations occur after secretion of collagen VI tetramers and during microfibril assembly. Differential localization of N- and C-terminal regions of the collagen VI α3 chain revealed that cleavage products are deposited in tissue and cell cultures. The detailed information on the processing of the collagen VI α3 chain reported here provides a basis for unraveling the function of endotrophin (C5) and larger endotrophin-containing fragments and for refining their use as biomarkers of disease progression.
© 2019 Heumüller et al.

Entities:  

Keywords:  BMP-1; Kunitz domain; Pro-C6; collagen; collagen VI; electron microscopy (EM); endotrophin; extracellular matrix protein; microfibrils; muscular dystrophy; proprotein convertase; protein processing

Mesh:

Substances:

Year:  2019        PMID: 31346034      PMCID: PMC6746452          DOI: 10.1074/jbc.RA119.008641

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  71 in total

1.  A short sequence in the N-terminal region is required for the trimerization of type XIII collagen and is conserved in other collagenous transmembrane proteins.

Authors:  A Snellman; H Tu; T Väisänen; A P Kvist; P Huhtala; T Pihlajaniemi
Journal:  EMBO J       Date:  2000-10-02       Impact factor: 11.598

2.  The N-terminal N5 subdomain of the alpha 3(VI) chain is important for collagen VI microfibril formation.

Authors:  J Fitzgerald; M Mörgelin; C Selan; C Wiberg; D R Keene; S R Lamandé; J F Bateman
Journal:  J Biol Chem       Date:  2001-01-05       Impact factor: 5.157

3.  TEM8 interacts with the cleaved C5 domain of collagen alpha 3(VI).

Authors:  Akash Nanda; Eleanor B Carson-Walter; Steven Seaman; Thomas D Barber; Jason Stampfl; Sujay Singh; Bert Vogelstein; Kenneth W Kinzler; Brad St Croix
Journal:  Cancer Res       Date:  2004-02-01       Impact factor: 12.701

4.  Proteinases of the bone morphogenetic protein-1 family convert procollagen VII to mature anchoring fibril collagen.

Authors:  Anke Rattenholl; William N Pappano; Manuel Koch; Douglas R Keene; Karl E Kadler; Takako Sasaki; Rupert Timpl; Robert E Burgeson; Daniel S Greenspan; Leena Bruckner-Tuderman
Journal:  J Biol Chem       Date:  2002-05-01       Impact factor: 5.157

5.  The C5 domain of Col6A3 is cleaved off from the Col6 fibrils immediately after secretion.

Authors:  T Aigner; L Hambach; S Söder; U Schlötzer-Schrehardt; E Pöschl
Journal:  Biochem Biophys Res Commun       Date:  2002-01-18       Impact factor: 3.575

6.  Mutations in COL6A3 cause severe and mild phenotypes of Ullrich congenital muscular dystrophy.

Authors:  Ercan Demir; Patrizia Sabatelli; Valérie Allamand; Ana Ferreiro; Behzad Moghadaszadeh; Mohamed Makrelouf; Haluk Topaloglu; Bernard Echenne; Luciano Merlini; Pascale Guicheney
Journal:  Am J Hum Genet       Date:  2002-04-24       Impact factor: 11.025

7.  Procollagen VII self-assembly depends on site-specific interactions and is promoted by cleavage of the NC2 domain with procollagen C-proteinase.

Authors:  Morgana Colombo; Raymond J Brittingham; John F Klement; Ireneusz Majsterek; David E Birk; Jouni Uitto; Andrzej Fertala
Journal:  Biochemistry       Date:  2003-10-07       Impact factor: 3.162

8.  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.

Authors:  William N Pappano; Barry M Steiglitz; Ian C Scott; Douglas R Keene; Daniel S Greenspan
Journal:  Mol Cell Biol       Date:  2003-07       Impact factor: 4.272

9.  The PeptideAtlas project.

Authors:  Frank Desiere; Eric W Deutsch; Nichole L King; Alexey I Nesvizhskii; Parag Mallick; Jimmy Eng; Sharon Chen; James Eddes; Sandra N Loevenich; Ruedi Aebersold
Journal:  Nucleic Acids Res       Date:  2006-01-01       Impact factor: 16.971

10.  Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency.

Authors:  William A Irwin; Natascha Bergamin; Patrizia Sabatelli; Carlo Reggiani; Aram Megighian; Luciano Merlini; Paola Braghetta; Marta Columbaro; Dino Volpin; Giorgio M Bressan; Paolo Bernardi; Paolo Bonaldo
Journal:  Nat Genet       Date:  2003-11-16       Impact factor: 38.330

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  10 in total

1.  Structure of a collagen VI α3 chain VWA domain array: adaptability and functional implications of myopathy causing mutations.

