Matrix disruptions, growth, and degradation of cartilage with impaired sulfation

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 22030-22042

  Mertz, Edward L ^a   Facchini, Marcella ^b   Pham, Anna T ^a   Gualeni, Benedetta ^b   De Leonardis, Fabio ^b   Rossi, Antonio ^b   Forlino, Antonella ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICULAR CARTILAGES; ARTICULAR SURFACES; BONE DEVELOPMENT; CARTILAGE GROWTH; CHONDROCYTES; CHONDROITIN; GLYCOSAMINOGLYCANS; GROWTH PLATE; HIGH DEFINITION; HYPERSPECTRAL IMAGING; IN-VIVO; NON-COLLAGENOUS PROTEINS; PHYSIOLOGICAL CONDITION; PROTEOGLYCAN DEPLETION; PROXIMAL FEMUR; SPATIAL RESOLUTION; SYNTHESIS RATE; UNDERLYING MECHANISM; WILD TYPES;

BONE; COLLAGEN; DEGRADATION; MAMMALS;

CARTILAGE;

CHONDROITIN; COLLAGEN; PROTEOGLYCAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARBOHYDRATE SYNTHESIS; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL DISRUPTION; CELL ENLARGEMENT; CELL GROWTH; CHONDRODYSPLASIA; COLLAGEN DEGRADATION; CONTROLLED STUDY; DIASTROPHIC DYSPLASIA; DISEASE ACTIVITY; DISEASE PREDISPOSITION; EPIPHYSEAL CARTILAGE; EXTRACELLULAR MATRIX; FEMUR; GENE MUTATION; LEG LENGTHENING; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEPLETION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SULFATION;

ANIMALS; ANION TRANSPORT PROTEINS; CARTILAGE; CHONDROCYTES; COLLAGEN; EXTRACELLULAR MATRIX; FEMUR; GLYCOSAMINOGLYCANS; GROWTH PLATE; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, TRANSGENIC; MODELS, STATISTICAL; MUTATION; PHENOTYPE; SPECTROPHOTOMETRY, INFRARED; SULFATES; SULFUR;

EID: 84862702877     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M110.116467     Document Type: Article

References (73)

