Extracellular matrix turnover and inflammation in chemically-induced TMJ arthritis mouse models

English version

Autoři: Mallory Morel ^aff001; Angela Ruscitto ^aff001; Serhiy Pylawka ^aff001; Gwendolyn Reeve ^aff002; Mildred C. Embree ^aff001
Působiště autorů: TMJ Biology and Regenerative Medicine Laboratory, College of Dental Medicine, Columbia University Irving Medical Center, New York, NY, United States of America ^aff001; Division of Oral and Maxillofacial Surgery, New York Presbyterian Weill Cornell Medical Center, New York, NY, United States of America ^aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223244

Souhrn

The temporomandibular joint (TMJ) is a fibrocartilaginous tissue critical for chewing and speaking. In patients with temporomandibular disorders (TMDs), permanent tissue loss can occur. Recapitulating the complexity of TMDs in animal models is difficult, yet critical for the advent of new therapies. Synovial fluid from diseased human samples revealed elevated levels of tumor necrosis factor alpha (TNF-alpha). Here, we propose to recapitulate these findings in mice by subjecting murine TMJs with TNF-alpha or CFA (Complete Freund’s Adjuvant) in mandibular condyle explant cultures and by local delivery in vivo using TMJ intra-articular injections. Both TNF-alpha and CFA delivery to whole mandibular explants and in vivo increased extracellular matrix deposition and increased cartilage thickness, while TNF-alpha treated explants had increased expression of inflammatory cytokines and degradative enzymes. Moreover, the application of TNF-alpha or CFA in both models reduced cell number. CFA delivery in vivo caused soft tissue inflammation, including pannus formation. Our work provides two methods of chemically induced TMJ inflammatory arthritis through a condyle explant model and intra-articular injection model that replicate findings seen in synovial fluid of human patients, which can be used for further studies delineating the mechanisms underlying TMJ pathology.

Klíčová slova:

Arthritis – Cartilage – Collagens – Extracellular matrix – Chondrocytes – Inflammation – Mouse models – Synovial fluid

Zdroje

1. International Association for the Study of Pain. Task Force on Epidemiology., Crombie IKEpidemiology of pain: a report of the Task Force on Epidemiology of the International Association for the Study of Pain. Seattle: IASP Press; 1999. xi, 321 p. p.

2. Scrivani SJ, Keith DA, Kaban LB. Temporomandibular disorders. N Engl J Med. 2008;359(25):2693–705. Epub 2008/12/19. doi: 10.1056/NEJMra0802472 19092154.

3. Ohrbach R, Dworkin SF. The Evolution of TMD Diagnosis: Past, Present, Future. J Dent Res. 2016;95(10):1093–101. Epub 2016/06/18. doi: 10.1177/0022034516653922 27313164; PubMed Central PMCID: PMC5004241.

4. Slade GD, Bair E, Greenspan JD, Dubner R, Fillingim RB, Diatchenko L, et al. Signs and symptoms of first-onset TMD and sociodemographic predictors of its development: the OPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T20-32 e1-3. Epub 2013/12/07. doi: 10.1016/j.jpain.2013.07.014 24275221; PubMed Central PMCID: PMC3857109.

5. Wang XD, Zhang JN, Gan YH, Zhou YH. Current understanding of pathogenesis and treatment of TMJ osteoarthritis. J Dent Res. 2015;94(5):666–73. Epub 2015/03/07. doi: 10.1177/0022034515574770 25744069.

6. Al-Baghdadi M, Durham J, Araujo-Soares V, Robalino S, Errington L, Steele J. TMJ Disc Displacement without Reduction Management: A Systematic Review. J Dent Res. 2014;93(7 Suppl):37S–51S. Epub 2014/03/25. doi: 10.1177/0022034514528333 24659775; PubMed Central PMCID: PMC4293719.

7. List T, Dworkin SF. Comparing TMD diagnoses and clinical findings at Swedish and US TMD centers using research diagnostic criteria for temporomandibular disorders. J Orofac Pain. 1996;10(3):240–53. Epub 1996/07/01. 9161229.

8. Embree MC, Kilts TM, Ono M, Inkson CA, Syed-Picard F, Karsdal MA, et al. Biglycan and fibromodulin have essential roles in regulating chondrogenesis and extracellular matrix turnover in temporomandibular joint osteoarthritis. The American journal of pathology. 2010;176(2):812–26. Epub 2009/12/26. doi: 10.2353/ajpath.2010.090450 20035055; PubMed Central PMCID: PMC2808087.

