Biomechanical signals and the C-type natriuretic peptide counteract catabolic activities induced by IL-1β in chondrocyte/agarose constructs

Arthritis Research and Therapy

Volumn 13, Issue 5, 2011, Pages

  Ramachandran, Manoj ^b   Achan, Prim ^b   Salter, Donald M ^c   Bader, Dan L ^a   Chowdhury, Tina T ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGAROSE; AGGRECAN; COLLAGEN TYPE 2; CYCLOOXYGENASE 2; INTERLEUKIN 1BETA; NATRIURETIC PEPTIDE TYPE C; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROSTAGLANDIN E2; RNA; SULFATE; THYMIDINE; SEPHAROSE;

ARTICLE; BIOSYNTHESIS; CARTILAGE CELL; CATABOLISM; CELL ACTIVITY; CYTOKINE RELEASE; GENE EXPRESSION; HORMONE RELEASE; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; ADULT; BIOMECHANICS; CELL CULTURE; COMPARATIVE STUDY; FEMALE; MALE; METABOLISM; MIDDLE AGED; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADULT; BIOMECHANICS; CELLS, CULTURED; CHONDROCYTES; FEMALE; HUMANS; INTERLEUKIN-1BETA; MALE; METABOLISM; MIDDLE AGED; NATRIURETIC PEPTIDE, C-TYPE; SEPHAROSE; SIGNAL TRANSDUCTION;

EID: 80052660771     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3459     Document Type: Article

References (56)

