Elevated expression of periostin in human osteoarthritic cartilage and its potential role in matrix degradation via matrix metalloproteinase-13

FASEB Journal

Volumn 29, Issue 10, 2015, Pages 4107-4121

  Attur, Mukundan ^a   Yang, Qing ^a   Shimada, Kohei ^d   Tachida, Yuki ^d   Nagase, Hiroyuki ^d   Mignatti, Paolo ^a,b   Statman, Lauren ^a   Palmer, Glyn ^a,e   Kirsch, Thorsten ^c   Beier, Frank ^f   Abramson, Steven B ^a  

^a NYU HOSPITAL FOR JOINT DISEASES   (United States)

^b Department of Cell Biology ^*  (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DAIICHI SANKYO CO   (Japan)

^e UNIVERSITY OF FLORIDA   (United States)

^f WESTERN UNIVERSITY   (Canada)

Author keywords

ADAMTS; Chondrocytes; Posttraumatic osteoarthritis; Wnt signaling

Indexed keywords

AGGRECANASE 1; BETA CATENIN; BROMIDE; COLLAGEN TYPE 2; COLLAGENASE 3; PROTEOGLYCAN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX2; WNT PROTEIN; ADAM PROTEIN; ADAMTS4 PROTEIN, HUMAN; ADAMTS4 PROTEIN, MOUSE; CELL ADHESION MOLECULE; POSTN PROTEIN, HUMAN; PROCOLLAGEN N PROTEINASE;

ADENOVIRIDAE; ADULT; AGED; ANIMAL CELL; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CARTILAGE EXPLANT; COLLAGEN DEGRADATION; CONTROLLED STUDY; EC50; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; FEMUR CONDYLE; FEMUR HEAD; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KNEE MENISCUS; KNEE OSTEOARTHRITIS; MALE; MENISCECTOMY; MOUSE; MTT ASSAY; NONHUMAN; OSTEOBLAST; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VERY ELDERLY; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; BOVINE; C57BL MOUSE; CELL CULTURE; CHONDROCYTE; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MIDDLE AGED; OSTEOARTHRITIS; RNA INTERFERENCE; SPRAGUE DAWLEY RAT;

ADAM PROTEINS; ADAMTS4 PROTEIN; AGED; AGED, 80 AND OVER; ANIMALS; BLOTTING, WESTERN; CARTILAGE, ARTICULAR; CATTLE; CELL ADHESION MOLECULES; CELLS, CULTURED; CHONDROCYTES; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MATRIX METALLOPROTEINASE 13; MICE, INBRED C57BL; MIDDLE AGED; OSTEOARTHRITIS; PROCOLLAGEN N-ENDOPEPTIDASE; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 84946944485     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-272427     Document Type: Article

References (60)