9. Ohrbach R, Fillingim RB, Mulkey F, Gonzalez Y, Gordon S, Gremillion H, et al. Clinical findings and pain symptoms as potential risk factors for chronic TMD: descriptive data and empirically identified domains from the OPPERA case-control study. J Pain. 2011;12(11 Suppl):T27–45. Epub 2011/12/07. doi: 10.1016/j.jpain.2011.09.001 22074750; PubMed Central PMCID: PMC3443556.

10. Fenton BT, Goulet JL, Bair MJ, Cowley T, Kerns RD. Relationships Between Temporomandibular Disorders, MSD Conditions, and Mental Health Comorbidities: Findings from the Veterans Musculoskeletal Disorders Cohort. Pain Med. 2018;19(suppl_1):S61–S8. Epub 2018/09/12. doi: 10.1093/pm/pny145 30203016.

11. Smith SB, Mir E, Bair E, Slade GD, Dubner R, Fillingim RB, et al. Genetic variants associated with development of TMD and its intermediate phenotypes: the genetic architecture of TMD in the OPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T91-101 e1-3. Epub 2013/12/07. doi: 10.1016/j.jpain.2013.09.004 24275226; PubMed Central PMCID: PMC3855664.

12. Fillingim RB, Ohrbach R, Greenspan JD, Knott C, Diatchenko L, Dubner R, et al. Psychological factors associated with development of TMD: the OPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T75–90. Epub 2013/12/07. doi: 10.1016/j.jpain.2013.06.009 24275225; PubMed Central PMCID: PMC3855656.

13. Bair E, Ohrbach R, Fillingim RB, Greenspan JD, Dubner R, Diatchenko L, et al. Multivariable modeling of phenotypic risk factors for first-onset TMD: the OPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T102–15. Epub 2013/12/07. doi: 10.1016/j.jpain.2013.09.003 24275218; PubMed Central PMCID: PMC4036699.

14. Goldring MB, Otero M, Plumb DA, Dragomir C, Favero M, El Hachem K, et al. Roles of inflammatory and anabolic cytokines in cartilage metabolism: signals and multiple effectors converge upon MMP-13 regulation in osteoarthritis. European cells & materials. 2011;21:202.

15. Sandell LJ, Aigner T. Articular cartilage and changes in arthritis: cell biology of osteoarthritis. Arthritis Research & Therapy. 2001;3(2):107.

16. Goldring MB. Osteoarthritis and cartilage: the role of cytokines. Current rheumatology reports. 2000;2(6):459–65. 11123098

17. Rintala M, Metsaranta M, Saamanen AM, Vuorio E, Ronning O. Abnormal craniofacial growth and early mandibular osteoarthritis in mice harbouring a mutant type II collagen transgene. Journal of anatomy. 1997;190 (Pt 2):201–8. Epub 1997/02/01. doi: 10.1046/j.1469-7580.1997.19020201.x 9061443; PubMed Central PMCID: PMC1467599.

18. Gu Z, Zhou Y, Zhang Y, Zhao S, Liu J, Hu J. An animal model for inducing anterior disc displacement of the temporomandibular joint. Journal of orofacial pain. 2006;20(2):166–73. Epub 2006/05/20. 16708834.

19. Cledes G, Felizardo R, Foucart JM, Carpentier P. Validation of a chemical osteoarthritis model in rabbit temporomandibular joint: a compliment to biomechanical models. International journal of oral and maxillofacial surgery. 2006;35(11):1026–33. Epub 2006/07/11. doi: 10.1016/j.ijom.2006.05.003 16829037.

20. Embree MC, Chen M, Pylawka S, Kong D, Iwaoka GM, Kalajzic I, et al. Exploiting endogenous fibrocartilage stem cells to regenerate cartilage and repair joint injury. Nat Commun. 2016;7:13073. Epub 2016/10/11. doi: 10.1038/ncomms13073 27721375; PubMed Central PMCID: PMC5062541.

21. Embree MC, Iwaoka GM, Kong D, Martin BN, Patel RK, Lee AH, et al. Soft tissue ossification and condylar cartilage degeneration following TMJ disc perforation in a rabbit pilot study. Osteoarthritis Cartilage. 2015;23(4):629–39. Epub 2015/01/13. doi: 10.1016/j.joca.2014.12.015 25573797; PubMed Central PMCID: PMC4368469.

22. Li W, Wu M, Jiang S, Ding W, Luo Q, Shi J. Expression of ADAMTs-5 and TIMP-3 in the condylar cartilage of rats induced by experimentally created osteoarthritis. Archives of oral biology. 2014;59(5):524–9. Epub 2014/03/19. doi: 10.1016/j.archoralbio.2014.02.016 24632095.

