Distribution of pericellular matrix molecules in the temporomandibular joint and their chondroprotective effects against inflammation

Abstract

A type of collagen found surrounding cells in jaw cartilage may help protect against inflammation associated with osteoarthritis. Cells called chondrocytes, which are responsible for maintaining healthy joint cartilage, are surrounded by a thin matrix layer known as the pericellular matrix (PCM). While interactions between chondrocytes and PCM molecules have been analyzed in knee joints, little is known about PCM molecules in the temporomandibular joint, where the upper jaw links to the skull. Wei Seong Toh at the National University of Singapore and co-workers investigated three PCM molecules (collagen VI, collagen IV and laminin) in rat jaws, and discovered that collagen VI is the most widely distributed across jaw cartilage. Pre-treating chondrocytes with collagen VI reduced nitric oxide levels and limited potentially damaging expression of some genes, thereby protecting the cells from inflammation. The discovery could inform osteoarthritis treatments.

Keywords

cartilage / chondrocytes / collagen IV / collagen VI / inflammation / laminin / pericellular matrix / temporomandibular joint

References

[1] Poole CA, Flint MH, Beaumont BW. Chondrons in cartilage: ultrastructural analysis of the pericellular microenvironment in adult human articular cartilages. J Orthop Res, 1987, 5(4): 509-522.

[2] Wilusz RE, Sanchez-Adams J, Guilak F. The structure and function of the pericellular matrix of articular cartilage. Matrix Biol, 2014, 39: 25-32.

[3] Schminke B, Frese J, Bode C. Laminins and nidogens in the pericellular matrix of chondrocytes: their role in osteoarthritis and chondrogenic differentiation. Am J Pathol, 2016, 186(2): 410-418.

[4] Guilak F, Alexopoulos LG, Upton ML. The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage. Ann N Y Acad Sci, 2006, 1068: 498-512.

[5] Hing WA, Sherwin AF, Poole CA. The influence of the pericellular microenvironment on the chondrocyte response to osmotic challenge. Osteoarthr Cartil, 2002, 10(4): 297-307.

[6] Poole CA, Ayad S, Schofield JR. Chondrons from articular cartilage: I. Immunolocalization of type VI collagen in the pericellular capsule of isolated canine tibial chondrons. J Cell Sci, 1988, 90(4): 635-643.

[7] Poole AR, Rosenberg LC, Reiner A. Contents and distributions of the proteoglycans decorin and biglycan in normal and osteoarthritic human articular cartilage. J Orthop Res, 1996, 14(5): 681-689.

[8] Pufe T, Petersen WJ, Miosge N. Endostatin/collagen XVIII—an inhibitor of angiogenesis—is expressed in cartilage and fibrocartilage. Matrix Biol, 2004, 23(5): 267-276.

[9] Kvist AJ, Nyström A, Hultenby K. The major basement membrane components localize to the chondrocyte pericellular matrix—a cartilage basement membrane equivalent?. Matrix Biol, 2008, 27(1): 22-33.

[10] Kruegel J, Miosge N. Basement membrane components are key players in specialized extracellular matrices. Cell Mol Life Sci, 2010, 67(17): 2879-2895.

[11] Smith SM, Shu C, Melrose J. Comparative immunolocalisation of perlecan with collagen II and aggrecan in human foetal, newborn and adult ovine joint tissues demonstrates perlecan as an early developmental chondrogenic marker. Histochem Cell Biol, 2010, 134(3): 251-263.

[12] Toh WS, Foldager CB, Olsen BR. Basement membrane molecule expression attendant to chondrogenesis by nucleus pulposus cells and mesenchymal stem cells. J Orthop Res, 2013, 31(7): 1136-1143.

[13] Cao L, Guilak F, Setton LA. Three-dimensional morphology of the pericellular matrix of intervertebral disc cells in the rat. J Anat, 2007, 211(4): 444-452.