Authors:  Herimela Solomon-Degefa; Jan M Gebauer; Cy M Jeffries; Carolin D Freiburg; Patrick Meckelburg; Louise E Bird; Ulrich Baumann; Dmitri I Svergun; Raymond J Owens; Jörn M Werner; Elmar Behrmann; Mats Paulsson; Raimund Wagener
Journal:  J Biol Chem       Date:  2020-07-21       Impact factor: 5.157

2.  Critical Role of Matrix Metalloproteinase 14 in Adipose Tissue Remodeling during Obesity.

Authors:  Xin Li; Yueshui Zhao; Chuan Chen; Li Yang; Hyun-Ho Lee; Zening Wang; Ningyan Zhang; Mikhail G Kolonin; Zhiqiang An; Xin Ge; Philipp E Scherer; Kai Sun
Journal:  Mol Cell Biol       Date:  2020-03-30       Impact factor: 4.272

3.  Collagen VI Muscle Disorders: Mutation Types, Pathogenic Mechanisms and Approaches to Therapy.

Authors:  Shireen R Lamandé
Journal:  Adv Exp Med Biol       Date:  2021       Impact factor: 2.622

4.  Circulating Levels of Endotrophin Are Prognostic for Long-Term Mortality after AKI.

Authors:  Nadja Sparding; Daniel Guldager Kring Rasmussen; Federica Genovese; Morten Asser Karsdal; Mads Hornum; Bo Feldt-Rasmussen; Rebecca Packington; Nicholas M Selby
Journal:  Kidney360       Date:  2022-03-03

5.  Collagen VI Regulates Motor Circuit Plasticity and Motor Performance by Cannabinoid Modulation.

Authors:  Daniel D Lam; Rhîannan H Williams; Ernesto Lujan; Koji Tanabe; Georg Huber; Nay Lui Saw; Juliane Merl-Pham; Aaro V Salminen; David Lohse; Sally Spendiff; Melanie J Plastini; Michael Zech; Hanns Lochmüller; Arie Geerlof; Stefanie M Hauck; Mehrdad Shamloo; Marius Wernig; Juliane Winkelmann
Journal:  J Neurosci       Date:  2021-12-27       Impact factor: 6.709

6.  A 9-kDa matricellular SPARC fragment released by cathepsin D exhibits pro-tumor activity in the triple-negative breast cancer microenvironment.

Authors:  Lindsay B Alcaraz; Aude Mallavialle; Timothée David; Danielle Derocq; Frédéric Delolme; Cindy Dieryckx; Caroline Mollevi; Florence Boissière-Michot; Joëlle Simony-Lafontaine; Stanislas Du Manoir; Pitter F Huesgen; Christopher M Overall; Sophie Tartare-Deckert; William Jacot; Thierry Chardès; Séverine Guiu; Pascal Roger; Thomas Reinheckel; Catherine Moali; Emmanuelle Liaudet-Coopman
Journal:  Theranostics       Date:  2021-04-15       Impact factor: 11.556

7.  Endotrophin, a pro-peptide of Type VI collagen, is a biomarker of survival in cirrhotic patients with hepatocellular carcinoma.

Authors:  Diana Julie Leeming; Signe Holm Nielsen; Roslyn Vongsuvanh; Pruthviraj Uchila; Mette Juul Nielsen; Alexander L Reese-Petersen; David van der Poorten; Mohammed Eslam; Detlef Schuppan; Morten Asser Karsdal; Jacob George
Journal:  Hepat Oncol       Date:  2020-12-18

Review 8.  The Biological Role of the Collagen Alpha-3 (VI) Chain and Its Cleaved C5 Domain Fragment Endotrophin in Cancer.

Authors:  Jingya Wang; Wensheng Pan
Journal:  Onco Targets Ther       Date:  2020-06-22       Impact factor: 4.147

9.  Gene Expression Profiling of the Extracellular Matrix Signature in Macrophages of Different Activation Status: Relevance for Skin Wound Healing.

Authors:  Julia Etich; Manuel Koch; Raimund Wagener; Frank Zaucke; Mario Fabri; Bent Brachvogel
Journal:  Int J Mol Sci       Date:  2019-10-14       Impact factor: 5.923

10.  Lack of evidence for a role of anthrax toxin receptors as surface receptors for collagen VI and for its cleaved-off C5 domain/endotrophin.

Authors:  Matthias Przyklenk; Stefanie Elisabeth Heumüller; Carolin Freiburg; Steffen Lütke; Gerhard Sengle; Manuel Koch; Mats Paulsson; Alvise Schiavinato; Raimund Wagener
Journal:  iScience       Date:  2022-09-12
  10 in total

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