Activating enhancer binding protein 2 epsilon (AP-2ε)-deficient mice exhibit increased matrix metalloproteinase 13 expression and progressive osteoarthritis development

Arthritis Research and Therapy

Volumn 17, Issue 1, 2015, Pages

  Niebler, Stephan ^a,b   Schubert, Thomas ^a   Hunziker, Ernst B ^c   Bosserhoff, Anja K ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING ENHANCER BINDING PROTEIN 2 EPSILON; BINDING PROTEIN; COLLAGENASE 3; UNCLASSIFIED DRUG; MMP13 PROTEIN, MOUSE; TRANSCRIPTION FACTOR AP 2;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BIOLOGICAL MONITORING; BONE DEVELOPMENT; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE COURSE; EMBRYO; EMBRYO DEVELOPMENT; EXPLANT; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; GENOTYPE; HISTOPATHOLOGY; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; KNEE MENISCUS; KNEE OSTEOARTHRITIS; MALE; MESENCHYME CELL; MOLECULAR BIOLOGY; MOUSE; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; BIOSYNTHESIS; DEFICIENCY; DISEASE MODEL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; OSTEOARTHRITIS; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CARTILAGE, ARTICULAR; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MATRIX METALLOPROTEINASE 13; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; OSTEOARTHRITIS; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR AP-2;

EID: 84930626492     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-015-0648-8     Document Type: Article

References (56)