1. Amin AR, Abramson SB. The role of nitric oxide in articular cartilage breakdown in osteoarthritis. Curr Opin Rheumatol 1998, 10:263-268. 10.1097/00002281-199805000-00018, 9608331.
2. Fitzgerald JB, Jin M, Grodzinsky AJ. Shear and compression differentially regulate clusters of functionally related temporal transcription patterns in cartilage tissue. J Biol Chem 2006, 281:24095-24103. 10.1074/jbc.M510858200, 16782710.
3. Millward-Sadler SJ, Salter DM. Integrin-dependent signal cascades in chondrocyte mechanotransduction. Ann Biomed Eng 2004, 32:435-446.
4. Malemud CJ. Protein kinases in chondrocyte signaling and osteoarthritis. Clin Orthop Relat Res 2004, (427 Suppl):S145-S151.
5. Griffin TM, Guilak F. The role of mechanical loading in the onset and progression of osteoarthritis. Exerc Sport Sci Rev 2005, 33:195-200. 10.1097/00003677-200510000-00008, 16239837.
6. Blom AB, van der Kraan PM, van den Berg WB. Cytokine targeting in osteoarthritis. Curr Drug Targets 2007, 8:283-292. 10.2174/138945007779940179, 17305506.
7. Guilak F, Fermor B, Keefe FJ, Kraus VB, Olson SA, Pisetsky DS, Setton LA, Weinberg JB. The role of biomechanics and inflammation in cartilage injury and repair. 2004, 423:17-26.
8. Loeser RF. Molecular mechanisms of cartilage destruction: mechanics, inflammatory mediators, and aging collide. Arthritis Rheum 2006, 54:1357-1360. 10.1002/art.21813, 1774815, 16645963.
9. Chusho H, Tamura N, Ogawa Y, Yasoda A, Suda M, Miyazawa T, Nakamura K, Nakao K, Kurihara T, Komatsu Y, Itoh H, Tanaka K, Saito Y, Katsuki M, Nakao K. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc Natl Acad Sci USA 2001, 98:4016-4021. 10.1073/pnas.071389098, 31171, 11259675.
10. Schulz S. C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides 2005, 26:1024-1034. 10.1016/j.peptides.2004.08.027, 15911070.
11. Kuhn M. Molecular physiology of natriuretic peptide signalling. Basic Res Cardiol 2004, 99:76-82. 10.1007/s00395-004-0460-0, 14963665.
12. Krejci P, Masri B, Fontaine V, Mekikian PB, Weis M, Prats H, Wilcox WR. Interaction of fibroblast growth factor and C-natriuretic peptide signaling in regulation of chondrocyte proliferation and extracellular matrix homeostasis. J Cell Sci 2005, 118:5089-5100. 10.1242/jcs.02618, 16234329.
13. Waldman SD, Usmani Y, Tse MY, Pang SC. Differential effects of natriuretic peptide stimulation on tissue engineered cartilage. Tissue Eng Part A 2008, 14:441-448. 10.1089/tea.2007.0035, 18333796.
14. Agoston H, Baybayan L, Beier F. Dexamethasone stimulates expression of C-type natriuretic peptide in chondrocytes. BMC Musculoskel Disord 2006, 7:87.
15. Hagiwara H, Sakaguchi H, Itakura M, Yoshimoto T, Furuya M, Tanaka S, Hirose S. Autocrine regulation of rat chondrocyte proliferation by natriuretic peptide C and its receptor, natriuretic peptide receptor-B. J Biol Chem 1994, 269:10729-10733.
16. Hagiwara H, Inoue A, Yamaguchi A, Yokose S, Furuya M, Tanaka S, Hirose S. cGMP produced in response to ANP and CNP regulates proliferation and differentiation of osteoblastic cells. Am J Physiol 1996, 270:C1311-C1308.
17. Pfeifer A, Ruth P, Dostmann W, Sausbier M, Klatt P, Hofmann F. Structure and function of cGMP-dependent protein kinases. Rev Physiol Biochem Pharmacol 1999, 135:105-149. 10.1007/BFb0033671, 9932482.
18. Komatsu Y, Chusho H, Tamura N, Yasoda A, Miyzawa T, Suda M, Miura M, Ogawa Y, Nako K. Significance of C-type natriuretic peptide (CNP) in endochondral ossification: analysis of CNP knockout mice. J Bone Miner Metab 2002, 20:331-336. 10.1007/s007740200048, 12434160.
19. Yasoda A, Ogawa Y, Suda M, Tamura N, Mori K, Sakuma Y, Chusho H, Shiota K, Tanaka K, Nakao K. Natriuretic peptide regulation of endochondral ossification: evidence for possible roles of the C-type natriuretic peptide/guanylyl cyclase-B pathway. J Biol Chem 1998, 273:11695-11700. 10.1074/jbc.273.19.11695, 9565590.
20. Yasoda A, Komatsu Y, Chusho H, Miyazawa T, Ozasa A, Miura M, Kurihara T, Rogi T, Tanaka S, Suda M, Tamura N, Ogawa Y, Nakao K. Overexpression of CNP in chondrocytes rescues achondroplasia through an MAPK-dependent pathway. Nat Med 2004, 10:80-86. 10.1038/nm971, 14702637.