[14] Foldager CB, Toh WS, Gomoll AH. Distribution of basement membrane molecules, laminin and collagen type IV, in normal and degenerated cartilage tissues. Cartilage, 2014, 5(2): 123-132.

[15] Loreto C, Galanti C, Almeida LE. Expression and localization of aquaporin-1 in temporomandibular joint disc with internal derangement. J Oral Pathol Med, 2012, 41(8): 642-647.

[16] Fang W, Friis TE, Long X. Expression of chondromodulin-1 in the temporomandibular joint condylar cartilage and disc. J Oral Pathol Med, 2010, 39(4): 356-360.

[17] Figueroba SR, Desjardins MP, Ferreira LE. The influence of altered occlusion on pro-inflammatory cytokine levels in the TMJ synovial tissues of rats. Arch Oral Biol, 2014, 59(11): 1164-1171.

[18] Toh WS, Guo XM, Choo AB. Differentiation and enrichment of expandable chondrogenic cells from human embryonic stem cells in vitro. J Cell Mol Med, 2009, 13(9b): 3570-3590.

[19] Toh WS, Yap AU, Lim SY. In vitro biocompatibility of contemporary bulk-fill composites. Oper Dent, 2015, 40(6): 644-652.

[20] Agarwal S, Long P, Gassner R. Cyclic tensile strain suppresses catabolic effects of interleukin-1beta in fibrochondrocytes from the temporomandibular joint. Arthritis Rheum, 2001, 44(3): 608-617.

[21] Alexopoulos LG, Youn I, bonaldo P. Developmental and osteoarthritic changes in Col6a1-knockout mice: biomechanics of type VI collagen in the cartilage pericellular matrix. Arthritis Rheum, 2009, 60(3): 771-779.

[22] Mizoguchi I, Takahashi I, Nakamura M. An immunohistochemical study of regional differences in the distribution of type I and type II collagens in rat mandibular condylar cartilage. Arch Oral Biol, 1996, 41(8/9): 863-869.

[23] de Bont LG, Boering G, Havinga P. Spatial arrangement of collagen fibrils in the articular cartilage of the mandibular condyle: a light microscopic and scanning electron microscopic study. J Oral Maxillofac Surg, 1984, 42(5): 306-313.

[24] Wadhwa S, Kapila S. TMJ disorders: future innovations in diagnostics and therapeutics. J Dent Educ, 2008, 72(8): 930-947.

[25] Smeriglio P, Dhulipala L, Lai JH. Collagen VI enhances cartilage tissue generation by stimulating chondrocyte proliferation. Tissue Eng Part A, 2015, 21(3/4): 840-849.

[26] Pullig O, Weseloh G, Swoboda B. Expression of type VI collagen in normal and osteoarthritic human cartilage. Osteoarthr Cartil, 1999, 7(2): 191-202.

[27] Kubota E, Kubota T, Matsumoto J. Synovial fluid cytokines and proteinases as markers of temporomandibular joint disease. J Oral Maxillofac Surg, 1998, 56(2): 192-198.

[28] Daheshia M, Yao JQ. The interleukin 1β pathway in the pathogenesis of osteoarthritis. J Rheumatol, 2008, 35(12): 2306-2312.

[29] Peters HC, Otto TJ, Enders TJ. The protective role of the pericellular matrix in chondrocyte apoptosis. Tissue Eng Part A, 2011, 17(15/16): 2017-2024.

[30] Zhang S, Yap, Toh WS. Stem cells for temporomandibular joint repair and regeneration. Stem Cell Rev, 2015, 11(5): 728-742.

[31] Toh WS, Foldager CB, Hui JH. Exploiting stem cell-extracellular matrix interactions for cartilage regeneration: a focus on basement membrane molecules. Curr Stem Cell Res Ther, 2016, 11(8): 618-625.

[32] Toh WS, Foldager CB, Pei M. Advances in mesenchymal stem cell-based strategies for cartilage repair and regeneration. Stem Cell Rev, 2014, 10(5): 686-696.