Coordinate Regulation of IL-1beta and MMP-13 in Rat Tendons Following Subrupture Fatigue Damage

Overview

Journal Clin Orthop Relat Res

Publisher Wolters Kluwer

Specialty Orthopedics

Date 2008 May 13

PMID 18470577

Citations 56

Authors

Hui B Sun

Yonghui Li

David T Fung

Robert J Majeska

Mitchell B Schaffler

Evan L Flatow

Affiliations

Soon will be listed here.

Abstract

Mechanical overloading is a major causative factor of tendinopathy; however, its underlying mechanisms are unclear. We hypothesized mechanical overloading would damage tendons and alter genes associated with tendinopathy in a load-dependent manner. To test this hypothesis, we fatigue loaded rat patellar tendons in vivo and measured expression of the matrix-degrading enzyme MMP-13 and the inflammatory cytokine IL-1beta. We also examined these responses in cultured tenocytes exposed to intermittent hydrostatic pressure in vitro. Additionally, we hypothesized load-induced changes in tenocyte MMP-13 expression would be dependent on expression of IL-1beta. In vivo fatigue loading at 1.7% strain caused overt microstructural damage and upregulated expression of MMP-13 and IL-1beta, while 0.6% strain produced only minor changes in matrix microstructure and downregulated expression of both MMP-13 and IL-1beta. Loading of cultured tenocytes at 2.5 and 7.5 MPa produced comparable changes in expression to those of in vivo tendon loading. Blocking IL-1beta expression with siRNA suppressed load-induced both MMP-13 mRNA expression and activity. The data suggest fatigue loading alters expression of MMP-13 and IL-1beta in tendons in vivo and tenocytes in vitro in a load-dependent manner. The data also suggest MMP-13 is regulated by both IL-1beta-dependent and IL-1beta-independent pathways.

Citing Articles

Collagen denaturation in post-run Achilles tendons and Achilles tendinopathy: In vivo mechanophysiology and magnetic resonance imaging.

Fang Y, Zhu D, Wei J, Qian L, Qiu R, Jia T Sci Adv. 2024; 10(40):eado2015.

PMID: 39356750 PMC: 11446262. DOI: 10.1126/sciadv.ado2015.

Upregulation of FABP4 induced inflammation in the pathogenesis of chronic tendinopathy.

Ma Z, Lee A, Kot C, Yung P, Chen S, Lui P J Orthop Translat. 2024; 47:105-115.

PMID: 39007036 PMC: 11245957. DOI: 10.1016/j.jot.2024.06.007.

Establishment of a Mouse Degenerative Model of Patellar Tendinopathy with Upregulation of Inflammation.

Lui P, Liang Z, Tan R, Yung P Int J Mol Sci. 2024; 25(7).

PMID: 38612656 PMC: 11011606. DOI: 10.3390/ijms25073847.

Rat Plantar Fascia Stem/Progenitor Cells Showed Lower Expression of Ligament Markers and Higher Pro-Inflammatory Cytokines after Intensive Mechanical Loading or Interleukin-1β Treatment In Vitro.

Siu W, Ma H, Ko C, Shiu H, Cheng W, Lee Y Cells. 2023; 12(18).

PMID: 37759446 PMC: 10526819. DOI: 10.3390/cells12182222.

Animal model for tendinopathy.

Luo J, Wang Z, Tang C, Yin Z, Huang J, Ruan D J Orthop Translat. 2023; 42:43-56.

PMID: 37637777 PMC: 10450357. DOI: 10.1016/j.jot.2023.06.005.

References

Archambault J, Tsuzaki M, Herzog W, Banes A . Stretch and interleukin-1beta induce matrix metalloproteinases in rabbit tendon cells in vitro. J Orthop Res. 2002; 20(1):36-9. DOI: 10.1016/S0736-0266(01)00075-4. View

Devkota A, Tsuzaki M, Almekinders L, Banes A, Weinhold P . Distributing a fixed amount of cyclic loading to tendon explants over longer periods induces greater cellular and mechanical responses. J Orthop Res. 2007; 25(8):1078-86. DOI: 10.1002/jor.20389. View

Wang J, Iosifidis M, Fu F . Biomechanical basis for tendinopathy. Clin Orthop Relat Res. 2006; 443:320-32. DOI: 10.1097/01.blo.0000195927.81845.46. View

Maffulli N, Wong J, Almekinders L . Types and epidemiology of tendinopathy. Clin Sports Med. 2003; 22(4):675-92. DOI: 10.1016/s0278-5919(03)00004-8. View