1. Hästbacka, J., de la Chapelle, A., Mahtani, M. M., Clines, G., Reeve-Daly, M. P., Daly, M., Hamilton, B. A., Kusumi, K., Trivedi, B., and Weaver, A. (1994) The diastrophic dysplasia gene encodes a novel sulfate transporter. Positional cloning by fine-structure linkage disequilibrium mapping. Cell 78, 1073-1087
2. Faiyaz ul Haque, M., King, L. M., Krakow, D., Cantor, R. M., Rusiniak, M. E., Swank, R. T., Superti-Furga, A., Haque, S., Abbas, H., Ahmad, W., Ahmad, M., and Cohn, D. H. (1998) Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse. Nat. Genet. 20, 157-162
3. Thiele, H., Sakano, M., Kitagawa, H., Sugahara, K., Rajab, A., Höhne, W., Ritter, H., Leschik, G., Nürnberg, P., and Mundlos, S. (2004) Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc. Natl. Acad. Sci. U.S.A. 101, 10155-10160
4. Hermanns, P., Unger, S., Rossi, A., Perez-Aytes, A., Cortina, H., Bonafé, L., Boccone, L., Setzu, V., Dutoit, M., Sangiorgi, L., Pecora, F., Reicherter, K., Nishimura, G., Spranger, J., Zabel, B., and Superti-Furga, A. (2008) Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis. Am. J. Hum. Genet. 82, 1368-1374
5. Orkin, R. W., Williams, B. R., Cranley, R. E., Poppke, D. C., and Brown, K. S. (1977) Defects in the cartilaginous growth plates of brachymorphic mice. J. Cell Biol. 73, 287-299
6. Schwartz, N. B., Lyle, S., Ozeran, J. D., Li, H., Deyrup, A., Ng, K., and Westley, J. (1998) Sulfate activation and transport in mammals. System components and mechanisms. Chem. Biol. Interact. 109, 143-151
7. Bullock, S. L., Fletcher, J. M., Beddington, R. S., and Wilson, V. A. (1998) Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 12, 1894-1906
8. Forlino, A., Piazza, R., Tiveron, C., Della Torre, S., Tatangelo, L., Bonafè, L., Gualeni, B., Romano, A., Pecora, F., Superti-Furga, A., Cetta, G., and Rossi, A. (2005) A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse. Morphological and biochemical characterization of the resulting chondrodysplasia phenotype. Hum. Mol. Genet. 14, 859-871
9. Klüppel, M., Wight, T. N., Chan, C., Hinek, A., and Wrana, J. L. (2005) Maintenance of chondroitin sulfation balance by chondroitin-4- sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132, 3989-4003
10. Frederick, J. P., Tafari, A. T., Wu, S. M., Megosh, L. C., Chiou, S. T., Irving, R. P., and York, J. D. (2008) A role for a lithium-inhibited Golgi nucleotidase in skeletal development and sulfation. Proc. Natl. Acad. Sci. U.S.A. 105, 11605-11612
11. Walker, B. A., Scott, C. I., Hall, J. G., Murdoch, J. L., and McKusick, V. A. (1972) Diastrophic dwarfism. Medicine 51, 41-59
12. Horton, W. A., Rimoin, D. L., Lachman, R. S., Skovby, F., Hollister, D. W., Spranger, J., Scott, C. I., and Hall, J. G. (1978) The phenotypic variability of diastrophic dysplasia. J. Pediatr. 93, 609-613
13. Mäkitie, O., and Kaitila, I. (1997) Growth in diastrophic dysplasia. J. Pediatr. 130, 641-646
14. Rossi, A., Kaitila, I., Wilcox, W. R., Rimoin, D. L., Steinmann, B., Cetta, G., and Superti-Furga, A. (1998) Proteoglycan sulfation in cartilage and cell cultures from patients with sulfate transporter chondrodysplasias. Relationship to clinical severity and indications on the role of intracellular sulfate production. Matrix Biol. 17, 361-369
15. Lamb, R., Thomson, W., British Society of Paediatric and Adolescent Rheumatology, Ogilvie, E. M., and Donn, R. (2007) Positive association of SLC26A2 gene polymorphisms with susceptibility to systemic-onset juve- nile idiopathic arthritis. Arthritis Rheum. 56, 1286-1291
16. Forlino, A., Gualeni, B., Pecora, F., Torre, S. D., Piazza, R., Tiveron, C., Tatangelo, L., Superti-Furga, A., Cetta, G., and Rossi, A. (2006) Insights from a transgenic mouse model on the role of SLC26A2 in health and disease. Novartis Found. Symp. 273, 193-206; discussion 206-212, 261-264