23. Chantaracherd P, John MT, Hodges JS, Schiffman EL. Temporomandibular joint disorders' impact on pain, function, and disability. J Dent Res. 2015;94(3 Suppl):79S–86S. Epub 2015/01/13. doi: 10.1177/0022034514565793 25572112; PubMed Central PMCID: PMC4336155.

24. Garnero P, Ayral X, Rousseau JC, Christgau S, Sandell LJ, Dougados M, et al. Uncoupling of type II collagen synthesis and degradation predicts progression of joint damage in patients with knee osteoarthritis. Arthritis Rheum. 2002;46(10):2613–24. Epub 2002/10/18. doi: 10.1002/art.10576 12384919.

25. Lohmander LS, Atley LM, Pietka TA, Eyre DR. The release of crosslinked peptides from type II collagen into human synovial fluid is increased soon after joint injury and in osteoarthritis. Arthritis Rheum. 2003;48(11):3130–9. Epub 2003/11/13. doi: 10.1002/art.11326 14613275.

26. Vos LM, Kuijer R, Huddleston Slater JJ, Stegenga B. Alteration of cartilage degeneration and inflammation markers in temporomandibular joint osteoarthritis occurs proportionally. J Oral Maxillofac Surg. 2013;71(10):1659–64. Epub 2013/08/13. doi: 10.1016/j.joms.2013.06.201 23932112.

27. Ok SM, Lee SM, Park HR, Jeong SH, Ko CC, Kim YI. Concentrations of CTX I, CTX II, DPD, and PYD in the urine as a biomarker for the diagnosis of temporomandibular joint osteoarthritis: A preliminary study. Cranio. 2017:1–7. Epub 2017/08/08. doi: 10.1080/08869634.2017.1361624 28782462; PubMed Central PMCID: PMC5814361.

28. Kapoor M, Martel-Pelletier J, Lajeunesse D, Pelletier JP, Fahmi H. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol. 2011;7(1):33–42. Epub 2010/12/02. doi: 10.1038/nrrheum.2010.196 21119608.

29. Kellesarian SV, Al-Kheraif AA, Vohra F, Ghanem A, Malmstrom H, Romanos GE, et al. Cytokine profile in the synovial fluid of patients with temporomandibular joint disorders: A systematic review. Cytokine. 2016;77:98–106. Epub 2015/11/12. doi: 10.1016/j.cyto.2015.11.005 26556103.

30. Wuelling M, Vortkamp A. Cartilage explant cultures. Methods Mol Biol. 2014;1130:89–97. Epub 2014/02/01. doi: 10.1007/978-1-62703-989-5_7 24482167.

31. Mak KK, Kronenberg HM, Chuang PT, Mackem S, Yang Y. Indian hedgehog signals independently of PTHrP to promote chondrocyte hypertrophy. Development. 2008;135(11):1947–56. Epub 2008/04/25. doi: 10.1242/dev.018044 18434416.

32. Minina E, Kreschel C, Naski MC, Ornitz DM, Vortkamp A. Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell. 2002;3(3):439–49. Epub 2002/10/04. 12361605.

33. Minina E, Wenzel HM, Kreschel C, Karp S, Gaffield W, McMahon AP, et al. BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development. 2001;128(22):4523–34. Epub 2001/11/21. 11714677.

34. Mau E, Whetstone H, Yu C, Hopyan S, Wunder JS, Alman BA. PTHrP regulates growth plate chondrocyte differentiation and proliferation in a Gli3 dependent manner utilizing hedgehog ligand dependent and independent mechanisms. Dev Biol. 2007;305(1):28–39. Epub 2007/03/03. doi: 10.1016/j.ydbio.2007.01.031 17328886.

35. Xue XT, Kou XX, Li CS, Bi RY, Meng Z, Wang XD, et al. Progesterone attenuates temporomandibular joint inflammation through inhibition of NF-kappaB pathway in ovariectomized rats. Sci Rep. 2017;7(1):15334. Epub 2017/11/12. doi: 10.1038/s41598-017-15285-w 29127312; PubMed Central PMCID: PMC5681685.

36. Wang XD, Kou XX, Mao JJ, Gan YH, Zhou YH. Sustained inflammation induces degeneration of the temporomandibular joint. J Dent Res. 2012;91(5):499–505. Epub 2012/03/20. doi: 10.1177/0022034512441946 22427270; PubMed Central PMCID: PMC3327731.

