Accelerated and increased joint damage in young mice with global inactivation of mitogen-inducible gene 6 after ligament and meniscus injury

Arthritis Research and Therapy

Volumn 16, Issue 2, 2014, Pages

  Joiner, Danese M ^a,c   Less, Kennen D ^a   Van Wieren, Emily M ^a   Zhang, Yu Wen ^a   Hess, Daniel ^b   Williams, Bart O ^a  

^a VAN ANDEL RESEARCH INSTITUTE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; OSTEOCLAST DIFFERENTIATION FACTOR; ERRFI1 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTHROPATHY; ARTICLE; BONE DENSITY; BONE EROSION; CARTILAGE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; GENE; GENE MUTATION; INFLAMMATORY CELL; KNEE; KNEE LIGAMENT; KNEE MENISCUS RUPTURE; KNEE SURGERY; LIGAMENT INJURY; MENISCECTOMY; MITOGEN INDUCIBLE GENE 6; MOUSE; NONHUMAN; STAINING; THICKNESS; TIBIA; TRABECULAR BONE; WILD TYPE; ANIMAL; ARTHRITIS, EXPERIMENTAL; COMPLICATION; ENZYME LINKED IMMUNOSORBENT ASSAY; INJURIES; KNEE INJURY; KNEE MENISCUS; KNOCKOUT MOUSE; LIGAMENT; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; OSTEOARTHRITIS; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ARTHRITIS, EXPERIMENTAL; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KNEE INJURIES; KNEE JOINT; LIGAMENTS; MENISCI, TIBIAL; MICE; MICE, KNOCKOUT; OSTEOARTHRITIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; X-RAY MICROTOMOGRAPHY;

EID: 84899151656     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4522     Document Type: Article

References (52)

