Clinicopathological correlations of podoplanin (gp38) expression in rheumatoid synovium and its potential contribution to fibroblast platelet crosstalk

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Del Rey, Manuel J ^a   Faré, Regina ^a   Izquierdo, Elena ^b   Usategui, Alicia ^a   RodrÍguez Fernández, José L ^b   Suárez Fueyo, Abel ^a   Cañete, Juan D ^c   Pablos, José L ^a  

^a Universidad Complutense   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CLEC2 PLATELET RECEPTOR; INTERLEUKIN 6; INTERLEUKIN 8; PODOPLANIN; THROMBOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; ANTIRHEUMATIC AGENT; CLEC2B PROTEIN, HUMAN; LECTIN; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

AGED; ARTICLE; CELL INTERACTION; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FIBROBLAST; FIBROBLAST CULTURE; HUMAN; HUMAN TISSUE; IL 6 GENE; IL 8 GENE; IMMUNOHISTOCHEMISTRY; JOINT BIOPSY; MALE; PATHOGENESIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RHEUMATOID ARTHRITIS; RNA INTERFERENCE; SYNOVIUM; THROMBOCYTE; UPREGULATION; ANTAGONISTS AND INHIBITORS; ARTHRITIS, RHEUMATOID; BIOSYNTHESIS; CELL CULTURE; CELL MOTION; GENE EXPRESSION; GENE SILENCING; GENETICS; INFLAMMATION; LYMPHOID TISSUE; METABOLISM; OSTEOARTHRITIS; PATHOLOGY; PHYSIOLOGY; STROMA CELL; VASCULAR ENDOTHELIUM;

ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; BLOOD PLATELETS; CELL MOVEMENT; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIUM, VASCULAR; FIBROBLASTS; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INFLAMMATION; LECTINS, C-TYPE; LYMPHOID TISSUE; MEMBRANE GLYCOPROTEINS; OSTEOARTHRITIS; RNA, SMALL INTERFERING; STROMAL CELLS; SYNOVIAL MEMBRANE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84903281074     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099607     Document Type: Article

References (44)