21. Pelletier JP, DiBattista JA, Roughley P, McCollum R, Martel-Pelletier J. Cytokines and inflammation in cartilage degradation. Rheum Dis Clin North Am 1993, 19:545-568.
22. Saklatvala J. Tumour necrosis factor alpha stimulates resorption and inhibits synthesis of proteoglycan in cartilage. Nature 1986, 322:547-549. 10.1038/322547a0, 3736671.
23. Häuselmann HJ, Oppliger L, Michel BA, Stefanovic-Racic M, Evans CH. Nitric oxide and proteoglycan biosynthesis by human articular chondrocytes in alginate culture. FEBS Lett 1994, 352:361-364. 10.1016/0014-5793(94)00994-5, 7926002.
24. Shakibaei M, John T, Schulze-Tanzil G, Lehmann I, Mobasheri A. Suppression of NF-kappaB activation by curcumin leads to inhibition of expression of cyclo-oxygenase-2 and matrix metalloproteinase-9 in human articular chondrocytes: implications for the treatment of osteoarthritis. Biochem Pharmacol 2007, 73:1434-1445. 10.1016/j.bcp.2007.01.005, 17291458.
25. Deschner J, Hofman CR, Piesco NP, Agarwal S. Signal transduction by mechanical strain in chondrocytes. Curr Opin Clin Nutr Metab Care 2003, 6:289-293.
26. Madhavan S, Anghelina M, Rath-Deschner B, Deschner J, Piesco N, Agarwal S. Biomechanical signals exert sustained attenuation of proinflammatory gene induction in articular chondrocytes. Osteoarthrit Cart 2006, 14:1023-1032.
27. De Croos JN, Dhaliwal SS, Grynpas MD, Pilliar RM, Kandel RA. Cyclic compressive mechanical stimulation induces sequential catabolic and anabolic gene changes in chondrocytes resulting in increased extracellular matrix accumulation. Matrix Biol 2006, 25:323-331. 10.1016/j.matbio.2006.03.005, 16697175.
28. Chowdhury TT, Arghandawi S, Brand J, Akanji OO, Salter DM, Bader DL, Lee DA. Dynamic compression counteracts IL-1β induced inducible nitric oxide synthase and cyclo-oxygenase-2 expression in chondrocyte/agarose constructs. Arthritis Res Ther 2008, 10:R35. 10.1186/ar2389, 2453754, 18348730, 18348730.
29. Chowdhury TT, Bader DL, Lee DA. Dynamic compression inhibits the synthesis of nitric oxide and PGE(2) by IL-1beta-stimulated chondrocytes cultured in agarose constructs. Biophys Res Commun 2001, 285:1168-1174.
30. Das UN. Anti-inflammatory nature of exercise. Nutrition 2004, 20:323-326. 10.1016/j.nut.2003.11.017, 14990277.
31. Bennell K, Hinmann R. Exercise as a treatment for osteoarthritis. Curr Opin Rheumatol 2005, 17:634-640. 10.1097/01.bor.0000171214.49876.38, 16093845.
32. Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol 1999, 515:287-291. 10.1111/j.1469-7793.1999.287ad.x, 2269132, 9925898.
33. Rannou F, Poiraudeau S, Revel M. Cartilage: from biomechanics to physical therapy. Ann Readapt Med Physiol 2001, 44:259-267.
34. Lee DA, Bader DL. Compressive strains at physiological frequencies influence the metabolism of chondrocytes seeded in agarose. J Orthop Res 1997, 15:181-188. 10.1002/jor.1100150205, 9167619.
35. Lee DA, Knight MM. Mechanical loading of chondrocytes embedded in 3D constructs: in vitro methods for assessment of morphological and metabolic response to compressive strain. Methods Mol Med 2004, 100:307-324.
36. Chowdhury TT, Bader DL, Shelton JC, Lee DA. Temporal regulation of chondrocyte metabolism in agarose constructs subjected to dynamic compression. Arch Biochem Biophys 2003, 417:105-111. 10.1016/S0003-9861(03)00340-0, 12921786.
37. Lee DA, Brand J, Salter D, Akanji OO, Chowdhury TT. Quantification of mRNA using real-time PCR and Western blot analysis of MAPK events in chondrocyte/agarose constructs. Methods Mol Biol 2011, 695:77-97. 10.1007/978-1-60761-984-0_6, 21042967.
38. Pejchalova K, Krejci P, Wilcox WR. C-natriuretic peptide: an important regulator of cartilage. Mol Genet Metab 2007, 92:210-215. 10.1016/j.ymgme.2007.06.014, 17681481.
39. Mericq V, Uyeda JA, Barnes KM, De Luca F, Baron J. Regulation of fetal rat bone growth by C-type natriuretic peptide and cGMP. Pediatr Res 2000, 47:189-193. 10.1203/00006450-200002000-00007, 10674345.