1. Loeser, R. F. (2006) Molecular mechanisms of cartilage destruction: mechanics, inflammatory mediators, and aging collide. Arthritis Rheum. 54,1357-1360
2. Abramson,S.B.,Attur,M.,andYazici,Y.(2006)Prospectsfordisease modification in osteoarthritis. Nat. Clin. Pract. Rheumatol. 2, 304-312
3. Goldring, M. B., and Goldring, S. R. (2007) Osteoarthritis. J. Cell. Physiol. 213, 626-634
4. Attur, M., Krasnokutsky-Samuels, S., Samuels, J., and Abramson, S. B. (2013) Prognostic biomarkers in osteoarthritis. Curr. Opin. Rheumatol. 25,136-144
5. Houard,X.,Goldring,M.B.,andBerenbaum,F.(2013)Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis. Curr. Rheumatol. Rep. 15,375
6. Sandell, L. J. (2007) Modern molecular analysis of a traditional disease: progression in osteoarthritis. Arthritis Rheum. 56, 2474-2477
7. Lotz, M. (2012) Osteoarthritis year 2011 in review: biology. Osteoarthritis Cartilage 20,192-196
8. Attur, M. G., Dave, M. N., Stuchin, S., Kowalski, A. J., Steiner, G., Abramson, S. B., Denhardt, D. T., and Amin, A. R. (2001) Osteopontin: an intrinsic inhibitor of inflammation in cartilage. Arthritis Rheum. 44, 578-584
9. Attur, M. G., Palmer, G. D., Al-Mussawir, H. E., Dave, M., Teixeira, C. C., Rifkin, D. B., Appleton, C. T., Beier, F., and Abramson, S. B. (2009) F-spondin, a neuroregulatory protein, is up-regulated in osteoarthritis and regulates cartilage metabolism via TGF-beta activation. FASEB J. 23,79-89
10. Maldonado, M., and Nam, J. (2013) The role of changes in extracellular matrix of cartilage in the presence of inflammation on the pathology of osteoarthritis. Biomed. Res. Int. 2013, 284873
11. Amin, A. R., Di Cesare, P. E., Vyas, P., Attur, M., Tzeng, E., Billiar, T. R., Stuchin, S. A., and Abramson, S. B. (1995) The expression and regulation of nitric oxide synthase in human osteoarthritis-affected chondrocytes: evidence for up-regulated neuronal nitric oxide synthase. J. Exp. Med. 182, 2097-2102
12. Amin, A. R., Attur, M., Patel, R. N., Thakker, G. D., Marshall, P. J., Rediske, J., Stuchin, S. A., Patel, I. R., and Abramson, S. B. (1997) Superinduction of cyclooxygenase-2 activity in human osteoarthritisaffected cartilage. Influence of nitric oxide. J. Clin. Invest. 99, 1231-1237
13. Attur, M. G., Dave, M. N., Tsunoyama, K., Akamatsu, M., Kobori, M., Miki, J., Abramson, S. B., Katoh, M., and Amin, A. R. (2002) 'A system biology' approach to bioinformatics and functional genomics in complex human diseases: arthritis. Curr. Issues Mol. Biol. 4, 129-146
14. Wen, W., Chau, E., Jackson-Boeters, L., Elliott, C., Daley, T. D., and Hamilton, D. W. (2010) TGF-β1 and FAK regulate periostin expression in PDL fibroblasts. J. Dent. Res. 89, 1439-1443
15. Bonnet, N., Conway, S. J., and Ferrari, S. L. (2012) Regulation of beta catenin signaling and parathyroid hormone anabolic effects in bone by the matricellular protein periostin. Proc. Natl. Acad. Sci. USA 109, 15048-15053
16. Loeser, R. F. (2014) Integrins and chondrocyte-matrix interactions in articular cartilage. Matrix Biol. 39, 11-16
17. Marie, P. J., Haÿ, E., and Saidak, Z. (2014) Integrin and cadherin signaling in bone: role and potential therapeutic targets. Trends Endocrinol. Metab. 25,567-575
18. Attur, M., Millman, J. S., Dave, M. N., Al-Mussawir, H. E., Patel, J., Palmer, G., and Abramson, S. B. (2011) Glatiramer acetate (GA), the immunomodulatory drug, inhibits inflammatory mediators and collagen degradation in osteoarthritis (OA) cartilage. Osteoarthritis Cartilage 19, 1158-1164
19. Minashima, T., Zhang, Y., Lee, Y., and Kirsch, T. (2014) Lithium protects against cartilage degradation in osteoarthritis. Arthritis Rheumatol. 66,1228-1236
20. Handley, C. J., and Buttle, D. J. (1995) Assay of proteoglycan degradation. Methods Enzymol. 248,47-58
21. Bendele, A. M. (2001) Animal models of osteoarthritis. J. Musculoskelet. Neuronal Interact. 1,363-376
22. Bove,S.E.,Laemont,K.D.,Brooker,R.M.,Osborn,M.N.,Sanchez, B.M.,Guzman,R.E.,Hook,K.E.,Juneau,P.L.,Connor,J.R.,and Kilgore, K. S. (2006) Surgically induced osteoarthritis in the rat results in the development of both osteoarthritis-like joint pain and secondary hyperalgesia. Osteoarthritis Cartilage 14,1041-1048