1. Loeser RF, Goldring SR, Scanzello CR, Goldring MB. Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum 2012, 64:1697-1707. 10.1002/art.34453, 3366018, 22392533.
2. Lorenz H, Richter W. Osteoarthritis: cellular and molecular changes in degenerating cartilage. Prog Histochem Cytochem 2006, 40:135-163. 10.1016/j.proghi.2006.02.003, 16759941.
3. Goldring MB, Marcu KB. Cartilage homeostasis in health and rheumatic diseases. Arthritis Res Ther 2009, 11:224. 10.1186/ar2592, 2714092, 19519926.
4. Borrelli J, Silva MJ, Zaegel MA, Franz C, Sandell LJ. Single high-energy impact load causes posttraumatic OA in young rabbits via a decrease in cellular metabolism. J Orthop Res 2009, 27:347-352. 10.1002/jor.20760, 18924142.
5. Hashimoto S, Rai MF, Janiszak KL, Cheverud JM, Sandell LJ. Cartilage and bone changes during development of post-traumatic osteoarthritis in selected LGXSM recombinant inbred mice. Osteoarthritis Cartilage 2012, 20:562-571. 10.1016/j.joca.2012.01.022, 3353722, 22361237.
6. Sandell LJ. Etiology of osteoarthritis: genetics and synovial joint development. Nat Rev Rheumatol 2012, 8:77-89. 10.2174/157339712802083795, 22231237.
7. McGlashan SR, Cluett EC, Jensen CG, Poole CA. Primary cilia in osteoarthritic chondrocytes: from chondrons to clusters. Dev Dyn 2008, 237:2013-2020. 10.1002/dvdy.21501, 18330928.
8. Scanzello CR, Goldring SR. The role of synovitis in osteoarthritis pathogenesis. Bone 2012, 51:249-257. 10.1016/j.bone.2012.02.012, 3372675, 22387238.
9. Gravallese EM, Goldring SR. Cellular mechanisms and the role of cytokines in bone erosions in rheumatoid arthritis. Arthritis Rheum 2000, 43:2143-2151. 10.1002/1529-0131(200010)43:10<2143::AID-ANR1>3.0.CO;2-S, 11037873.
10. Citri A, Yarden Y. EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 2006, 7:505-516. 10.1038/nrm1962, 16829981.
11. Schneider MR, Sibilia M, Erben RG. The EGFR network in bone biology and pathology. Trends Endocrinol Metab 2009, 20:517-524. 10.1016/j.tem.2009.06.008, 19819718.
12. Xian CJ. Roles of epidermal growth factor family in the regulation of postnatal somatic growth. Endocr Rev 2007, 28:284-296. 10.1210/er.2006-0049, 17322455.
13. Zhang X, Tamasi J, Lu X, Zhu J, Chen H, Tian X, Lee TC, Threadgill DW, Kream BE, Kang Y, Partridge NC, Qin L. Epidermal growth factor receptor plays an anabolic role in bone metabolism in vivo. J Bone Miner Res 2011, 26:1022-1034. 10.1002/jbmr.295, 3179301, 21542005.
14. Zhang X, Siclari VA, Lan S, Zhu J, Koyama E, Dupuis HL, Enomoto-Iwamoto M, Beier F, Qin L. The critical role of the epidermal growth factor receptor in endochondral ossification. J Bone Miner Res 2011, 26:2622-2633. 10.1002/jbmr.502, 3200483, 21887704.
15. Sibilia M, Wagner B, Hoebertz A, Elliott C, Marino S, Jochum W, Wagner EF. Mice humanised for the EGF receptor display hypomorphic phenotypes in skin, bone and heart. Development 2003, 130:4515-4525. 10.1242/dev.00664, 12925580.
16. 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, 51:131-141. 10.1016/j.bone.2012.04.012, 22575362.
17. Lo SF, Wan L, Lin HC, Huang CM, Chen SY, Liu SC, Tsai FJ. Association of rheumatoid arthritis risk with EGFR genetic polymorphisms in Taiwan's Han Chinese population. Rheumatol Int 2012, 32:2301-2306. 10.1007/s00296-011-1961-4, 21604062.
18. Hallbeck AL, Walz TM, Briheim K, Wasteson A. TGF-α and ErbB2 production in synovial joint tissue: increased expression in arthritic joints. Scand J Rheumatol 2005, 34:204-211. 10.1080/03009740510017715, 16134726.
19. Swanson CD, Akama-Garren EH, Stein EA, Petralia JD, Ruiz PJ, Edalati A, Lindstrom TM, Robinson WH. Inhibition of epidermal growth factor receptor tyrosine kinase ameliorates collagen-induced arthritis. J Immunol 2012, 188:3513-3521. 10.4049/jimmunol.1102693, 3311775, 22393153.
