CCN2/CTGF is required for matrix organization and to protect growth plate chondrocytes from cellular stress

Journal of Cell Communication and Signaling

Volumn 7, Issue 3, 2013, Pages 219-230

  Hall Glenn, Faith ^a   Aivazi, Armen ^a,e   Akopyan, Lusi ^a,f   Ong, Jessica R ^a   Baxter, Ruth R ^a   Benya, Paul D ^a   Goldschmeding, Roel ^b   Van Nieuwenhoven, Frans A ^c   Hunziker, Ernst B ^d   Lyons, Karen M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF BERN   (Switzerland)

^e STONY BROOK UNIVERSITY   (United States)

^f WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

Autophagy; Cartilage; CCN2 CTGF; Cellular stress; Chondrocytes; Nuclear factor B

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CARTILAGE CELL; CELL PROTECTION; CELL STRESS; CELL SURVIVAL; CHONDRODYSPLASIA; EXTRACELLULAR MATRIX; GROWTH PLATE; IMMUNOFLUORESCENCE; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

EID: 84880333471     PISSN: 18739601     EISSN: 1873961X     Source Type: Journal    
DOI: 10.1007/s12079-013-0201-y     Document Type: Article

References (52)

1. Ahmed YA, Tatarczuch L, Pagel CN, Davies HM, Mirams M, Mackie EJ (2007) Physiological death of hypertrophic chondrocytes. Osteoarthr Cartil OARS Osteoarthr Res Soc 15(5):575-586 (Pubitemid 46667715)
2. Altaf FM, Hering TM, Kazmi NH, Yoo JU, Johnstone B (2006) Ascorbate-enhanced chondrogenesis of ATDC5 cells. Eur Cell Mater 12:64-69, discussion 69-70 (Pubitemid 44898118)
3. Araki K, Araki M, Miyazaki J, Vassalli P (1995) Site-specific recombination of a transgene in fertilized eggs by transient expression of Cre recombinase. Proc Natl Acad Sci U S A 92(1):160-164
4. Aszodi A, Hunziker EB, Brakebusch C, Fassler R (2003) Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev 17(19):2465-2479 (Pubitemid 37214793)
5. Avivar-Valderas A, Salas E, Bobrovnikova-Marjon E, Diehl JA, Nagi C, Debnath J, Aguirre-Ghiso JA (2011) PERK integrates autophagy and oxidative stress responses to promote survival during extracellular matrix detachment. Mol Cell Biol 31(17):3616-3629
6. Barbieri O, Astigiano S, Morini M, Tavella S, Schito A, Corsi A, Di Martino D, Bianco P, Cancedda R, Garofalo S (2003) Depletion of cartilage collagen fibrils in mice carrying a dominant negative Col2a1 transgene affects chondrocyte differentiation. Am J Physiol Cell Physiol 285(6):C1504-C1512
7. Bateman JF, Boot-Handford RP, Lamande SR (2009) Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nature reviews. Genetics 10(3):173-183
8. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2(6):326-332
9. Blaney Davidson EN, Vitters EL, Mooren FM, Oliver N, Berg WB, van der Kraan PM (2006) Connective tissue growth factor/CCN2 overexpression in mouse synovial lining results in transient fibrosis and cartilage damage. Arthritis Rheum 54(5):1653-1661
10. Bornstein P (2009) Matricellular proteins: an overview. J Cell Commun Signal 3(3-4):163-165
11. Brigstock DR (2010) Connective tissue growth factor (CCN2, CTGF) and organ fibrosis: lessons from transgenic animals. J Cell Commun Signal 4(1):1-4
12. Chaqour B, Yang R, Sha Q (2006) Mechanical stretch modulates the promoter activity of the profibrotic factor CCN2 through increased actin polymerization and NF-kappaB activation. J Biol Chem 281(29):20608-20622 (Pubitemid 44065832)
13. Chen CC, Lau LF (2009) Functions and mechanisms of action of CCN matricellular proteins. Int J Biochem Cell Biol 41(4):771-783
14. Copetti T, Bertoli C, Dalla E, Demarchi F, Schneider C (2009) p65/RelA modulates BECN1 transcription and autophagy. Mol Cell Biol 29(10):2594-2608
15. Gao R, Brigstock DR (2005) Activation of nuclear factor kappa B (NF-kappaB) by connective tissue growth factor (CCN2) is involved in sustaining the survival of primary rat hepatic stellate cells. Cell Commun Signal 3:14 (Pubitemid 44848524)