Li Z, Yang G, Khan M, Stone D, Woo S, Wang J . Inflammatory response of human tendon fibroblasts to cyclic mechanical stretching. Am J Sports Med. 2004; 32(2):435-40. DOI: 10.1177/0095399703258680. View

Agarwal S, Long P, Gassner R, Piesco N, Buckley M . Cyclic tensile strain suppresses catabolic effects of interleukin-1beta in fibrochondrocytes from the temporomandibular joint. Arthritis Rheum. 2001; 44(3):608-17. PMC: 4955545. DOI: 10.1002/1529-0131(200103)44:3<608::AID-ANR109>3.0.CO;2-2. View

Hernandez M, Valenzuela M, Lopez-Otin C, Alvarez J, Lopez J, Vernal R . Matrix metalloproteinase-13 is highly expressed in destructive periodontal disease activity. J Periodontol. 2006; 77(11):1863-70. DOI: 10.1902/jop.2006.050461. View

Sun H, Yokota H . Reduction of cytokine-induced expression and activity of MMP-1 and MMP-13 by mechanical strain in MH7A rheumatoid synovial cells. Matrix Biol. 2002; 21(3):263-70. DOI: 10.1016/s0945-053x(02)00003-3. View

Zipfel W, Williams R, Christie R, Nikitin A, Hyman B, Webb W . Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci U S A. 2003; 100(12):7075-80. PMC: 165832. DOI: 10.1073/pnas.0832308100. View

10.

Scott A, Cook J, Hart D, Walker D, Duronio V, Khan K . Tenocyte responses to mechanical loading in vivo: a role for local insulin-like growth factor 1 signaling in early tendinosis in rats. Arthritis Rheum. 2007; 56(3):871-81. DOI: 10.1002/art.22426. View

11.

Wang J, Jia F, Yang G, Yang S, Campbell B, Stone D . Cyclic mechanical stretching of human tendon fibroblasts increases the production of prostaglandin E2 and levels of cyclooxygenase expression: a novel in vitro model study. Connect Tissue Res. 2003; 44(3-4):128-33. DOI: 10.1080/03008200390223909. View

12.

Skutek M, van Griensven M, Zeichen J, Brauer N, Bosch U . Cyclic mechanical stretching enhances secretion of Interleukin 6 in human tendon fibroblasts. Knee Surg Sports Traumatol Arthrosc. 2001; 9(5):322-6. DOI: 10.1007/s001670100217. View

13.

Soslowsky L, Thomopoulos S, Tun S, Flanagan C, Keefer C, Mastaw J . Neer Award 1999. Overuse activity injures the supraspinatus tendon in an animal model: a histologic and biomechanical study. J Shoulder Elbow Surg. 2000; 9(2):79-84. View

14.

Nakama L, King K, Abrahamsson S, Rempel D . VEGF, VEGFR-1, and CTGF cell densities in tendon are increased with cyclical loading: An in vivo tendinopathy model. J Orthop Res. 2006; 24(3):393-400. DOI: 10.1002/jor.20053. View

15.

Williams R, Zipfel W, Webb W . Interpreting second-harmonic generation images of collagen I fibrils. Biophys J. 2004; 88(2):1377-86. PMC: 1305140. DOI: 10.1529/biophysj.104.047308. View

16.

Lo I, Marchuk L, Hollinshead R, Hart D, Frank C . Matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase mRNA levels are specifically altered in torn rotator cuff tendons. Am J Sports Med. 2004; 32(5):1223-9. DOI: 10.1177/0363546503262200. View

17.

Kannus P, Jozsa L . Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg Am. 1991; 73(10):1507-25. View

18.

Sharma P, Maffulli N . Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am. 2005; 87(1):187-202. DOI: 10.2106/JBJS.D.01850. View

19.

Tsuzaki M, Guyton G, Garrett W, Archambault J, Herzog W, Almekinders L . IL-1 beta induces COX2, MMP-1, -3 and -13, ADAMTS-4, IL-1 beta and IL-6 in human tendon cells. J Orthop Res. 2003; 21(2):256-64. DOI: 10.1016/S0736-0266(02)00141-9. View

20.

Archambault J, Tsuzaki M, Herzog W, Banes A . Rabbit tendon cells produce MMP-3 in response to fluid flow without significant calcium transients. J Biomech. 2002; 35(3):303-9. DOI: 10.1016/s0021-9290(01)00217-2. View