20. Sumariwalla PF, Jin P, Zhang J, Ni I, Crawford D, Shepard HM, Paleolog EM, Feldmann M. Antagonism of the human epidermal growth factor receptor family controls disease severity in murine collagen-induced arthritis. Arthritis Rheum 2008, 58:3071-3080. 10.1002/art.23885, 18821697.
21. 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. 10.1038/labinvest.2009.111, 19823173.
22. 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, 56:3693-3705. 10.1002/art.22968, 17968906.
23. Iacob S, Cs-Szabo G. Biglycan regulates the expression of EGF receptors through EGF signaling pathways in human articular chondrocytes. Connect Tissue Res 2010, 51:347-358. 10.3109/03008200903427695, 20367117.
24. Zhang YW, Vande Woude GF. Mig-6, signal transduction, stress response and cancer. Cell Cycle 2007, 6:507-513. 10.4161/cc.6.5.3928, 17351343.
25. Zhang X, Pickin KA, Bose R, Jura N, Cole PA, Kuriyan J. Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 2007, 450:741-744. 10.1038/nature05998, 3561764, 18046415.
26. Zhang YW, Su Y, Lanning N, Swiatek PJ, Bronson RT, Sigler R, Martin RW, Vande Woude GF. Targeted disruption of Mig-6 in the mouse genome leads to early onset degenerative joint disease. Proc Natl Acad Sci U S A 2005, 102:11740-11745. 10.1073/pnas.0505171102, 1187996, 16087873.
27. Velasquillo C, Garciadiego-Cázares D, Almonte M, Bustamante M, Ibarra C, Kouri JB, Chimal-Monroy J. Expression of MIG-6, WNT-9A, and WNT-7B during osteoarthritis. Ann N Y Acad Sci 2007, 1117:175-180. 10.1196/annals.1402.019, 18056042.
28. Louboutin H, Debarge R, Richou J, Selmi TA, Donell ST, Neyret P, Dubrana F. Osteoarthritis in patients with anterior cruciate ligament rupture: a review of risk factors. Knee 2009, 16:239-244. 10.1016/j.knee.2008.11.004, 19097796.
29. Nelson F, Billinghurst RC, Pidoux I, Reiner A, Langworthy M, McDermott M, Malogne T, Sitler DF, Kilambi NR, Lenczner E, Poole AR. Early post-traumatic osteoarthritis-like changes in human articular cartilage following rupture of the anterior cruciate ligament. Osteoarthritis Cartilage 2006, 14:114-119. 10.1016/j.joca.2005.08.005, 16242972.
30. Kuroki K, Cook CR, Cook JL. Subchondral bone changes in three different canine models of osteoarthritis. Osteoarthritis Cartilage 2011, 19:1142-1149. 10.1016/j.joca.2011.06.007, 21736944.
31. Jin N, Cho SN, Raso MG, Wistuba I, Smith Y, Yang Y, Kurie JM, Yen R, Evans CM, Ludwig T, Jeong JW, DeMayo FJ. Mig-6 is required for appropriate lung development and to ensure normal adult lung homeostasis. Development 2009, 136:3347-3356. 10.1242/dev.032979, 2739148, 19710174.
32. Kamekura S, Hoshi K, Shimoaka T, Chung U, Chikuda H, Yamada T, Uchida M, Ogata N, Seichi A, Nakamura K, Kawaguchi H. Osteoarthritis development in novel experimental mouse models induced by knee joint instability. Osteoarthritis Cartilage 2005, 13:632-641. 10.1016/j.joca.2005.03.004, 15896985.
33. Pan J, Wang B, Li W, Zhou X, Scherr T, Yang Y, Price C, Wang L. Elevated cross-talk between subchondral bone and cartilage in osteoarthritic joints. Bone 2012, 51:212-217. 10.1016/j.bone.2011.11.030, 3335971, 22197997.
34. Joiner DM, Less KD, Van Wieren EM, Hess D, Williams BO. Heterozygosity for an inactivating mutation in low-density lipoprotein-related receptor 6 (Lrp6) increases osteoarthritis severity in mice after ligament and meniscus injury. Osteoarthritis Cartilage 2013, 21:1576-1585. 10.1016/j.joca.2013.05.019, 23756208.
35. Pritzker KP, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, Salter D, van den Berg WB. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 2006, 14:13-29. 10.1016/j.joca.2005.07.014, 16242352.
36. Yi T, Lee HL, Cha JH, Ko SI, Kim HJ, Shin HI, Woo KM, Ryoo HM, Kim GS, Baek JH. Epidermal growth factor receptor regulates osteoclast differentiation and survival through cross-talking with RANK signaling. J Cell Physiol 2008, 217:409-422. 10.1002/jcp.21511, 18543257.
