Disturbed cartilage and joint homeostasis resulting from a loss of mitogen-inducible gene 6 in a mouse model of joint dysfunction

Arthritis and Rheumatology

Volumn 66, Issue 10, 2014, Pages 2816-2827

  Pest, Michael A ^a   Russell, Bailey A ^a   Zhang, Yu Wen ^b   Jeong, Jae Wook ^c   Beier, Frank ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN INDUCIBLE GENE 6; MITOGENIC AGENT; PROTEOGLYCAN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; ERRFI1 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BONE EROSION; CARTILAGE CELL; CELL DENSITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; JOINT; JOINT DEGENERATION; KNEE; MALE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOARTHRITIS; PROTEIN EXPRESSION; ANIMAL; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROCYTES; DISEASE MODELS, ANIMAL; HOMEOSTASIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JOINTS; MICE; MICE, KNOCKOUT; OSTEOARTHRITIS;

EID: 84908377358     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38758     Document Type: Article

References (50)

1. Losina E, Weinstein AM, Reichmann WM, Burbine SA, Solomon DH, Daigle ME, et al. Lifetime risk and age at diagnosis of symptomatic knee osteoarthritis in the US. Arthritis Care Res (Hoboken) 2013; 65: 703-11.
2. Aigner T, Sachse A, Gebhard PM, Roach HI,. Osteoarthritis: pathobiology-targets and ways for therapeutic intervention. Adv Drug Deliv Rev 2006; 58: 128-49.
3. Goldring SR, Goldring MB,. Bone and cartilage in osteoarthritis: is what's best for one good or bad for the other? Arthritis Res Ther 2010; 12: 143.
4. Cooke D, Scudamore A, Li J, Wyss U, Bryant T, Costigan P,. Axial lower-limb alignment: comparison of knee geometry in normal volunteers and osteoarthritis patients. Osteoarthritis Cartilage 1997; 5: 39-47.
5. Glasson SS, Blanchet TJ, Morris EA,. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage 2007; 15: 1061-9.
6. Appleton CT, McErlain DD, Pitelka V, Schwartz N, Bernier SM, Henry JL, et al. Forced mobilization accelerates pathogenesis: characterization of a preclinical surgical model of osteoarthritis [published erratum appears in Arthritis Res Ther 2008;10:407]. Arthritis Res Ther 2007; 9: R13.
7. Welch ID, Cowan MF, Beier F, Underhill TM,. The retinoic acid binding protein CRABP2 is increased in murine models of degenerative joint disease. Arthritis Res Ther 2009; 11: R14.
8. Joiner DM, Less KD, Van Wieren EM, Zhang YW, Hess D, Williams BO,. Accelerated and increased joint damage in young mice with global inactivation of mitogen-inducible gene 6 (MIG-6) after ligament and meniscus injury. Arthritis Res Ther 2014; 16: R81.
9. Schneider MR, Sibilia M, Erben RG,. The EGFR network in bone biology and pathology. Trends Endocrinol Metab 2009; 20: 517-24.
10. Humtsoe JO, Kramer RH,. Differential epidermal growth factor receptor signaling regulates anchorage-independent growth by modulation of the PI3K/AKT pathway. Oncogene 2010; 29: 1214-26.
11. Schneider MR, Wolf E,. The epidermal growth factor receptor ligands at a glance. J Cell Physiol 2009; 218: 460-6.
12. Usmani SE, Pest MA, Kim G, Ohora SN, Qin L, Beier F,. Transforming growth factor α controls the transition from hypertrophic cartilage to bone during endochondral bone growth. Bone 2012; 51: 131-41.
13. Zhang X, Siclari VA, Lan S, Zhu J, Koyama E, Dupuis HL, et al. The critical role of the epidermal growth factor receptor in endochondral ossification. J Bone Miner Res 2011; 26: 2622-33.
