Literature DB >> 19790060

Thrombin-activatable carboxypeptidase B cleavage of osteopontin regulates neutrophil survival and synoviocyte binding in rheumatoid arthritis.

Shadi A Sharif1, Xiaoyan Du, Timothy Myles, Jason J Song, Elizabeth Price, David M Lee, Stuart B Goodman, Mariko Nagashima, John Morser, William H Robinson, Lawrence L K Leung.   

Abstract

OBJECTIVE: Osteopontin (OPN) is a proinflammatory cytokine that plays an important role in the pathogenesis of rheumatoid arthritis (RA). OPN can be cleaved by thrombin, resulting in OPN-R and exposing the cryptic C-terminal alpha4beta1 and alpha9beta1 integrin-binding motif (SVVYGLR). Thrombin-activatable carboxypeptidase B (CPB), also called thrombin-activatable fibrinolysis inhibitor, removes the C-terminal arginine from OPN-R, generating OPN-L and abrogating its enhanced cell binding. We undertook this study to investigate the roles of OPN-R and OPN-L in synoviocyte adhesion, which contributes to the formation of invasive pannus, and in neutrophil survival, which affects inflammatory infiltrates in RA.
METHODS: Using specifically developed enzyme-linked immunosorbent assays, we tested the synovial fluid of patients with RA, osteoarthritis (OA), and psoriatic arthritis (PsA) to determine OPN-R, OPN-L, and full-length OPN (OPN-FL) levels.
RESULTS: Elevated levels of OPN-R and OPN-L were found in synovial fluid samples from RA patients, but not in samples from OA or PsA patients. Increased levels of OPN-R and OPN-L correlated with increased levels of multiple inflammatory cytokines, including tumor necrosis factor alpha and interleukin-6. Immunohistochemical analyses revealed robust expression of OPN-FL, but only minimal expression of OPN-R, in RA synovium, suggesting that cleaved OPN is released into synovial fluid. In cellular assays, OPN-FL, and to a lesser extent OPN-R and OPN-L, had an antiapoptotic effect on neutrophils. OPN-R augmented RA fibroblast-like synoviocyte binding mediated by SVVYGLR binding to alpha4beta1, whereas OPN-L did not.
CONCLUSION: Thrombin activation of OPN (resulting in OPN-R) and its subsequent inactivation by thrombin-activatable CPB (generating OPN-L) occurs locally within inflamed joints in RA. Our data suggest that thrombin-activatable CPB plays a central homeostatic role in RA by regulating neutrophil viability and reducing synoviocyte adhesion.

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Year:  2009        PMID: 19790060      PMCID: PMC3757557          DOI: 10.1002/art.24814

Source DB:  PubMed          Journal:  Arthritis Rheum        ISSN: 0004-3591


  35 in total

Review 1.  Osteopontin (Eta-1) in cell-mediated immunity: teaching an old dog new tricks.

Authors:  A W O'Regan; G J Nau; G L Chupp; J S Berman
Journal:  Immunol Today       Date:  2000-10

Review 2.  Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival.

Authors:  D T Denhardt; M Noda; A W O'Regan; D Pavlin; J S Berman
Journal:  J Clin Invest       Date:  2001-05       Impact factor: 14.808

3.  Identification of dual alpha 4beta1 integrin binding sites within a 38 amino acid domain in the N-terminal thrombin fragment of human osteopontin.

Authors:  K J Bayless; G E Davis
Journal:  J Biol Chem       Date:  2001-01-25       Impact factor: 5.157

4.  The integrin alpha(9)beta(1) binds to a novel recognition sequence (SVVYGLR) in the thrombin-cleaved amino-terminal fragment of osteopontin.

Authors:  Y Yokosaki; N Matsuura; T Sasaki; I Murakami; H Schneider; S Higashiyama; Y Saitoh; M Yamakido; Y Taooka; D Sheppard
Journal:  J Biol Chem       Date:  1999-12-17       Impact factor: 5.157

5.  Amelioration of collagen-induced arthritis by thrombin inhibition.

Authors:  I Marty; V Péclat; G Kirdaite; R Salvi; A So; N Busso
Journal:  J Clin Invest       Date:  2001-03       Impact factor: 14.808

6.  Expression of osteopontin messenger RNA and protein in rheumatoid arthritis: effects of osteopontin on the release of collagenase 1 from articular chondrocytes and synovial fibroblasts.

Authors:  P K Petrow; K M Hummel; J Schedel; J K Franz; C L Klein; U Müller-Ladner; J Kriegsmann; P L Chang; C W Prince; R E Gay; S Gay
Journal:  Arthritis Rheum       Date:  2000-07

7.  Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin).