1. Bartok B, Firestein GS (2010) Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev 233: 233-255.
2. Naylor AJ, Filer A, Buckley CD (2013) The role of stromal cells in the persistence of chronic inflammation. Clin Exp Immunol 171: 30-35.
3. Neumann E, Lefèvre S, Zimmermann B, Gay S, Müller-Ladner U (2010) Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends Mol Med 16: 458-468.
4. Lee A, Qiao Y, Grigoriev G, Chen J, Park-Min KH, et al. (2013) Tumor necrosis factor α induces sustained signaling and a prolonged and unremitting inflammatory response in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 65: 928-938.
5. Müller-Ladner U, Kriegsmann J, Franklin BN, Matsumoto S, Geiler T, et al. (1996) Synovial fibroblasts of patients with rheumatoid arthritis attach to and invade normal human cartilage when engrafted into SCID mice. Am J Pathol 149: 1607-1615. (Pubitemid 26363967)
6. del Rey MJ, Izquierdo E, Caja S, Usategui A, Santiago B, et al. (2009) Human inflammatory synovial fibroblasts induce enhanced myeloid cell recruitment and angiogenesis through a hypoxia-inducible transcription factor 1alpha/vascular endothelial growth factor-mediated pathway in immunodeficient mice. Arthritis Rheum 60: 2926-2934.
7. Bradfield PF, Amft N, Vernon-Wilson E, Exley AE, Parsonage G, et al. (2003) Rheumatoid fibroblast-like synoviocytes overexpress the chemokine stromal cell-derived factor 1 (CXCL12), which supports distinct patterns and rates of CD4+ and CD8+ T cell migration within synovial tissue. Arthritis Rheum 48: 2472-2482. (Pubitemid 37129424)
8. Benito-Miguel M, García-Carmona Y, Balsa A, Bautista-Caro MB, Arroyo-Villa I, et al. (2012) IL-15 expression on RA synovial fibroblasts promotes B cell survival. PLoS One 2012, 7: e40620.
9. Lindhout E, van Eijk M, van Pel M, Lindeman J, Dinant HJ, et al. (1999) Fibroblast-like synoviocytes from rheumatoid arthritis patients have intrinsic properties of follicular dendritic cells. J Immunol 162: 5949-5956. (Pubitemid 29314950)
10. Manzo A, Paoletti S, Carulli M, Blades MC, Barone F, et al. (2005) Systematic microanatomical analysis of CXCL13 and CCL21 in situ production and progressive lymphoid organization in rheumatoid synovitis. Eur J Immunol 35: 1347-1359. (Pubitemid 40691416)
11. Bajénoff M, Egen JG, Koo LY, Laugier JP, Brau F, et al. (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25: 989-1001. (Pubitemid 44914055)
12. Link A, Hardie DL, Favre S, Britschgi MR, Adams DH, et al. (2011) Association of T-zone reticular networks and conduits with ectopic lymphoid tissues in mice and humans. Am J Pathol 178: 1662-1675.
13. Farr AG, Berry ML, Kim A, Nelson AJ, Welch MP, et al. (1992) Characterization and cloning of a novel glycoprotein expressed by stromal cells in T-dependent areas of peripheral lymphoid tissues. J Exp Med 176: 1477-1482.
14. Ekwall AK, Eisler T, Anderberg C, Jin C, Karlsson N, et al. (2011) The tumour-associated glycoprotein podoplanin is expressed in fibroblast-like synoviocytes of the hyperplastic synovial lining layer in rheumatoid arthritis. Arthritis Res Ther 13: R40
15. Kawase A, Ishii G, Nagai K, Ito T, Nagano T, et al. (2008) Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer 123: 1053-1059.
16. Dulauroy S, Di Carlo SE, Langa F, Eberl G, Peduto L (2012) Lineage tracing and genetic ablation of ADAM12(+) perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat Med 18: 1262-1270.
17. Peduto L, Dulauroy S, Lochner M, Späth GF, Morales MA, et al. (2009) Inflammation recapitulates the ontogeny of lymphoid stromal cells. J Immunol 182: 5789-5799.
18. Peters A, Pitcher LA, Sullivan JM, Mitsdoerffer M, Acton SE, et al. (2011) Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 35: 986-996.
19. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, et al. (2006) Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9: 261-272.
20. Martín-Villar E, Megías D, Castel S, Yurrita MM, Vilaró S, et al. (2006) Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J Cell Sci 119: 4541-4553. (Pubitemid 44830653)
21. Navarro A, Perez RE, Rezaiekhaligh MH, Mabry SM, Ekekezie II (2011) Polarized migration of lymphatic endothelial cells is critically dependent on podoplanin regulation of Cdc42. Am J Physiol Lung Cell Mol Physiol 300: L32-42.
22. Schacht V, Ramirez MI, Hong YK, Hirakawa S, Feng D, et al. (2003) T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J 22: 3546-3556. (Pubitemid 36898332)
23. Uhrin P, Zaujec J, Breuss JM, Olcaydu D, Chrenek P, et al. (2010) Novel function for blood platelets and podoplanin in developmental separation of blood and lymphatic circulation. Blood 115: 3997-4005.
