Regulation of Chondrocyte Survival in Mouse Articular Cartilage by p63

Arthritis and Rheumatology

Volumn 69, Issue 3, 2017, Pages 598-609

  Taniguchi, Yuki ^a   Kawata, Manabu ^a   Ho Chang, Song ^a   Mori, Daisuke ^a   Okada, Keita ^a   Kobayashi, Hiroshi ^a   Sugita, Shurei ^a   Hosaka, Yoko ^a   Inui, Hiroshi ^a   Taketomi, Shuji ^a   Yano, Fumiko ^a   Ikeda, Toshiyuki ^a   Akiyama, Haruhiko ^b   Mills, Alea A ^c   Chung, Ung Il ^a   Tanaka, Sakae ^a   Kawaguchi, Hiroshi ^d   Saito, Taku ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c Simons Center for Quantitative Biology   (United States)

^d TOKYO KOSEI NENKIN HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN P53; PROTEIN P63; PHOSPHOPROTEIN; TRANSACTIVATOR PROTEIN; TRP63 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ARTICULAR CARTILAGE; BAX GENE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHONDROCYTE; CONTROLLED STUDY; EMBRYO; EPIPHYSIS PLATE; FAS GENE; GENE; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIMB BUD MESENCHYMAL CELL; MALE; MOUSE; NONHUMAN; NOXA GENE; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUMA GENE; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; TISSUE SPECIFICITY; ANIMAL; CYTOLOGY; KNOCKOUT MOUSE; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CARTILAGE, ARTICULAR; CELL SURVIVAL; CHONDROCYTES; GROWTH PLATE; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHOPROTEINS; TRANS-ACTIVATORS;

EID: 85014125018     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39976     Document Type: Article

References (56)