Authors:  R Agnihotri; H C Crawford; H Haro; L M Matrisian; M C Havrda; L Liaw
Journal:  J Biol Chem       Date:  2001-05-25       Impact factor: 5.157

8.  Analysis of the alpha4beta1 integrin-osteopontin interaction.

Authors:  S T Barry; S B Ludbrook; E Murrison; C M Horgan
Journal:  Exp Cell Res       Date:  2000-08-01       Impact factor: 3.905

Review 9.  Thrombin signalling and protease-activated receptors.

Authors:  S R Coughlin
Journal:  Nature       Date:  2000-09-14       Impact factor: 49.962

10.  Thrombin hydrolysis of human osteopontin is dependent on thrombin anion-binding exosites.

Authors:  Timothy Myles; Lawrence L K Leung
Journal:  J Biol Chem       Date:  2008-04-14       Impact factor: 5.157

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  31 in total

1.  Chemerin158K protein is the dominant chemerin isoform in synovial and cerebrospinal fluids but not in plasma.

Authors:  Lei Zhao; Yasuto Yamaguchi; Shadi Sharif; Xiao-Yan Du; Jason J Song; David M Lee; Lawrence D Recht; William H Robinson; John Morser; Lawrence L K Leung
Journal:  J Biol Chem       Date:  2011-09-19       Impact factor: 5.157

2.  Osteopontin controls immunosuppression in the tumor microenvironment.

Authors:  Michael R Shurin
Journal:  J Clin Invest       Date:  2018-11-05       Impact factor: 14.808

Review 3.  Role of osteopontin in the pathophysiology of cancer.

Authors:  Lalita A Shevde; Rajeev S Samant
Journal:  Matrix Biol       Date:  2014-03-19       Impact factor: 11.583

4.  Angiotensin 1-7, but not the thrombin-cleaved osteopontin C-terminal fragment, attenuates osteopontin-mediated macrophage-induced endothelial-cell inflammation.

Authors:  Rachel Hamias; Assaf Rudich; George Greenberg; Gabriel Szendro; Talya Wolak
Journal:  Inflamm Res       Date:  2017-11-27       Impact factor: 4.575

5.  TAFI deficiency causes maladaptive vascular remodeling after hemophilic joint bleeding.

Authors:  Tine Wyseure; Tingyi Yang; Jenny Y Zhou; Esther J Cooke; Bettina Wanko; Merissa Olmer; Ruchi Agashe; Yosuke Morodomi; Niels Behrendt; Martin Lotz; John Morser; Annette von Drygalski; Laurent O Mosnier
Journal:  JCI Insight       Date:  2019-10-03

6.  Brief report: carboxypeptidase B serves as a protective mediator in osteoarthritis.

Authors:  Christin M Lepus; Jason J Song; Qian Wang; Catriona A Wagner; Tamsin M Lindstrom; Constance R Chu; Jeremy Sokolove; Lawrence L Leung; William H Robinson
Journal:  Arthritis Rheumatol       Date:  2014-01       Impact factor: 10.995

7.  Elevated levels of full-length and thrombin-cleaved osteopontin during acute dengue virus infection are associated with coagulation abnormalities.

Authors:  Haorile Chagan-Yasutan; Talitha Lea Lacuesta; Lishomwa C Ndhlovu; Shigeru Oguma; Prisca Susan A Leano; Elizabeth Freda O Telan; Toru Kubo; Kouichi Morita; Toshimitsu Uede; Efren M Dimaano; Toshio Hattori
Journal:  Thromb Res       Date:  2014-05-14       Impact factor: 3.944

8.  Thrombin cleavage of osteopontin disrupts a pro-chemotactic sequence for dendritic cells, which is compensated by the release of its pro-chemotactic C-terminal fragment.

Authors:  Zhifei Shao; John Morser; Lawrence L K Leung
Journal:  J Biol Chem       Date:  2014-08-11       Impact factor: 5.157

9.  Osteopontin is cleaved at multiple sites close to its integrin-binding motifs in milk and is a novel substrate for plasmin and cathepsin D.

Authors:  Brian Christensen; Lotte Schack; Eva Kläning; Esben S Sørensen
Journal:  J Biol Chem       Date:  2010-01-13       Impact factor: 5.157

10.  Thrombin-cleaved fragments of osteopontin are overexpressed in malignant glial tumors and provide a molecular niche with survival advantage.

Authors:  Yasuto Yamaguchi; Zhifei Shao; Shadi Sharif; Xiao-Yan Du; Timothy Myles; Milton Merchant; Griffith Harsh; Michael Glantz; Lawrence Recht; John Morser; Lawrence L K Leung
Journal:  J Biol Chem       Date:  2012-11-30       Impact factor: 5.157

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