16. Gao R, Brigstock DR (2006) A novel integrin alpha5beta1 binding domain in module 4 of connective tissue growth factor (CCN2/CTGF) promotes adhesion and migration of activated pancreatic stellate cells. Gut 55(6):856-862 (Pubitemid 43764558)
17. Hall-Glenn F, De Young RA, Huang BL, van Handel B, Hofmann JJ, Chen TT, Choi A, Ong JR, Benya PD, Mikkola H, Iruela-Arispe ML, Lyons KM (2012) CCN2/connective tissue growth factor is essential for pericyte adhesion and endothelial basement membrane formation during angiogenesis. PLoS One 7(2):e30562
18. Hamamura K, Goldring MB, Yokota H (2009) Involvement of p38 MAPK in regulation of MMP13 mRNA in chondrocytes in response to surviving stress to endoplasmic reticulum. Arch Oral Biol 54(3):279-286
19. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stephenson RC, Daluiski A, Lyons KM (2003) Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130(12):2779-2791 (Pubitemid 37069592)
20. Jun JI, Lau LF (2011) Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat Rev Drug Discov 10(12):945-963
21. Kaneko M, Niinuma Y, Nomura Y (2003) Activation signal of nuclear factor-kappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol Pharm Bull 26(7):931-935 (Pubitemid 41685414)
22. Kawaki H, Kubota S, Suzuki A, Lazar N, Yamada T, Matsumura T, Ohgawara T, Maeda T, Perbal B, Lyons KM, Takigawa M (2008) Cooperative regulation of chondrocyte differentiation by CCN2 and CCN3 shown by a comprehensive analysis of the CCN family proteins in cartilage. J Bone Miner Res 23(11):1751-1764
23. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T (2007) ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14(2):230-239 (Pubitemid 46092226)
24. Lee GM, Poole CA, Kelley SS, Chang J, Caterson B (1997) Isolated chondrons: a viable alternative for studies of chondrocyte metabolism in vitro. Osteoarthr Cartil 5(4):261-274 (Pubitemid 27315905)
25. Lengner CJ, Lepper C, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2004) Primary mouse embryonic fibroblasts: a model of mesenchymal cartilage formation. J Cell Physiol 200(3):327-333 (Pubitemid 39006923)
26. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS (2008) The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ 15(9):1460-1471
27. Lotz MK, Carames B (2011) Autophagy and cartilage homeostasis mechanisms in joint health, aging and OA. Nat Rev Rheumatol 7(10):579-587
28. Marcu KB, Otero M, Olivotto E, Borzi RM, Goldring MB (2010) NF-kappaB signaling: multiple angles to target OA. Current Drug Targets 11(5):599-613
29. Marino G, Fernandez AF, Cabrera S, Lundberg YW, Cabanillas R, Rodriguez F, Salvador-Montoliu N, Vega JA, Germana A, Fueyo A, Freije JM, Lopez-Otin C (2010) Autophagy is essential for mouse sense of balance. J Clin Investig 120(7):2331-2344
30. Mehrpour M, Esclatine A, Beau I, Codogno P (2010) Overview of macroautophagy regulation in mammalian cells. Cell Res 20(7):748-762
31. Ni M, Zhang Y, Lee AS (2011) Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. Biochem J 434(2):181-188
32. Nishida T, Kubota S, Kojima S, Kuboki T, Nakao K, Kushibiki T, Tabata Y, Takigawa M (2004) Regeneration of defects in articular cartilage in rat knee joints by CCN2 (connective tissue growth factor). J Bone Miner Res 19(8):1308-1319 (Pubitemid 41094373)
33. Nishida T, Kawaki H, Baxter RM, Deyoung RA, Takigawa M, Lyons KM (2007) CCN2 (Connective Tissue Growth Factor) is essential for extracellular matrix production and integrin signaling in chondrocytes. J Cell Commun Signal 1(1):45-58
34. Nozaki S, Sledge GW Jr, Nakshatri H (2001) Repression of GADD153/CHOP by NF-kappaB: a possible cellular defense against endoplasmic reticulum stress-induced cell death. Oncogene 20(17):2178-2185 (Pubitemid 32424012)
35. Nugent AE, McBurney DL, Horton WE Jr (2011) The presence of extracellular matrix alters the chondrocyte response to endoplasmic reticulum stress. J Cell Biochem 112(4):1118-1129