37. Vos LM, Kuijer R, Huddleston Slater JJR, Stegenga B. Alteration of Cartilage Degeneration and Inflammation Markers in Temporomandibular Joint Osteoarthritis Occurs Proportionally. Journal of Oral and Maxillofacial Surgery. 2013;71(10):1659–64. doi: 10.1016/j.joms.2013.06.201 23932112

38. Vilcek J, Palombella VJ, Henriksen-DeStefano D, Swenson C, Feinman R, Hirai M, et al. Fibroblast growth enhancing activity of tumor necrosis factor and its relationship to other polypeptide growth factors. Journal of Experimental Medicine. 1986;163(3):632–43. doi: 10.1084/jem.163.3.632 3512757

39. Byun S, Sinskey YL, Lu YC, Frank EH, Grodzinsky AJ. Transport and binding of tumor necrosis factor-α in articular cartilage depend on its quaternary structure. Archives of biochemistry and biophysics. 2013;540(1–2):1–8. doi: 10.1016/j.abb.2013.10.003 24135706

40. Sandell LJ, Aigner T. Articular cartilage and changes in arthritis. An introduction: cell biology of osteoarthritis. Arthritis Res. 2001;3(2):107–13. doi: 10.1186/ar148 11178118.

41. Goldring MB. Update on the biology of the chondrocyte and new approaches to treating cartilage diseases. Best Pract Res Clin Rheumatol. 2006;20(5):1003–25. doi: 10.1016/j.berh.2006.06.003 16980220.

42. Silbermann M, Livne E. Age-related degenerative changes in the mouse mandibular joint. J Anat. 1979;129(Pt 3):507–20. 541239.

43. Paegle DI, Holmlund A, Hjerpe A. Expression of proteoglycan mRNA in patients with painful clicking and chronic closed lock of the temporomandibular joint. Int J Oral Maxillofac Surg. 2005;34(6):656–8. doi: 10.1016/j.ijom.2005.02.008 16053890.

44. Meng J, Ma X, Ma D, Xu C. Microarray analysis of differential gene expression in temporomandibular joint condylar cartilage after experimentally induced osteoarthritis. Osteoarthritis Cartilage. 2005;13(12):1115–25. doi: 10.1016/j.joca.2005.03.010 15905105.

45. Axelsson S, Bjornsson S, Holmlund A, Hjerpe A. Metabolic turnover of sulfated glycosaminoglycans and proteoglycans in rabbit temporomandibular joint cartilages with experimentally induced osteoarthrosis. Acta Odontol Scand. 1994;52(2):65–71. doi: 10.3109/00016359409029056 8048323

46. Spears R, Oakes R, Bellinger LL, Hutchins B. Tumour necrosis factor-alpha and apoptosis in the rat temporomandibular joint. Arch Oral Biol. 2003;48(12):825–34. doi: 10.1016/s0003-9969(03)00175-4 14596872.

47. Kaneyama K, Segami N, Nishimura M, Suzuki T, Sato J. Importance of proinflammatory cytokines in synovial fluid from 121 joints with temporomandibular disorders. Br J Oral Maxillofac Surg. 2002;40(5):418–23. 12379189.

48. Fu K, Ma X, Zhang Z, Chen W. Tumor necrosis factor in synovial fluid of patients with temporomandibular disorders. J Oral Maxillofac Surg. 1995;53(4):424–6. doi: 10.1016/0278-2391(95)90717-3 7699497.

49. Kardel R, Ulfgren AK, Reinholt FP, Holmlund A. Inflammatory cell and cytokine patterns in patients with painful clicking and osteoarthritis in the temporomandibular joint. Int J Oral Maxillofac Surg. 2003;32(4):390–6. doi: 10.1054/ijom.2002.0357 14505622.

50. Suzuki T, Segami N, Nishimura M, Nojima T. Co-expression of interleukin-1beta and tumor necrosis factor alpha in synovial tissues and synovial fluids of temporomandibular joint with internal derangement: comparison with histological grading of synovial inflammation. J Oral Pathol Med. 2002;31(9):549–57. doi: 10.1034/j.1600-0714.2002.00022.x 12269994.

51. Puzas JE, Landeau JM, Tallents R, Albright J, Schwarz EM, Landesberg R. Degradative pathways in tissues of the temporomandibular joint. Use of in vitro and in vivo models to characterize matrix metalloproteinase and cytokine activity. Cells Tissues Organs. 2001;169(3):248–56. 11455120.