14. Saito K, Horiuchi K, Kimura T, Mizuno S, Yoda M, Morioka H, et al. Conditional inactivation of -converting enzyme in chondrocytes results in an elongated growth plate and shorter long bones. PLoS One 2013; 8: e54853.
15. Appleton CT, Usmani SE, Mort JS, Beier F,. Rho/ROCK and MEK/ERK activation by transforming growth factor-α induces articular cartilage degradation. Lab Invest 2010; 90: 20-30.
16. Long DL, Willey JS, Loeser RF,. Rac1 is required for matrix metalloproteinase 13 production by chondrocytes in response to fibronectin fragments. Arthritis Rheum 2013; 65: 1561-8.
17. Appleton CT, McErlain DD, Henry JL, Holdsworth DW, Beier F,. Molecular and histological analysis of a new rat model of experimental knee osteoarthritis. Ann N Y Acad Sci 2007; 1117: 165-74.
18. Appleton CT, Usmani SE, Bernier SM, Aigner T, Beier F,. Transforming growth factor α suppression of articular chondrocyte phenotype and Sox9 expression in a rat model of osteoarthritis. Arthritis Rheum 2007; 56: 3693-705.
19. Hallbeck AL, Walz TM, Briheim K, Wasteson A, Wasteson A,. TGF-α and ErbB2 production in synovial joint tissue: increased expression in arthritic joints. Scand J Rheumatol 2005; 34: 204-11.
20. Yi T, Lee HL, Cha JH, Ko SI, Kim HJ, Shin HI, et al. Epidermal growth factor receptor regulates osteoclast differentiation and survival through cross-talking with RANK signaling. J Cell Physiol 2008; 217: 409-22.
21. Avraham R, Yarden Y,. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol 2011; 12: 104-17.
22. Frosi Y, Anastasi S, Ballaro C, Varsano G, Castellani L, Maspero E, et al. A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation. J Cell Biol 2010; 189: 557-71.
23. Descot A, Hoffmann R, Shaposhnikov D, Reschke M, Ullrich A, Posern G,. Negative regulation of the EGFR-MAPK cascade by actin-MAL-mediated Mig6/Errfi-1 induction. Mol Cell 2009; 35: 291-304.
24. Makkinje A, Quinn DA, Chen A, Cadilla CL, Force T, Bonventre JV, et al. Gene 33/Mig-6, a transcriptionally inducible adapter protein that binds GTP-Cdc42 and activates SAPK/JNK: a potential marker transcript for chronic pathologic conditions, such as diabetic nephropathy. Possible role in the response to persistent stress. J Biol Chem 2000; 275: 17838-47.
25. Zhang YW, Su Y, Lanning N, Swiatek PJ, Bronson RT, Sigler R, et al. Targeted disruption of Mig-6 in the mouse genome leads to early onset degenerative joint disease. Proc Natl Acad Sci U S A 2005; 102: 11740-5.
26. Jin N, Gilbert JL, Broaddus RR, Demayo FJ, Jeong J,. Generation of a Mig-6 conditional null allele. Genesis 2007; 45: 716-21.
27. Ferby I, Reschke M, Kudlacek O, Knyazev P, Pante G, Amann K, et al. Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumor formation. Nat Med 2006; 12: 568-73.
28. Shepard JB, Jeong JW, Maihle NJ, O'Brien S, Dealy CN,. Transient anabolic effects accompany epidermal growth factor receptor signal activation in articular cartilage in vivo. Arthritis Res Ther 2013; 15: R60.
29. Terpstra L, Prud'homme J, Arabian A, Takeda S, Karsenty G, Dedhar S, et al. Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J Cell Biol 2003; 162: 139-48.
30. Solomon LA, Li JR, Berube NG, Beier F,. Loss of ATRX in chondrocytes has minimal effects on skeletal development. PLoS One 2009; 4: e7106.