37. Bell NH. RANK ligand and the regulation of skeletal remodeling. J Clin Invest 2003, 111:1120-1122. 10.1172/JCI18358, 152945, 12697730.
38. Pante G, Thompson J, Lamballe F, Iwata T, Ferby I, Barr FA, Davies AM, Maina F, Klein R. Mitogen-inducible gene 6 is an endogenous inhibitor of HGF/Met-induced cell migration and neurite growth. J Cell Biol 2005, 171:337-348. 10.1083/jcb.200502013, 2171179, 16247031.
39. Rush JS, Quinalty LM, Engelman L, Sherry DM, Ceresa BP. Endosomal accumulation of the activated epidermal growth factor receptor (EGFR) induces apoptosis. J Biol Chem 2012, 287:712-722. 3249126, 22102283.
40. Bhowmik A, Das N, Pal U, Mandal M, Bhattacharya S, Sarkar M, Jaisankar P, Maiti NC, Ghosh MK. 2,2′-diphenyl-3,3′-diindolylmethane: a potent compound induces apoptosis in breast cancer cells by inhibiting EGFR pathway. PLoS One 2013, 8:e59798. 10.1371/journal.pone.0059798, 3610887, 23555785.
41. Tracy S, Mukohara T, Hansen M, Meyerson M, Johnson BE, Janne PA. Gefitinib induces apoptosis in the EGFRL858R non-small-cell lung cancer cell line H3255. Cancer Res 2004, 64:7241-7244. 10.1158/0008-5472.CAN-04-1905, 15492241.
42. Hopkins S, Linderoth E, Hantschel O, Suarez-Henriques P, Pilia G, Kendrick H, Smalley MJ, Superti-Furga G, Ferby I. Mig6 is a sensor of EGF receptor inactivation that directly activates c-Abl to induce apoptosis during epithelial homeostasis. Dev Cell 2012, 23:547-559. 10.1016/j.devcel.2012.08.001, 3657149, 22975324.
43. Chen YC, Colvin ES, Maier BF, Mirmira RG, Fueger PT. Mitogen-inducible gene 6 triggers apoptosis and exacerbates ER stress-induced β-cell death. Mol Endocrinol 2013, 27:162-171. 10.1210/me.2012-1174, 3545216, 23204325.
44. Xu J, Keeton AB, Wu L, Franklin JL, Cao X, Messina JL. Gene 33 inhibits apoptosis of breast cancer cells and increases poly(ADP-ribose) polymerase expression. Breast Cancer Res Treat 2005, 91:207-215. 10.1007/s10549-005-1040-1, 15952054.
45. Amishima M, Munakata M, Nasuhara Y, Sato A, Takahashi T, Homma Y, Kawakami Y. Expression of epidermal growth factor and epidermal growth factor receptor immunoreactivity in the asthmatic human airway. Am J Respir Crit Care Med 1998, 157:1907-1912. 10.1164/ajrccm.157.6.9609040, 9620926.
46. Hur GY, Lee SY, Lee SH, Kim SJ, Lee KJ, Jung JY, Lee EJ, Kang EH, Jung KH, Lee SY, Kim JH, Shin C, Shim JJ, In KH, Kang KH, Yoo SH. Potential use of an anticancer drug gefinitib, an EGFR inhibitor, on allergic airway inflammation. Exp Mol Med 2007, 39:367-375. 10.1038/emm.2007.41, 17603291.
47. Makkinje A, Quinn DA, Chen A, Cadilla CL, Force T, Bonventre JV, Kyriakis JM. 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, 275:17838-17847. 3668664, 10749885.
48. Mateescu RG, Todhunter RJ, Lust G, Burton-Wurster N. Increased MIG-6 mRNA transcripts in osteoarthritic cartilage. Biochem Biophys Res Commun 2005, 332:482-486. 10.1016/j.bbrc.2005.04.144, 15910752.
49. Tapper JE, Funakoshi Y, Hariu M, Marchuk L, Thornton GM, Ronsky JL, Zernicke R, Shrive NG, Frank CB. ACL/MCL transection affects knee ligament insertion distance of healing and intact ligaments during gait in the ovine model. J Biomech 2009, 42:1825-1833. 10.1016/j.jbiomech.2009.05.034, 19643414.
50. Kreider JM, Goldstein SA. Trabecular bone mechanical properties in patients with fragility fractures. Clin Orthop Relat Res 2009, 467:1955-1963. 10.1007/s11999-009-0751-8, 2706345, 19247731.
51. Turk HF, Monk JM, Fan YY, Callaway ES, Weeks B, Chapkin RS. Inhibitory effects of ω-3 fatty acids on injury-induced epidermal growth factor receptor transactivation contribute to delayed wound healing. Am J Physiol Cell Physiol 2013, 304:C905-C917. 10.1152/ajpcell.00379.2012, 23426968.
52. Goldring SR. The role of bone in osteoarthritis pathogenesis. Rheum Dis Clin North Am 2008, 34:561-571. 10.1016/j.rdc.2008.07.001, 18687272.