40. Suda M, Tanaka K, Yasoda A, Komatsu Y, Chusho H, Miura M, Tamura N, Ogawa Y, Nakao K. C-type natriuretic peptide/guanylate cyclase B system in ATDC5 cells, a chondrogenic cell line. J Bone Miner Metab 2002, 20:136-141. 10.1007/s007740200019, 11984695.
41. Woods A, Khan S, Beier F. C-type natriuretic peptide regulates cellular condensation and glycosaminoglycan synthesis during chondrogenesis. Endocrinology 2007, 148:5030-5041. 10.1210/en.2007-0695, 17640987.
42. Fujishige K, Kotera J, Yanaka N, Akatsuka H, Omori K. Alteration of cGMP metabolism during chondrogenic differentiation of chondroprogenitor-like EC cells, ATDC5. Biochim Biophys Acta 1999, 1452:219-227. 10.1016/S0167-4889(99)00141-X, 10590311.
43. Johnson KA, van Etten D, Nanda N, Graham RM, Terkeltaub RA. Distinct transglutaminase 2-independent and transglutaminase 2-dependent pathways mediate articular chondrocyte hypertrophy. J Biol Chem 2003, 278:18824-18832. 10.1074/jbc.M301055200, 12606540.
44. Chikuda H, Kugimiya F, Hoshi K, Ikeda T, Ogasawara T, Shimoaka T, Kawano H, Kamekura S, Tsuchida A, Yokoi N, Nakamura K, Komeda K, Chung UI, Kawaguchi H. Cyclic GMP-dependent protein kinase II is a molecular switch from proliferation to hypertrophic differentiation of chondrocytes. Genes Dev 2004, 18:2418-2429. 10.1101/gad.1224204, 522991, 15466490.
45. Clancy RM, Amin AR, Abramson SB. The role of nitric oxide in inflammation and immunity. Arthritis Rheum 1998, 41:1141-1151. 10.1002/1529-0131(199807)41:7<1141::AID-ART2>3.0.CO;2-S, 9663469.
46. Studer RK, Decker K, Melhem S, Georgescu H. Nitric oxide inhibition of IGF-1 stimulated proteoglycan synthesis: role of cGMP. J Orthop Res 2003, 21:914-921. 10.1016/S0736-0266(03)00029-9, 12919881.
47. Geng Y, Zhou L, Thompson WJ, Lotz M. Cyclic GMP and cGMP-binding phosphodiesterase are required for interleukin-1-induced nitric oxide synthesis in human articular chondrocytes. J Biol Chem 1998, 273:27484-27491. 10.1074/jbc.273.42.27484, 9765278.
48. Tenor H, Hedbom E, Häuselmann HJ, Schudt C, Hatzelmann A. Phosphodiesterase isoenzyme families in human osteoarthritis chondrocytes: functional importance of phosphodiesterase 4. Br J Pharmacol 2002, 135:609-618. 10.1038/sj.bjp.0704480, 1573165, 11834608.
49. Morales TI. The insulin-like growth factor binding proteins in uncultured human cartilage: increases in insulin-like growth factor binding protein 3 during osteoarthritis. Arthritis Rheum 2002, 46:2358-2367. 10.1002/art.10482, 12355483.
50. Iwanaga H, Matsumoto T, Enomoto H, Okano K, Hishikawa Y, Shindo H, Koji T. Enhanced expression of insulin-like growth factor-binding proteins in human osteoarthritic cartilage detected by immunohistochemistry and in situ hybridization. Osteoarthritis Cart 2005, 13:439-448.
51. Kaupp UB, Seifert R. Cyclic nucleotide-gated ion channels. Physiol Rev 2002, 82:769-824.
52. Lotz M, Hashimoto S, Kühn K. Mechanisms of chondrocyte apoptosis. Osteoarthritis Cart 1999, 7:389-391.
53. Sugimoto T, Yoshino M, Nagao M, Ishii S, Yabu H. Voltage-gated ionic channels in cultured rabbit articular chondrocytes. Comp Biochem Physiol C 1996, 115:223-232.
54. Mobasheri A, Gent TC, Womack MD, Carter SD, Clegg PD, Barrett-Jolley R. Quantitative analysis of voltage-gated potassium currents from primary equine (Equus caballus) and elephant (Loxodonta africana) articular chondrocytes. Am J Physiol Regul Integr Comp Physiol 2005, 289:R172-R180. 10.1152/ajpregu.00710.2004, 15802557.
55. Chowdhury TT, Salter DM, Bader DL, Lee DA. Signal transduction pathways involving p38 MAPK, JNK, NFkappaB and AP-1 influence the response of chondrocytes cultured in agarose constructs to IL-1beta and dynamic compression. Inflam Res 2008, 57:306-313.
56. Chowdhury TT, Knight MM. Purinergic pathway suppresses the release of .NO and stimulates proteoglycan synthesis in chondrocyte/agarose constructs subjected to dynamic compression. J Cell Physiol 2006, 209:845-853. 10.1002/jcp.20768, 16924659.