1. Kronenberg HM. Developmental regulation of the growth plate. Nature 2003;423:332–6.
2. Hirai T, Chagin AS, Kobayashi T, Mackem S, Kronenberg HM. Parathyroid hormone/parathyroid hormone-related protein receptor signaling is required for maintenance of the growth plate in postnatal life. Proc Natl Acad Sci U S A 2011;108:191–6.
3. Van der Kraan PM, van den Berg WB. Chondrocyte hypertrophy and osteoarthritis: role in initiation and progression of cartilage degeneration? Osteoarthritis Cartilage 2012;20:223–32.
4. Blanco FJ, Guitian R, Vazquez-Martul E, de Toro FJ, Galdo F. Osteoarthritis chondrocytes die by apoptosis: a possible pathway for osteoarthritis pathology. Arthritis Rheum 1998;41:284–9.
5. Hashimoto S, Ochs RL, Komiya S, Lotz M. Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis. Arthritis Rheum 1998;41:1632–8.
6. Kim HA, Lee YJ, Seong SC, Choe KW, Song YW. Apoptotic chondrocyte death in human osteoarthritis. J Rheumatol 2000;27:455–62.
7. Matsuo M, Nishida K, Yoshida A, Murakami T, Inoue H. Expression of caspase-3 and -9 relevant to cartilage destruction and chondrocyte apoptosis in human osteoarthritic cartilage. Acta Med Okayama 2001;55:333–40.
8. Mistry D, Oue Y, Chambers MG, Kayser MV, Mason RM. Chondrocyte death during murine osteoarthritis. Osteoarthritis Cartilage 2004;12:131–41.
9. Thomas CM, Fuller CJ, Whittles CE, Sharif M. Chondrocyte death by apoptosis is associated with cartilage matrix degradation. Osteoarthritis Cartilage 2007;15:27–34.
10. Zamli Z, Sharif M. Chondrocyte apoptosis: a cause or consequence of osteoarthritis? Int J Rheum Dis 2011;14:159–66.
11. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999;398:708–13.
12. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, et al. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999;398:714–8.
13. Bergholz J, Xiao ZX. Role of p63 in development, tumorigenesis and cancer progression. Cancer Microenviron 2012;5:311–22.
14. Candi E, Dinsdale D, Rufini A, Salomoni P, Knight RA, Mueller M, et al. TAp63 and DeltaNp63 in cancer and epidermal development. Cell Cycle 2007;6:274–85.
15. Vanbokhoven H, Melino G, Candi E, Declercq W. p63, a story of mice and men. J Invest Dermatol 2011;131:1196–207.
16. Ihrie RA, Attardi LD. A new perp in the lineup: linking p63 and desmosomal adhesion. Cell Cycle 2005;4:873–6.
17. Ihrie RA, Marques MR, Nguyen BT, Horner JS, Papazoglu C, Bronson RT, et al. Perp is a p63-regulated gene essential for epithelial integrity. Cell 2005;120:843–56.
18. Koster MI, Dai D, Marinari B, Sano Y, Costanzo A, Karin M, et al. p63 induces key target genes required for epidermal morphogenesis. Proc Natl Acad Sci U S A 2007;104:3255–60.
19. Su X, Cho MS, Gi YJ, Ayanga BA, Sherr CJ, Flores ER. Rescue of key features of the p63-null epithelial phenotype by inactivation of Ink4a and Arf. EMBO J 2009;28:1904–15.
20. Vigano MA, Lamartine J, Testoni B, Merico D, Alotto D, Castagnoli C, et al. New p63 targets in keratinocytes identified by a genome-wide approach. EMBO J 2006;25:5105–16.
21. Yang A, Zhu Z, Kapranov P, McKeon F, Church GM, Gingeras TR, et al. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006;24:593–602.
22. Gu J, Lu Y, Qiao L, Ran D, Li N, Cao H, et al. Mouse p63 variants and chondrogenesis. Int J Clin Exp Pathol 2013;6:2872–9.
23. Li F, Lu Y, Ding M, Wu G, Sinha S, Wang S, et al. Putative function of TAP63α during endochondral bone formation. Gene 2012;495:95–103.
24. Lu Y, Abbassi S, Li F, Ding M, Wu G, Gu J, et al. Distinct function of P63 isoforms during embryonic skeletal development. Gene 2013;519:251–9.
25. arcOGEN Consortium and arcOGEN Collaborators. Identification of new susceptibility loci for osteoarthritis (arcOGEN): a genome-wide association study. Lancet 2012;380:815–23.
26. Gosset M, Berenbaum F, Thirion S, Jacques C. Primary culture and phenotyping of murine chondrocytes. Nat Protoc 2008;3:1253–60.
27. Kamekura S, Hoshi K, Shimoaka T, Chung U, Chikuda H, Yamada T, et al. Osteoarthritis development in novel experimental mouse models induced by knee joint instability. Osteoarthritis Cartilage 2005;13:632–41.
28. Pritzker KP, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, et al. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 2006;14:13–29.
29. Hosaka Y, Saito T, Sugita S, Hikata T, Kobayashi H, Fukai A, et al. Notch signaling in chondrocytes modulates endochondral ossification and osteoarthritis development. Proc Natl Acad Sci U S A 2013;110:1875–80.