23. Kamekura, S., Kawasaki, Y., Hoshi, K., Shimoaka, T., Chikuda, H., Maruyama, Z., Komori, T., Sato, S., Takeda, S., Karsenty, G., Nakamura, K., Chung, U. I., and Kawaguchi, H. (2006) Contribution of runtrelated transcription factor 2 to the pathogenesis of osteoarthritis in mice after induction of knee joint instability. Arthritis Rheum. 54, 2462-2470
24. Nagase, H., Nagasawa, Y., Tachida, Y., Sakakibara, S., Okutsu, J., Suematsu, N., Arita, S., and Shimada, K. (2013) Deiodinase 2 upregulation demonstrated in osteoarthritis patients cartilage causes cartilage destruction in tissue-specific transgenic rats. Osteoarthritis Cartilage 21,514-523
25. Appleton, C. T., McErlain, D. D., Pitelka, V., Schwartz, N., Bernier, S. M., Henry, J. L., Holdsworth, D. W., and Beier, F. (2007) Forced mobilization accelerates pathogenesis: characterization of a preclinical surgical model of osteoarthritis. Arthritis Res. Ther. 9, R13
26. Appleton, C. T., Pitelka, V., Henry, J., and Beier, F. (2007) Global analyses of gene expression in early experimental osteoarthritis. Arthritis Rheum. 56,1854-1868
27. Campbell, K. A., Minashima, T., Zhang, Y., Hadley, S., Lee, Y. J., Giovinazzo, J., Quirno, M., and Kirsch, T. (2013) Annexin A6 interacts with p65 and stimulates NF-kB activity and catabolic events in articular chondrocytes. Arthritis Rheum. 65, 3120-3129
28. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(2Delta Delta C(T)) method. Methods 25, 402-408
29. Hakuno, D., Kimura, N., Yoshioka, M., Mukai, M., Kimura, T., Okada, Y., Yozu, R., Shukunami, C., Hiraki, Y., Kudo, A., Ogawa, S., and Fukuda, K. (2010) Periostin advances atherosclerotic and rheumatic cardiac valve degeneration by inducing angiogenesis and MMP production in humans and rodents. J. Clin. Invest. 120, 2292-2306
30. Yang, L., Serada, S., Fujimoto, M., Terao, M., Kotobuki, Y., Kitaba, S., Matsui, S., Kudo, A., Naka, T., Murota, H., and Katayama, I. (2012) Periostin facilitates skin sclerosis via PI3K/Akt dependent mechanism in a mouse model of scleroderma. PLoS ONE 7,e41994
31. Shih, C. H., Lacagnina, M., Leuer-Bisciotti, K., and Pröschel, C. (2014) Astroglial-derived periostin promotes axonal regeneration after spinal cord injury. J. Neurosci. 34, 2438-2443
32. Kikuchi, Y., Kunita, A., Iwata, C., Komura, D., Nishiyama, T., Shimazu, K., Takeshita, K., Shibahara, J., Kii, I., Morishita, Y., Yashiro,M.,Hirakawa,K.,Miyazono,K.,Kudo,A.,Fukayama,M.,and Kashima, T. G. (2014) The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation. Am.J.Pathol.184,859-870
33. Lourido, L., Calamia, V., Mateos, J., Fernández-Puente, P., Fernández-Tajes, J., Blanco, F. J., and Ruiz-Romero, C. (2014)Quantitative proteomic profiling of human articular cartilage degradation in osteoarthritis. J. Proteome Res. 13, 6096-6106
34. Olex, A. L., Turkett, W. H., Fetrow, J. S., and Loeser, R. F. (2014) Integration of gene expression data with network-based analysis to identify signaling and metabolic pathways regulated during the development of osteoarthritis. Gene 542, 38-45
35. Ewan, K., Pajak, B., Stubbs, M., Todd, H., Barbeau, O., Quevedo, C., Botfield, H., Young, R., Ruddle, R., Samuel, L., Battersby, A., Raynaud, F., Allen, N., Wilson, S., Latinkic, B., Workman, P., McDonald, E., Blagg, J., Aherne, W., and Dale, T. (2010) A useful approach to identify novel small-molecule inhibitors of Wntdependent transcription. Cancer Res. 70, 5963-5973
36. Attur,M.,Ben-Artzi,A.,Yang,Q.,Al-Mussawir,H.E.,Worman,H.J., Palmer, G., and Abramson, S. B. (2012) Perturbation of nuclear lamin A causes cell death in chondrocytes. Arthritis Rheum. 64, 1940-1949
37. Lotz, M., and Loeser, R. F. (2012) Effects of aging on articular cartilage homeostasis. Bone 51, 241-248
38. Loeser, R. F. (2013) Aging processes and the development of osteoarthritis. Curr. Opin. Rheumatol. 25, 108-113
39. Li, Y., Wei, X., Zhou, J., and Wei, L. (2013) The age-related changes in cartilage and osteoarthritis. Biomed. Res. Int. 2013, 916530
40. Van der Kraan, P. M., Blaney Davidson, E.N., and van den Berg, W. B. (2010) A role for age-related changes in TGFbeta signaling in aberrant chondrocyte differentiation and osteoarthritis. Arthritis Res. Ther. 12, 201
41. Shen, J., Li, J., Wang, B., Jin, H., Wang, M., Zhang, Y., Yang, Y., Im, H. J., O'Keefe, R., and Chen, D. (2013) Deletion of the transforming growth factor b receptor type II gene in articular chondrocytes leads to a progressive osteoarthritis-like phenotypein mice. Arthritis Rheum. 65, 3107-3119