17. Gualeni, B., Rossi, A., Geoffrey, V., Marty-Morieux, C., Forlino, A., Pecora, F., Houillier, P., and de Vernejoul, M. (2007) Morphological and biochemical characterization of bone phenotype in a chondrodysplasia mouse model. Calcif. Tissue Int. 80, S77-S78
18. Superti-Furga, A. (2002) in Connective Tissue and Its Heritable Disorders (Royce, P. M., and Steinmann, B., eds) 2nd Ed., pp. 939-960, Wiley-Liss, New York
19. Potter, K., Kidder, L. H., Levin, I. W., Lewis, E. N., and Spencer, R. G. (2001) Imaging of collagen and proteoglycan in cartilage sections using Fourier transform infrared spectral imaging. Arthritis Rheum. 44, 846-855
20. Camacho, N. P., West, P., Torzilli, P. A., and Mendelsohn, R. (2001) FTIR microscopic imaging of collagen and proteoglycan in bovine cartilage. Biopolymers 62, 1-8
21. Boskey, A., and Pleshko Camacho, N. (2007) FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials 28, 2465-2478
22. Rieppo, J., Hyttinen, M. M., Halmesmaki, E., Ruotsalainen, H., Vasara, A., Kiviranta, I., Jurvelin, J. S., and Helminen, H. J. (2009) Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. Osteoarthritis Cartilage 17, 448-455
23. Yin, J., and Xia, Y. (2010) Macromolecular concentrations in bovine nasal cartilage by Fourier transform infrared imaging and principal component regression. Appl. Spectrosc. 64, 1199-1208
24. Dukor, R. K. (2002) in Applications of Vibrational Spectroscopy in Life, Pharmaceutical and Natural Sciences (Chalmers, J. M., and Griffiths, P. R., eds) pp. 3335-3361, John Wiley & Sons, New York
25. Mertz, E. L., and Sullivan, J. V. (2008) Flow-through, thermal expansion-compensated cell for light spectroscopy. United States patent 7,355,697
26. Mertz, E. L., and Leikin, S. (2004) Interactions of inorganic phosphate and sulfate anions with collagen. Biochemistry 43, 14901-14912
27. 13C magnetic resonance. J. Biol. Chem. 252, 3617-3625
28. Mourao, P. A., and Dietrich, C. P. (1979) Chondroitin sulfates of the epiphyseal cartilages of different mammals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 62, 115-117
29. Wikstrom, B., Engfeldt, B., Heinegård, D., and Hjerpe, A. (1985) Proteoglycans and glycosaminoglycans in cartilage from the brachymorphic (bm/bm) mouse. Collagen Relat. Res. 5, 193-204
30. Rosenberg, L. C., Tang, L. H., Choi, H. U., Pal, S., Johnson, T. L., Poole, A. R., Roughley, P. J., Reiner, A., and Pidoux, I. (1983) in Limb development and regeneration (Kelley, R. O., Goetinck, P. F., and MacCabe, J. A., eds) pp. 67-84, Alan R. Liss, New York
31. Hiraoka, S., Furuichi, T., Nishimura, G., Shibata, S., Yanagishita, M., Rimoin, D. L., Superti-Furga, A., Nikkels, P. G., Ogawa, M., Katsuyama, K., Toyoda, H., Kinoshita-Toyoda, A., Ishida, N., Isono, K., Sanai, Y., Cohn, D. H., Koseki, H., and Ikegawa, S. (2007) Nucleotide-sugar transporter SLC35D1 is critical to chondroitin sulfate synthesis in cartilage and skeletal development in mouse and human. Nat. Med. 13, 1363-1367
32. Stanescu, V., Stanescu, R., and Maroteaux, P. (1984) Pathogenic mechanisms in osteochrondodysplasias. J. Bone Jt. Surg. 66, 817-836
33. Fraser, R. D. (1958) Interpretation of infrared dichoism in axially oriented polymers. J. Chem. Phys. 28, 1113-1115
34. Maroudas, A., and Evans, H. (1974) Sulfide diffusion and incorporation into human articularcartilage. Biochim. Biophys. Acta 338, 265-279
35. Rossi, A., Bonaventure, J., Delezoide, A. L., Superti-Furga, A., and Cetta, G. (1997) Undersulfation of cartilage proteoglycans ex vivo and increased contribution of amino acid sulfur to sulfation in vitro in McAlister dysplasia/ atelosteogenesis type 2. Eur. J. Biochem. 248, 741-747
36. Pecora, F., Gualeni, B., Forlino, A., Superti-Furga, A., Tenni, R., Cetta, G., and Rossi, A. (2006) In vivo contribution of amino acid sulfur to cartilage proteoglycan sulfation. Biochem. J. 398, 509-514