30. Saito T, Fukai A, Mabuchi A, Ikeda T, Yano F, Ohba S, et al. Transcriptional regulation of endochondral ossification by HIF-2α during skeletal growth and osteoarthritis development. Nat Med 2010;16:678–86.
31. Saito T, Ikeda T, Nakamura K, Chung UI, Kawaguchi H. S100A1 and S100B, transcriptional targets of SOX trio, inhibit terminal differentiation of chondrocytes. EMBO Rep 2007;8:504–9.
32. Ovchinnikov DA, Deng JM, Ogunrinu G, Behringer RR. Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 2000;26:145–6.
33. Mills AA, Qi Y, Bradley A. Conditional inactivation of p63 by Cre-mediated excision. Genesis 2002;32:138–41.
34. Akiyama H, Kim JE, Nakashima K, Balmes G, Iwai N, Deng JM, et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci U S A 2005;102:14665–70.
35. Logan M, Martin JF, Nagy A, Lobe C, Olson EN, Tabin CJ. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 2002;33:77–80.
36. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995;80:293–9.
37. Muller M, Wilder S, Bannasch D, Israeli D, Lehlbach K, Li-Weber M, et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J Exp Med 1998;188:2033–45.
38. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001;7:683–94.
39. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000;288:1053–8.
40. Glasson SS, Askew R, Sheppard B, Carito B, Blanchet T, Ma HL, et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 2005;434:644–8.
41. Kamekura S, Kawasaki Y, Hoshi K, Shimoaka T, Chikuda H, Maruyama Z, et al. Contribution of runt-related transcription factor 2 to the pathogenesis of osteoarthritis in mice after induction of knee joint instability. Arthritis Rheum 2006;54:2462–70.
42. Little CB, Barai A, Burkhardt D, Smith SM, Fosang AJ, Werb Z, et al. Matrix metalloproteinase 13–deficient mice are resistant to osteoarthritic cartilage erosion but not chondrocyte hypertrophy or osteophyte development. Arthritis Rheum 2009;60:3723–33.
43. Stanton H, Rogerson FM, East CJ, Golub SB, Lawlor KE, Meeker CT, et al. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 2005;434:648–52.
44. Sugita S, Hosaka Y, Okada K, Mori D, Yano F, Kobayashi H, et al. Transcription factor Hes1 modulates osteoarthritis development in cooperation with calcium/calmodulin-dependent protein kinase 2. Proc Natl Acad Sci U S A 2015;112:3080–5.
45. Yang S, Kim J, Ryu JH, Oh H, Chun CH, Kim BJ, et al. Hypoxia-inducible factor-2α is a catabolic regulator of osteoarthritic cartilage destruction. Nat Med 2010;16:687–93.
46. Moll UM, Slade N. p63 and p73: roles in development and tumor formation. Mol Cancer Res 2004;2:371–86.
47. Ohyama K, Chung CH, Chen E, Gibson CW, Misof K, Fratzl P, et al. p53 influences mice skeletal development. J Craniofac Genet Dev Biol 1997;17:161–71.
48. Ryu JH, Shin Y, Huh YH, Yang S, Chun CH, Chun JS. Hypoxia-inducible factor-2α regulates Fas-mediated chondrocyte apoptosis during osteoarthritic cartilage destruction. Cell Death Differ 2012;19:440–50.
49. Sezgin M, Barlas İÖ, Yıldır S, Türköz G, Ankaralı HÇ, Şahin G, et al. Apoptosis-related Fas and FasL gene polymorphisms’ associations with knee osteoarthritis. Rheumatol Int 2013;33:2039–43.
50. Li Z, Shen J, Chen Y, Pan J, Zeng H, Fang H, et al. Mitochondrial genome sequencing of chondrocytes in osteoarthritis by human mitochondria RT2 Profiler PCR array. Mol Med Rep 2012;6:39–44.
51. Karaliotas GI, Mavridis K, Scorilas A, Babis GC. Quantitative analysis of the mRNA expression levels of BCL2 and BAX genes in human osteoarthritis and normal articular cartilage: an investigation into their differential expression. Mol Med Rep 2015;12:4514–21.
52. Tonino SH, van Laar J, van Oers MH, Wang JY, Eldering E, Kater AP. ROS-mediated upregulation of Noxa overcomes chemoresistance in chronic lymphocytic leukemia. Oncogene 2011;30:701–13.
53. Keyes WM, Wu Y, Vogel H, Guo X, Lowe SW, Mills AA. p63 deficiency activates a program of cellular senescence and leads to accelerated aging. Genes Dev 2005;19:1986–99.
54. Fuchs E. Scratching the surface of skin development. Nature 2007;445:834–42.
55. Eckhart L, Lippens S, Tschachler E, Declercq W. Cell death by cornification. Biochim Biophys Acta 2013;1833:3471–80.
56. Kozhemyakina E, Zhang M, Ionescu A, Ayturk UM, Ono N, Kobayashi A, et al. Identification of a prg4-expressing articular cartilage progenitor cell population in mice. Arthritis Rheumatol 2015;67:1261–73.