52. Tiilikainen P, Pirttiniemi P, Kainulainen T, Pernu H, Raustia A. MMP-3 and -8 expression is found in the condylar surface of temporomandibular joints with internal derangement. J Oral Pathol Med. 2005;34(1):39–45. doi: 10.1111/j.1600-0714.2004.00262.x 15610405.

53. Gepstein A, Shapiro S, Arbel G, Lahat N, Livne E. Expression of matrix metalloproteinases in articular cartilage of temporomandibular and knee joints of mice during growth, maturation, and aging. Arthritis Rheum. 2002;46(12):3240–50. doi: 10.1002/art.10690 12483728.

54. Goldring MB. The role of the chondrocyte in osteoarthritis. Arthritis Rheum. 2000;43(9):1916–26. doi: 10.1002/1529-0131(200009)43:9<1916::AID-ANR2>3.0.CO;2-I 11014341.

55. Schaller S, Henriksen K, Hoegh-Andersen P, Sondergaard BC, Sumer EU, Tanko LB, et al. In vitro, ex vivo, and in vivo methodological approaches for studying therapeutic targets of osteoporosis and degenerative joint diseases: how biomarkers can assist? Assay Drug Dev Technol. 2005;3(5):553–80. doi: 10.1089/adt.2005.3.553 16305312.

56. Almarza AJ, Hagandora CK, Henderson SE. Animal Models of Temporomandibular Joint Disorders: Implications for Tissue Engineering Approaches. Annals of Biomedical Engineering. 2011;39(10):2479. doi: 10.1007/s10439-011-0364-8 21822741

57. Shiojiri T, Wada K, Nakajima A, Katayama K, Shibuya A, Kudo C, et al. PPARγ ligands inhibit nitrotyrosine formation and inflammatory mediator expressions in adjuvant-induced rheumatoid arthritis mice. European Journal of Pharmacology. 2002;448(2):231–8. doi: https://doi.org/10.1016/S0014-2999(02)01946-5

58. Ghassemi-Nejad S, Kobezda T, Rauch TA, Matesz C, Glant TT, Mikecz K. Osteoarthritis-like damage of cartilage in the temporomandibular joints in mice with autoimmune inflammatory arthritis. Osteoarthritis and Cartilage. 2011;19(4):458–65. doi: 10.1016/j.joca.2011.01.012 21262368

59. Wang XD, Kou XX, He DQ, Zeng MM, Meng Z, Bi RY, et al. Progression of cartilage degradation, bone resorption and pain in rat temporomandibular joint osteoarthritis induced by injection of iodoacetate. PLoS One. 2012;7(9):e45036. Epub 2012/09/18. doi: 10.1371/journal.pone.0045036 22984604; PubMed Central PMCID: PMC3439407.

60. Wang X-D, Kou X-X, He D-Q, Zeng M-M, Meng Z, Bi R-Y, et al. Progression of Cartilage Degradation, Bone Resorption and Pain in Rat Temporomandibular Joint Osteoarthritis Induced by Injection of Iodoacetate. PLOS ONE. 2012;7(9):e45036. doi: 10.1371/journal.pone.0045036 22984604

61. Snekhalatha U, Anburajan M, Venkatraman B, Menaka M. Evaluation of complete Freund’s adjuvant-induced arthritis in a Wistar rat model. Zeitschrift für Rheumatologie. 2013;72(4):375–82. doi: 10.1007/s00393-012-1083-8 23208192

62. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature. 2003;423(6937):356–61. doi: 10.1038/nature01661 12748655

63. McInnes IB, Schett G. The Pathogenesis of Rheumatoid Arthritis. New England Journal of Medicine. 2011;365(23):2205–19. doi: 10.1056/NEJMra1004965 22150039

64. McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. 2007;7:429. doi: 10.1038/nri2094 17525752

65. Lipsky PE, van der Heijde DMFM, St. Clair EW, Furst DE, Breedveld FC, Kalden JR, et al. Infliximab and Methotrexate in the Treatment of Rheumatoid Arthritis. New England Journal of Medicine. 2000;343(22):1594–602. doi: 10.1056/NEJM200011303432202 11096166

66. Lemos GA, da Silva PLP, Batista AUD, Palomari ET. Experimental model of temporomandibular joint arthritis: Evaluation of contralateral joint and masticatory muscles. Archives of Oral Biology. 2018;95:79–88. doi: 10.1016/j.archoralbio.2018.07.003 30071410

Extracellular matrix turnover and inflammation in chemically-induced TMJ arthritis mouse models

Souhrn

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Zdroje

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