1. Michigami T. Regulatory mechanisms for the development of growth plate cartilage. Cell Mol Life Sci. 2013;70:4213-21.
2. Hartmann C. Transcriptional networks controlling skeletal development. Curr Opin Genet Dev. 2009;19:437-43.
3. Goldring MB, Tsuchimochi K, Ijiri K. The control of chondrogenesis. J Cell Biochem. 2006;97:33-44.
4. Goldring MB. Chondrogenesis, chondrocyte differentiation, and articular cartilage metabolism in health and osteoarthritis. Ther Adv Musculoskelet Dis. 2012;4:269-85.
5. Karsenty G, Wagner EF. Reaching a genetic and molecular understanding of skeletal development. Dev Cell. 2002;2:389-406.
6. Bhosale AM, Richardson JB. Articular cartilage: structure, injuries and review of management. Br Med Bull. 2008;87:77-95.
7. Goldring MB, Goldring SR. Osteoarthritis. J Cell Physiol. 2007;213:626-34.
8. Appleton CT, Pitelka V, Henry J, Beier F. Global analyses of gene expression in early experimental osteoarthritis. Arthritis Rheum. 2007;56:1854-68.
9. Pulsatelli L, Addimanda O, Brusi V, Pavloska B, Meliconi R. New findings in osteoarthritis pathogenesis: therapeutic implications. Ther Adv Chronic Dis. 2013;4:23-43.
10. Lawrence RC, Felson DT, Helmick CG, Arnold LM, Choi H, Deyo RA, et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States: part II. Arthritis Rheum. 2008;58:26-35.
11. Murphy L, Schwartz TA, Helmick CG, Renner JB, Tudor G, Koch G, et al. Lifetime risk of symptomatic knee osteoarthritis. Arthritis Rheum. 2008;59:1207-13.
12. Felson DT. Osteoarthritis of the knee. N Engl J Med. 2006;354:841-8. A published erratum appears in. N Engl J Med. 2006;354:2520.
13. Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest. 1997;99:1534-45.
14. Shlopov BV, Lie WR, Mainardi CL, Cole AA, Chubinskaya S, Hasty KA. Osteoarthritic lesions: involvement of three different collagenases. Arthritis Rheum. 1997;40:2065-74.
15. Cawston TE, Wilson AJ. Understanding the role of tissue degrading enzymes and their inhibitors in development and disease. Best Pract Res Clin Rheumatol. 2006;20:983-1002.
16. Forsyth CB, Cole A, Murphy G, Bienias JL, Im HJ, Loeser Jr RF. Increased matrix metalloproteinase-13 production with aging by human articular chondrocytes in response to catabolic stimuli. J Gerontol A Biol Sci Med Sci. 2005;60:1118-24.
17. Reboul P, Pelletier JP, Tardif G, Cloutier JM, Martel-Pelletier J. The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes: a role in osteoarthritis. J Clin Invest. 1996;97:2011-9.
18. 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.
19. 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.
20. Wenke AK, Rothhammer T, Moser M, Bosserhoff AK. Regulation of integrin α10 expression in chondrocytes by the transcription factors AP-2ε and Ets-1. Biochem Biophys Res Commun. 2006;345:495-501.
21. Wenke AK, Grässel S, Moser M, Bosserhoff AK. The cartilage-specific transcription factor Sox9 regulates AP-2ε expression in chondrocytes. FEBS J. 2009;276:2494-504.
22. Tummala R, Romano RA, Fuchs E, Sinha S. Molecular cloning and characterization of AP-2ε, a fifth member of the AP-2 family. Gene. 2003;321:93-102.
23. Feng W, Williams T. Cloning and characterization of the mouse AP-2ε gene: a novel family member expressed in the developing olfactory bulb. Mol Cell Neurosci. 2003;24:460-75.
24. Hilger-Eversheim K, Moser M, Schorle H, Buettner R. Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene. 2000;260:1-12.
25. Wenke AK, Niebler S, Grässel S, Bosserhoff AK. The transcription factor AP-2ε regulates CXCL1 during cartilage development and in osteoarthritis. Osteoarthritis Cartilage. 2011;19:206-12.
26. Niebler S, Bosserhoff AK. The transcription factor activating enhancer-binding protein epsilon (AP-2ε) regulates the core promoter of type II collagen (COL2A1). FEBS J. 2013;280:1397-408.
27. Schmid R, Schiffner S, Opolka A, Grässel S, Schubert T, Moser M, et al. Enhanced cartilage regeneration in MIA/CD-RAP deficient mice. Cell Death Dis. 2010;1, e97.
28. nrb is a new regulator of progression of malignant melanoma. Carcinogenesis. 2011;32:1176-82.
29. Schmidl M, Adam N, Surmann-Schmitt C, Hattori T, Stock M, Dietz U, et al. Twisted gastrulation modulates bone morphogenetic protein-induced collagen II and X expression in chondrocytes in vitro and in vivo. J Biol Chem. 2006;281:31790-800.
30. Tatzel J, Poser I, Schroeder J, Bosserhoff AK. Inhibition of melanoma inhibitory activity (MIA) expression in melanoma cells leads to molecular and phenotypic changes. Pigment Cell Res. 2005;18:92-101.
31. Moser M, Bosserhoff AK, Hunziker EB, Sandell L, Fässler R, Buettner R. Ultrastructural cartilage abnormalities in MIA/CD-RAP-deficient mice. Mol Cell Biol. 2002;22:1438-45.
32. 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.
33. Wang M, Sampson ER, Jin H, Li J, Ke QH, Im HJ, et al. MMP13 is a critical target gene during the progression of osteoarthritis. Arthritis Res Ther. 2013;15:R5.
34. 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.
35. Stickens D, Behonick DJ, Ortega N, Heyer B, Hartenstein B, Yu Y, et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development. 2004;131:5883-95.
36. Schmid R, Bosserhoff AK. Redundancy in regulation of chondrogenesis in MIA/CD-RAP-deficient mice. Mech Dev. 2014;131:24-34.
37. Castagnola P, Moro G, Descalzi-Cancedda F, Cancedda R. Type X collagen synthesis during in vitro development of chick embryo tibial chondrocytes. J Cell Biol. 1986;102:2310-7.
38. Linsenmayer TF, Eavey RD, Schmid TM. Type X collagen: a hypertrophic cartilage-specific molecule. Pathol Immunopathol Res. 1988;7:14-9.
39. Reichenberger E, Aigner T, von der Mark K, Stoss H, Bertling W. In situ hybridization studies on the expression of type X collagen in fetal human cartilage. Dev Biol. 1991;148:562-72.
40. D'Angelo M, Yan Z, Nooreyazdan M, Pacifici M, Sarment DS, Billings PC, et al. MMP-13 is induced during chondrocyte hypertrophy. J Cell Biochem. 2000;77:678-93.
41. Huang Z, Xu H, Sandell L. Negative regulation of chondrocyte differentiation by transcription factor AP-2α. J Bone Miner Res. 2004;19:245-55.
42. Rock JR, Lopez MC, Baker HV, Harfe BD. Identification of genes expressed in the mouse limb using a novel ZPA microarray approach. Gene Expr Patterns. 2007;8:19-26.
43. Gannon JM, Walker G, Fischer M, Carpenter R, Thompson Jr RC, Oegema Jr TR. Localization of type X collagen in canine growth plate and adult canine articular cartilage. J Orthop Res. 1991;9:485-94.
44. Mitchell PG, Magna HA, Reeves LM, Lopresti-Morrow LL, Yocum SA, Rosner PJ, et al. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J Clin Invest. 1996;97:761-8.
45. Krane SM, Inada M. Matrix metalloproteinases and bone. Bone. 2008;43:7-18.
46. Mercuri FA, Maciewicz RA, Tart J, Last K, Fosang AJ. Mutations in the interglobular domain of aggrecan alter matrix metalloproteinase and aggrecanase cleavage patterns: evidence that matrix metalloproteinase cleavage interferes with aggrecanase activity. J Biol Chem. 2000;275:33038-45.
47. Fosang AJ, Last K, Knäuper V, Murphy G, Neame PJ. Degradation of cartilage aggrecan by collagenase-3 (MMP-13). FEBS Lett. 1996;380:17-20.
48. Singer II, Kawka DW, Bayne EK, Donatelli SA, Weidner JR, Williams HR, et al. VDIPEN, a metalloproteinase-generated neoepitope, is induced and immunolocalized in articular cartilage during inflammatory arthritis. J Clin Invest. 1995;95:2178-86.
49. Knäuper V, Cowell S, Smith B, López-Otin C, O'Shea M, Morris H, et al. The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem. 1997;272:7608-16.
50. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69:562-73.
51. Neuhold LA, Killar L, Zhao W, Sung ML, Warner L, Kulik J, et al. Postnatal expression in hyaline cartilage of constitutively active human collagenase-3 (MMP-13) induces osteoarthritis in mice. J Clin Invest. 2001;107:35-44.
52. 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.
53. Tardif G, Pelletier JP, Dupuis M, Hambor JE, Martel-Pelletier J. Cloning, sequencing and characterization of the 5'-flanking region of the human collagenase-3 gene. Biochem J. 1997;323:13-6.
54. Jiménez MJ, Balbín M, López JM, Alvarez J, Komori T, López-Otín C. Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation. Mol Cell Biol. 1999;19:4431-42.
55. Otero M, Plumb DA, Tsuchimochi K, Dragomir CL, Hashimoto K, Peng H, et al. E74-like factor 3 (ELF3) impacts on matrix metalloproteinase 13 (MMP13) transcriptional control in articular chondrocytes under proinflammatory stress. J Biol Chem. 2012;287:3559-72.
56. Hess J, Porte D, Munz C, Angel P. AP-1 and Cbfa/runt physically interact and regulate parathyroid hormone-dependent MMP13 expression in osteoblasts through a new osteoblast-specific element 2/AP-1 composite element. J Biol Chem. 2001;276:20029-38.