24. Suzuki-Inoue K, Inoue O, Ding G, Nishimura S, Hokamura K, et al. (2010) Essential in vivo roles of the C-type lectin receptor CLEC-2: embryonic/neonatal lethality of CLEC-2-deficient mice by blood/lymphatic misconnections and impaired thrombus formation of CLEC-2-deficient platelets. J Biol Chem 285: 24494-24507.
25. Acton SE, Astarita JL, Malhotra D, Lukacs-Kornek V, Franz B, et al. (2012) Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity 37: 276-289.
26. Bertozzi CC, Schmaier AA, Mericko P, Hess PR, Zou Z, et al. (2010) Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood 116: 661-670.
27. Osada M, Inoue O, Ding G, Shirai T, Ichise H, et al. (2012) Platelet activation receptor CLEC-2 regulates blood/lymphatic vessel separation by inhibiting proliferation, migration, and tube formation of lymphatic endothelial cells. J Biol Chem 287: 22241-22252.
28. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, et al. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31: 315-324. (Pubitemid 18091653)
29. Zimmer G, Oeffner F, Von Messling V, Tschernig T, Gröness HJ, et al. (1999) Cloning and characterization of gp36, a human mucin-type glycoprotein preferentially expressed in vascular endothelium. Biochem J 341 (Pt 2): 277-284. (Pubitemid 29373650)
30. Cañete JD, Celis R, Moll C, Izquierdo E, Marsal S, et al. (2009) Clinical significance of synovial lymphoid neogenesis and its reversal after anti-tumour necrosis factor alpha therapy in rheumatoid arthritis. Ann Rheum Dis 68: 751-756.
31. Izquierdo E, Cañete JD, Celis R, Del Rey MJ, Usategui A, et al. (2011) Synovial fibroblast hyperplasia in rheumatoid arthritis: clinicopathologic correlations and partial reversal by anti-tumor necrosis factor therapy. Arthritis Rheum 63: 2575-2583.
32. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, et al. (2005) Upregulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol 166: 913-921. (Pubitemid 40315647)
33. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, et al. (1998) Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72: 9873-9880. (Pubitemid 28520853)
34. Van Gestel AM, Prevoo ML, van't Hof MA, van Rijswijk MH, van de Putte LB, et al. (1996) Development and validation of the European League Against Rheumatism response criteria for rheumatoid arthritis: comparison with the preliminary American College of Rheumatology and the World Health Organization/International League Against Rheumatism criteria. Arthritis Rheum 39: 34-40. (Pubitemid 26036375)
35. Neidhart M, Seemayer CA, Hummel KM, Michel BA, Gay RE, et al. (2003) Functional characterization of adherent synovial fluid cells in rheumatoid arthritis: destructive potential in vitro and in vivo. Arthritis Rheum 48: 1873-1880. (Pubitemid 36828682)
36. Pretzel D, Pohlers D, Weinert S, Kinne RW (2009) In vitro model for the analysis of synovial fibroblast-mediated degradation of intact cartilage. Arthritis Res Ther 11: R25.
37. Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS (2010) Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 327: 580-583.
38. Hsu J, Gu Y, Tan SL, Narula S, DeMartino JA, et al. (2013) Bruton's Tyrosine Kinase mediates platelet receptor-induced generation of microparticles: a potential mechanism for amplification of inflammatory responses in rheumatoid arthritis synovial joints. Immunol Lett 150: 97-104.
39. Boulaftali Y, Hess PR, Getz TM, Cholka A, Stolla M, et al. (2013) Platelet ITAM signaling is critical for vascular integrity in inflammation. J Clin Invest 123: 908-916.
40. Genovese MC, Rubbert-Roth A, Smolen JS, Kremer J, Khraishi M, et al. (2013) Longterm Safety and Efficacy of Tocilizumab in Patients with Rheumatoid Arthritis: A Cumulative Analysis of Up to 4.6 Years of Exposure. J Rheumatol 40: 768-780.
41. Kopf M, Herren S, Wiles MV, Pepys MB, Kosco-Vilbois MH (1998) Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J Exp Med 188: 1895-1906. (Pubitemid 28536777)
42. Choi YS, Eto D, Yang JA, Lao C, Crotty S (2013) Cutting edge: STAT1 is required for IL-6-mediated Bcl6 induction for early follicular helper cell differentiation. J Immunol 190: 3049-3053.
43. Victoratos P, Kollias G (2009) Induction of autoantibody-mediated spontaneous arthritis critically depends on follicular dendritic cells. Immunity 30: 130-142.
44. Timmer TC, Baltus B, Vondenhoff M, Huizinga TW, Tak PP, et al. (2007) Inflammation and ectopic lymphoid structures in rheumatoid arthritis synovial tissues dissected by genomics technology: identification of the interleukin-7 signaling pathway in tissues with lymphoid neogenesis. Arthritis Rheum 56: 2492-2502. (Pubitemid 47237268)