37. Ooira, A., Kimata, K., Suzuki, S., Takata, K., and Suzuki, I. (1974) A correlation between synthetic activities for matrix macromolecules and specific stages of cyto-differentiation in developing cartilage. J. Biol. Chem. 249, 1637-1645
38. Dziewiatkowski, D. D. (1951) Radioautographic visualization of sulfur-35 disposition in the articular cartilage and bone of suckling rats following injection of labeled sodium sulfate. J. Exp. Med. 93, 451-458
39. 35S) metabolism in the articular cartilage and bone of suckling rats. J. Exp. Med. 95, 489-496
40. 35S in cartilage, bone, and dentine of young rats and the effect of hyaluronidase in vitro. Can. J. Biochem. Physiol. 32, 161-169
41. Hunziker, E. B., and Schenk, R. K. (1989) Physiological mechanisms adopted by chrondocytes in regulating longitudinal bone growth in rats. J. Physiol. 414, 55-71
42. Wilsman, N. J., Farnum, C. E., Leiferman, E. M., Fry, M., and Barreto, C. (1996) Differential growth by growth plates as a function of multiple parameters of chondrocytic kinetics. J. Orthop. Res. 14, 927-936
43. Buckwalter, J. A., Mower, D., Ungar, R., Schaeffer, J., and Ginsberg, B. (1986) Morphometric analysis of chrondrocyte hypertrophy. J. Bone Jt. Surg. Am. 68A, 243-255
44. Bayliss, M. T., Osborne, D., Woodhouse, S., and Davidson, C. (1999) Sulfation of chondroitin sulfate in human articular cartilage. The effect of age, topographical position, and zone of cartilage on tissue composition. J. Biol. Chem. 274, 15892-15900
45. Marcelino, J., Carpten, J. D., Suwairi, W. M., Gutierrez, O. M., Schwartz, S., Robbins, C., Sood, R., Makalowska, I., Baxevanis, A., Johnstone, B., Laxer, R. M., Zemel, L., Kim, C. A., Herd, J. K., Ihle, J., Williams, C., Johnson, M., Raman, V., Alonso, L. G., Brunoni, D., Gerstein, A., Papadopoulos, N., Bahabri, S. A., Trent, J. M., and Warman, M. L. (1999) CACP, encoding a secreted proteoglycan, is mutated in camptodactyly arthropathy- coxa vara-pericarditis syndrome. Nat. Genet. 23, 319-322
46. Scheck, M., Parker, J., and Daentl, D. (1978) Hyaline cartilage changes in diastrophic dwarfism. Virchows Arch. A Pathol. Anat. Histopathol. 378, 347-359
47. Shapiro, F. (1992) Light and electron microscopic abnormalities in diastrophic dysplasia growth cartilage. Calcif. Tissue Int. 51, 324-331
48. Diab, M., Wu, J. J., Shapiro, F., and Eyre, D. (1994) Abnormality of type IX collagen in a patient with diastrophic dysplasia. Am. J. Med. Genet. 49, 402-409
49. Stanescu, V., Do, T. P., Chaminade, F., Maroteaux, P., and Stanescu, R. (1994) Noncollagenous protein screening in the human chondrodysplasias. Link proteins, cartilage oligomeric matrix protein (COMP), and fibromodulin. Am. J. Med. Genet. 51, 22-28
50. Ghadially, F. N. (1983) Fine Structure of Synovial Joints, Butterworths, London
51. Cortes, M., Baria, A. T., and Schwartz, N. B. (2009) Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate. Development 136, 1697-1706
52. Sohaskey, M. L., Yu, J., Diaz, M. A., Plaas, A. H., and Harland, R. M. (2008) JAWS coordinates chondrogenesis and synovial joint positioning. Development 135, 2215-2220
53. Gualeni, B., Facchini, M., De Leonardis, F., Tenni, R., Cetta, G., Viola, M., Passi, A., Superti-Furga, A., Forlino, A., and Rossi, A. (2010) Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signaling. Matrix Biol. 29, 453-460
54. Kobayashi, T., Soegiarto, D. W., Yang, Y., Lanske, B., Schipani, E., McMahon, A. P., and Kronenberg, H. M. (2005) Indian hedgehog stimulates periarticular chondrocyte differentiation to regulate growth plate length independently of PTHrP. J. Clin. Invest. 115, 1734-1742
55. Chen, X., Macica, C. M., Nasiri, A., and Broadus, A. E. (2008) Regulation of articular chondrocyte proliferation and differentiation by indian hedgehog and parathyroid hormone-related protein in mice. Arthritis Rheum. 58, 3788-3797