42. Zhen, G., Wen, C., Jia, X., Li, Y., Crane, J. L., Mears, S. C., Askin, F. B., Frassica, F. J., Chang, W., Yao, J., Carrino, J. A., Cosgarea, A., Artemov, D., Chen, Q., Zhao, Z., Zhou, X., Riley, L., Sponseller, P., Wan, M., Lu, W. W., and Cao, X. (2013) Inhibition of TGF-b signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat. Med. 19, 704-712
43. Merle, B., and Garnero, P. (2012) The multiple facets of periostin in bone metabolism. Osteoporos. Int. 23, 1199-1212
44. Misra, D., Booth, S. L., Tolstykh, I., Felson, D. T., Nevitt, M. C., Lewis, C. E., Torner, J., and Neogi, T. (2013) Vitamin K deficiency is associated with incident knee osteoarthritis. Am. J. Med. 126, 243-248
45. McCann, J. C., and Ames, B. N. (2009) Vitamin K, an example of triage theory: is micronutrient inadequacy linked to diseases of aging? Am.J.Clin.Nutr.90, 889-907
46. Karlsson, C., Dehne, T., Lindahl, A., Brittberg, M., Pruss, A., Sittinger, M., and Ringe, J. (2010) Genome-wide expression profiling reveals new candidate genes associated with osteoarthritis. Osteoarthritis Cartilage 18,581-592
47. Conway, S. J., Izuhara, K., Kudo, Y., Litvin, J., Markwald, R., Ouyang, G., Arron, J. R., Holweg, C. T., and Kudo, A. (2014) The role of periostin in tissueremodeling acrosshealthanddisease. Cell. Mol. Life Sci. 71, 1279-1288
48. Bonnet, N., Gineyts, E., Ammann, P., Conway, S. J., Garnero, P., and Ferrari, S. (2013) Periostin deficiency increases bone damage and impairs injury response to fatigue loading in adult mice. PLoS ONE 8, e78347
49. Loeser, R. F., Olex, A. L., McNulty, M. A., Carlson, C. S., Callahan, M. F., Ferguson, C. M., Chou, J., Leng, X., and Fetrow, J. S. (2012) Microarray analysis reveals age-related differences in gene expression during the development of osteoarthritis in mice. Arthritis Rheum. 64,705-717
50. Zhang, R., Fang, H., Chen, Y., Shen, J., Lu, H., Zeng, C., Ren, J., Zeng, H., Li, Z., Chen, S., Cai, D., and Zhao, Q. (2012) Gene expression analyses of subchondral bone in early experimental osteoarthritis by microarray. PLoS ONE 7, e32356
51. Chou, C. H., Lee, C. H., Lu, L. S., Song, I. W., Chuang, H. P., Kuo, S. Y., Wu, J. Y., Chen, Y. T., Kraus, V. B., Wu, C. C., and Lee, M. T. (2013) Direct assessment of articular cartilage and underlying subchondral bone reveals a progressive gene expression change in human osteoarthritic knees. Osteoarthritis Cartilage 21, 450-461
52. Loeser, R. F., Olex, A. L., McNulty, M. A., Carlson, C. S., Callahan, M., Ferguson, C., and Fetrow, J. S. (2013) Disease progression and phasic changes in gene expression in a mouse model of osteoarthritis. PLoS ONE 8,e54633
53. Gardiner,M.D.,Vincent,T.L.,Driscoll,C.,Burleigh,A.,Bou-Gharios, G., Saklatvala, J., Nagase, H., and Chanalaris, A. (2015) Transcriptional analysis of micro-dissected articular cartilage in post-traumatic murine osteoarthritis. Osteoarthritis Cartilage 23, 616-628
54. Mariani, E., Pulsatelli, L., and Facchini, A. (2014) Signaling pathways in cartilage repair. Int. J. Mol. Sci. 15, 8667-8698
55. Blom, A. B., van Lent, P. L., van der Kraan, P. M., and van den Berg, W. B. (2010) To seek shelter from the WNT in osteoarthritis? WNTsignaling as a target for osteoarthritis therapy. Curr. Drug Targets 11, 620-629
56. Yuasa, T., Otani, T., Koike, T., Iwamoto, M., and Enomoto-Iwamoto, M. (2008) Wnt/beta-catenin signaling stimulates matrix catabolic genes and activity in articular chondrocytes: its possible role in joint degeneration. Lab. Invest. 88, 264-274
57. Fosang, A. J., and Beier, F. (2011) Emerging frontiers in cartilage and chondrocyte biology. Best Pract. Res. Clin. Rheumatol. 25, 751-766
58. Wang,M.,Sampson,E.R.,Jin,H.,Li,J.,Ke,Q.H.,Im,H.J.,andChen, D. (2013) MMP13 is a critical target gene during the progression of osteoarthritis. Arthritis Res. Ther. 15, R5
59. Orecchia,P.,Conte,R.,Balza,E.,Castellani,P.,Borsi,L.,Zardi,L., Mingari, M. C., and Carnemolla, B. (2011) Identification of a novel cell binding site of periostin involved in tumour growth. Eur. J. Cancer 47,2221-2229
60. Watanabe, T., Yasue, A., Fujihara, S., and Tanaka, E. (2012) Periostin regulates MMP-2 expression via the avb3 integrin/ERK pathway in human periodontal ligament cells. Arch. Oral Biol. 57, 52-59