36. Omoto S, Nishida K, Yamaai Y, Shibahara M, Nishida T, Doi T, Asahara H, Nakanishi T, Inoue H, Takigawa M (2004) Expression and localization of connective tissue growth factor (CTGF/Hcs24/CCN2) in osteoarthritic cartilage. Osteoarthr Cartil 12(10):771-778 (Pubitemid 39272839)
37. Ovchinnikov DA, Deng JM, Ogunrinu G, Behringer RR (2000) Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 26(2):145-146 (Pubitemid 30158102)
38. Park M, Yong Y, Choi SW, Kim JH, Lee JE, Kim DW (2007) Constitutive RelA activation mediated by Nkx3.2 controls chondrocyte viability. Nat Cell Biol 9(3):287-298 (Pubitemid 46344608)
39. Pulai JI, Del Carlo M Jr, Loeser RF (2002) The alpha5beta1 integrin provides matrix survival signals for normal and osteoarthritic human articular chondrocytes in vitro. Arthritis Rheum 46(6):1528-1535 (Pubitemid 34620199)
40. Rasheva VI, Domingos PM (2009) Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 14(8):996-1007
41. Sen T, Dutta A, Chatterjee A (2010) Epigallocatechin-3-gallate (EGCG) regulates gelatinase-B (MMP-9) by involvement of FAK/ERK/NFkappaB and AP-1 in the human breast cancer cell line MDA-MB-231. Anti-cancer drugs 21(6):632-644
42. Sirabella R, Secondo A, Pannaccione A, Scorziello A, Valsecchi V, Adornetto A, Bilo L, Di Renzo G, Annunziato L (2009) Anoxia-induced NF-kappaB-dependent upregulation of NCX1 contributes to Ca2+ refilling into endoplasmic reticulum in cortical neurons. Stroke J Cereb Circ 40(3):922-929
43. Srinivas V, Bohensky J, Shapiro IM (2009) Autophagy: a new phase in the maturation of growth plate chondrocytes is regulated by HIF, mTOR and AMP kinase. Cells Tissues Organs 189(1-4):88-92
44. Szafranski JD, Grodzinsky AJ, Burger E, Gaschen V, Hung HH, Hunziker EB (2004) Chondrocyte mechanotransduction: effects of compression on deformation of intracellular organelles and relevance to cellular biosynthesis. Osteoarthr Cartil 12(12):937-946 (Pubitemid 39618448)
45. Tan TW, Lai CH, Huang CY, Yang WH, Chen HT, Hsu HC, Fong YC, Tang CH (2009) CTGF enhances migration and MMP-13 up-regulation via alphavbeta3 integrin, FAK, ERK, and NF-kappaB-dependent pathway in human chondrosarcoma cells. J Cell Biochem 107(2):345-356
46. Tsang KY, Chan D, Cheslett D, Chan WC, So CL, Melhado IG, Chan TW, Kwan KM, Hunziker EB, Yamada Y, Bateman JF, Cheung KM, Cheah KS (2007) Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol 5(3):e44 (Pubitemid 46422975)
47. Voncken JW (2011) Genetic modification of the mouse: general technology - pronuclear and blastocyst injection. Methods Mol Biol 693:11-36
48. Vranka J, Mokashi A, Keene DR, Tufa S, Corson G, Sussman M, Horton WA, Maddox K, Sakai L, Bachinger HP (2001) Selective intracellular retention of extracellular matrix proteins and chaperones associated with pseudoachondroplasia. Matrix Biol 20(7):439-450 (Pubitemid 33016381)
49. Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334(6059):1081-1086
50. Wu S, Flint JK, Rezvani G, De Luca F (2007) Nuclear factor-kappaB p65 facilitates longitudinal bone growth by inducing growth plate chondrocyte proliferation and differentiation and by preventing apoptosis. J Biol Chem 282(46):33698-33706 (Pubitemid 350159544)
51. Yang L, Carlson SG, McBurney D, Horton WE Jr (2005) Multiple signals induce endoplasmic reticulum stress in both primary and immortalized chondrocytes resulting in loss of differentiation, impaired cell growth, and apoptosis. J Biol Chem 280(35):31156-31165 (Pubitemid 41291852)
52. Zahir N, Lakins JN, Russell A, Ming W, Chatterjee C, Rozenberg GI, Marinkovich MP, Weaver VM (2003) Autocrine laminin-5 ligates alpha6beta4 integrin and activates RAC and NFkappaB to mediate anchorage-independent survival of mammary tumors. J Cell Biol 163(6):1397-1407 (Pubitemid 38032099)