56. Serizawa, S., Nagai, T., Ito, M., and Sato, Y. (1990) Cholesterol sulfate levels in the hair and nails of patients with recessive X-linked ichthyosis. Clin. Exp. Dermatol. 15, 13-15
57. Cohen, M. M. (2003) The hedgehog signaling network. Am. J. Med. Genet. A 123, 5-28
58. Strott, C. A., and Higashi, Y. (2003) Cholesterol sulfate in human physiology. What's it all about? J. Lipid Res. 44, 1268-1278
59. Ai, X., Do, A. T., Lozynska, O., Kusche-Gullberg, M., Lindahl, U., and Emerson, C. P., Jr. (2003) QSulf1 remodels the 6-O-sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162, 341-351
60. Koziel, L., Kunath, M., Kelly, O. G., and Vortkamp, A. (2004) Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev. Cell 6, 801-813
61. Mohammadi, M., Olsen, S. K., and Ibrahimi, O. A. (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16, 107-137
62. Galante, L. L., and Schwarzbauer, J. E. (2007) Requirements for sulfate transport and the diastrophic dysplasia sulfate transporter in fibronectin matrix assembly. J. Cell Biol. 179, 999-1009
63. Arrington, C. B., and Yost, H. J. (2009) Extra-embryonic syndecan 2 regulates organ primordia migration and fibrillogenesis throughout the zebrafish embryo. Development 136, 3143-3152
64. Yamauchi, S., Hirahara, Y., Usui, H., Takeda, Y., Hoshino, M., Fukuta, M., Kimura, J. H., and Habuchi, O. (1999) Purification and characterization of chondroitin 4-sulfotransferase from the culture medium of a rat chondrosarcoma cell line. J. Biol. Chem. 274, 2456-2463
65. Orellana, A., Hirschberg, C. B., Wei, Z., Swiedler, S. J., and Ishihara, M. (1994) Molecular cloning and expression of a glycosaminoglycan N-acetylglucosaminyl N-deacetylase/N-sulfotransferase from a heparin-producing cell line. J. Biol. Chem. 269, 2270-2276
66. Habuchi, H., Habuchi, O., and Kimata, K. (1995) Purification and characterization of heparan sulfate 6-sulfotransferase from the culture medium of Chinese hamster ovary cells. J. Biol. Chem. 270, 4172-4179
67. Myette, J. R., Shriver, Z., Liu, J., Venkataraman, G., Rosenberg, R., and Sasisekharan, R. (2002) Expression in Escherichia coli, purification and kinetic characterization of human heparan sulfate 3-O-sulfotransferase-1. Biochem. Biophys. Res. Commun. 290, 1206-1213
68. Xu, D., Song, D., Pedersen, L. C., and Liu, J. (2007) Mutational study of heparan sulfate 2-O-sulfotransferase and chondroitin sulfate 2-O-sulfotransferase. J. Biol. Chem. 282, 8356-8367
69. Kester, M. H., Kaptein, E., Roest, T. J., van Dijk, C. H., Tibboel, D., Meinl, W., Glatt, H., Coughtrie, M. W., and Visser, T. J. (2003) Characterization of rat iodothyronine sulfotransferases. Am. J. Physiol. Endocrinol. Metab. 285, E592-E598
70. Carlsson, P., Presto, J., Spillmann, D., Lindahl, U., and Kjellén, L. (2008) Heparin/heparan sulfate biosynthesis. Processive formation of N-sulfated domains. J. Biol. Chem. 283, 20008-20014
71. Tsang, K. Y., Chan, D., Cheslett, D., Chan, W. C., So, C. L., Melhado, I. G., Chan, T. W. Y., Kwan, K. M., Hunziker, E. B., Yamada, Y., Bateman, J. F., Cheung, K. M., and Cheah, K. S. E. (2007) Surviving endoplasmic reticulum stress is coupled to altered chrondrocyte differentiation and function. PLoS Biol. 5, 568-585
72. Rajpar, M. H., McDermott, B., Kung, L., Eardley, R., Knowles, L., Heeran, M., Thornton, D. J., Wilson, R., Bateman, J. F., Poulsom, R., Arvan, P., Kadler, K. E., Briggs, M. D., and Boot-Handford, R. P. (2009) Targeted induction of endoplasmic reticulum stress induces cartilage pathology. PLoS Genet. 5, e1000691
73. Tsang, K. Y., Chan, D., Bateman, J. F., and Cheah, K. S. (2010) In vivo cellular adaptation to ER stress. Survival strategies with double-edged consequences. J. Cell Sci. 123, 2145-2154