31. Gillespie JR, Bush JR, Bell GI, Aubrey L, Dupuis H, Ferron M, et al. GSK-3β function in bone regulates skeletal development, whole-body metabolism, and male life span. Endocrinology 2013; 154: 3702-18.
32. Wang G, Woods A, Agoston H, Ulici V, Glogauer M, Beier F,. Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 2007; 306: 612-23.
33. Schmitz N, Laverty S, Kraus VB, Aigner T,. Basic methods in histopathology of joint tissues. Osteoarthritis Cartilage 2010; 18 Suppl 3: S113-6.
34. McErlain DD, Ulici V, Darling M, Gati JS, Pitelka V, Beier F, et al. An in vivo investigation of the initiation and progression of subchondral cysts in a rodent model of secondary osteoarthritis. Arthritis Res Ther 2012; 14: R26.
35. Ulici V, Hoenselaar KD, Agoston H, McErlain DD, Umoh J, Chakrabarti S, et al. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification. Bone 2009; 45: 1133-45.
36. Lin CI, Du J, Shen WT, Whang EE, Donner DB, Griff N, et al. Mitogen-inducible gene-6 is a multifunctional adaptor protein with tumor suppressor-like activity in papillary thyroid cancer. J Clin Endocrinol Metab 2011; 96: E554-65.
37. Zhang YW, Staal B, Su Y, Swiatek P, Zhao P, Cao B, et al. Evidence that MIG-6 is a tumor-suppressor gene. Oncogene 2007; 26: 269-76.
38. Zhang YW, Vande Woude GF,. Mig-6, signal transduction, stress response and cancer. Cell Cycle 2007; 6: 507-13.
39. Kim TH, Lee DK, Cho SN, Orvis GD, Behringer RR, Lydon JP, et al. Critical tumor suppressor function mediated by epithelial Mig-6 in endometrial cancer. Cancer Res 2013; 73: 5090-9.
40. Li Z, Dong Q, Wang Y, Qu L, Qiu X, Wang E,. Downregulation of Mig-6 in nonsmall-cell lung cancer is associated with EGFR signaling. Mol Carcinog 2012; 51: 522-34.
41. Ying H, Zheng H, Scott K, Wiedemeyer R, Yan H, Lim C, et al. Mig-6 controls EGFR trafficking and suppresses gliomagenesis. Proc Natl Acad Sci U S A 2010; 107: 6912-7.
42. Ling S, Chang X, Schultz L, Lee TK, Chaux A, Marchionni L, et al. An EGFR-ERK-SOX9 signaling cascade links urothelial development and regeneration to cancer. Cancer Res 2011; 71: 3812-21.
43. Aigner T, Stove J,. Collagens-major component of the physiological cartilage matrix, major target of cartilage degeneration, major tool in cartilage repair. Adv Drug Deliv Rev 2003; 55: 1569-93.
44. Radin EL, Rose RM,. Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 1986; 213: 34-40.
45. Mateescu RG, Todhunter RJ, Lust G, Burton-Wurster N,. Increased MIG-6 mRNA transcripts in osteoarthritic cartilage. Biochem Biophys Res Commun 2005; 332: 482-6.
46. Burton-Wurster N, Mateescu RG, Todhunter RJ, Clements KM, Sun Q, Scarpino V, et al. Genes in canine articular cartilage that respond to mechanical injury: gene expression studies with Affymetrix canine GeneChip. J Hered 2005; 96: 821-8.
47. LacZ reporter mice. Osteoarthritis Cartilage 2013; 21: 401-4.
48. Kambic HE, McDevitt CA,. Spatial organization of types I and II collagen in the canine meniscus. J Orthop Res 2005; 23: 142-9.
49. Zhang X, Zhu J, Li Y, Lin T, Siclari VA, Chandra A, et al. Epidermal growth factor receptor (EGFR) signaling regulates epiphyseal cartilage development through β-catenin-dependent and -independent pathways. J Biol Chem 2013; 288: 32229-40.
50. Staal B, Williams BO, Beier F, Vande Woude GF, Zhang YW,. Cartilage-specific deletion of Mig-6 results in osteoarthritis-like disorder with excessive articular chondrocyte proliferation. Proc Natl Acad Sci 2014; 111: 2590-5.