Chondroitin sulfate is a crucial determinant for skeletal muscle development/regeneration and improvement of muscular dystrophies

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38531-38542

  Mikami, Tadahisa ^a   Koyama, Shinji ^a   Yabuta, Yumi ^a   Kitagawa, Hiroshi ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; HYALURONIC ACID; SULFUR COMPOUNDS;

CATABOLIC ENZYMES; CHONDROITIN SULFATES; DEGRADING ENZYMES; DOWN-REGULATION; MOLECULAR REGULATION; MULTINUCLEATED MYOTUBES; MUSCULAR DYSTROPHY; MYOGENIC DIFFERENTIATIONS;

MUSCLE;

CHONDROITIN SULFATE; HYALURONIC ACID; HYALURONIDASE; HYALURONIDASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; ENZYME DEGRADATION; ENZYME MECHANISM; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; MYOBLAST; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION KINETICS; SKELETAL MUSCLE;

EID: 84869078857     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.336925     Document Type: Article

References (44)

1. Sugahara, K., Mikami, T., Uyama, T., Mizuguchi, S., Nomura, K., and Kitagawa, H. (2003) Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13, 612-620 (Pubitemid 37244117)
2. Uyama, T., Kitagawa, H., and Sugahara, K. (2007) in Comprehensive Glycoscience (Kamerling, J. P., ed) Vol. 3, pp. 79-104, Elsevier, Amsterdam
3. Mizuguchi, S., Uyama, T., Kitagawa, H., Nomura, K. H., Dejima, K., Gengyo-Ando, K., Mitani, S., Sugahara, K., and Nomura, K. (2003) Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 423, 443-448 (Pubitemid 36626996)
4. Izumikawa, T., Kanagawa, N., Watamoto, Y., Okada, M., Saeki, M., Sakano, M., Sugahara, K., Sugihara, K., Asano, M., and Kitagawa, H. (2010) Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice. J. Biol. Chem. 285, 12190-12196
5. Rochlin, K., Yu, S., Roy, S., and Baylies, M. K. (2010) Myoblast fusion. When it takes more to make one. Dev. Biol. 341, 66-83
6. Pavlath, G. K. (2010) Spatial and functional restriction of regulatory molecules during mammalian myoblast fusion. Exp. Cell Res. 316, 3067-3072
7. Yamada, S., Okada, Y., Ueno, M., Iwata, S., Deepa, S. S., Nishimura, S., Fujita, M., Van Die, I., Hirabayashi, Y., and Sugahara, K. (2002) Determination of the glycosaminoglycan-protein linkage region oligosaccharide structures of proteoglycans from Drosophila melanogaster and Caenorhabditis elegans. J. Biol. Chem. 277, 31877-31886 (Pubitemid 34975659)
8. Kinoshita, A., and Sugahara, K. (1999) Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high performance liquid chromatography. Application to disaccharide composition analysis and exosequencing of oligosaccharides. Anal. Biochem. 269, 367-378 (Pubitemid 29201038)
9. Yaffe, D., and Saxel, O. (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725-727 (Pubitemid 8239246)
10. Wright, W. E., Sassoon, D. A., and Lin, V. K. (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56, 607-617 (Pubitemid 19065530)
11. Carrino, D. A., Sorrell, J. M., and Caplan, A. I. (1999) Dynamic expression of proteoglycans during chicken skeletal muscle development and maturation. Poult. Sci. 78, 769-777 (Pubitemid 129555221)
12. 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 (Pubitemid 41410261)
13. Uyama, T., Ishida, M., Izumikawa, T., Trybala, E., Tufaro, F., Bergström, T., Sugahara, K., and Kitagawa, H. (2006) Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity. J. Biol. Chem. 281, 38668-38674 (Pubitemid 46041992)
14. Mizumoto, S., Mikami, T., Yasunaga, D., Kobayashi, N., Yamauchi, H., Miyake, A., Itoh, N., Kitagawa, H., and Sugahara, K. (2009) Chondroitin 4-O-sulfotransferase-1 is required for somitic muscle development and motor axon guidance in zebrafish. Biochem. J. 419, 387-399
15. Izumikawa, T., Okuura, Y., Koike, T., Sakoda, N., and Kitagawa, H. (2011) Chondroitin 4-O-sulfotransferase-1 regulates the chain length of chondroitin sulfate in co-operation with chondroitin N-acetylgalactosaminyltransferase-2. Biochem. J. 434, 321-331
16. Csoka, A. B., Frost, G. I., and Stern, R. (2001) The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biol. 20, 499-508 (Pubitemid 33109098)
17. Stern, R., and Jedrzejas, M. J. (2006) Hyaluronidases. Their genomics, structures, and mechanisms of action. Chem. Rev. 106, 818-839
18. Kaneiwa, T., Mizumoto, S., Sugahara, K., and Yamada, S. (2010) Identification of human hyaluronidase-4 as a novel chondroitin sulfate hydrolase that preferentially cleaves the galactosaminidic linkage in the trisulfated tetrasaccharide sequence. Glycobiology 20, 300-309
19. Mikami, T., Yasunaga, D., and Kitagawa, H. (2009) Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J. Biol. Chem. 284, 4494-4499
20. Shen, Y., Tenney, A. P., Busch, S. A., Horn, K. P., Cuascut, F. X., Liu, K., He, Z., Silver, J., and Flanagan, J. G. (2009) PTPσ is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326, 592-596
21. Nadanaka, S., Kinouchi, H., Taniguchi-Morita, K., Tamura, J., and Kitagawa, H. (2011) Down-regulation of chondroitin 4-O-sulfotransferase-1 by Wnt signaling triggers diffusion of Wnt-3a. J. Biol. Chem. 286, 4199-4208
22. Miyata, S., Komatsu, Y., Yoshimura, Y., Taya, C., and Kitagawa, H. (2012) Persistent cortical plasticity by up-regulation of chondroitin 6-sulfation. Nat. Neurosci. 15, 414-422
23. Koike, T., Izumikawa, T., Tamura, J., and Kitagawa, H. (2012) Chondroitin sulfate-E fine-tunes osteoblast differentiation via ERK1/2, Smad3, and Smad1/5/8 signaling by binding to N-cadherin and cadherin-11. Biochem. Biophys. Res. Commun. 420, 523-529
24. Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., Yancopoulos, G. D., and Glass, D. J. (2001) Mediation of IGF-1- induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3, 1009-1013 (Pubitemid 34428746)
25. Wilson, E. M., and Rotwein, P. (2007) Selective control of skeletal muscle differentiation by Akt1. J. Biol. Chem. 282, 5106-5110 (Pubitemid 47093711)
26. Roffe, S., Hagai, Y., Pines, M., and Halevy, O. (2010) Halofuginone inhibits Smad3 phosphorylation via the PI3K/Akt and MAPK/ERK pathways in muscle cells. Effect on myotube fusion. Exp. Cell Res. 316, 1061-1069
27. Sunadome, K., Yamamoto, T., Ebisuya, M., Kondoh, K., Sehara-Fujisawa, A., and Nishida, E. (2011) ERK5 regulates muscle cell fusion through Klf transcription factors. Dev. Cell 20, 192-205
28. Chargé, S. B., and Rudnicki, M. A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238 (Pubitemid 38049880)
29. Wagers, A. J., and Conboy, I. M. (2005) Cellular and molecular signatures of muscle regeneration. Current concepts and controversies in adult myogenesis. Cell 122, 659-667 (Pubitemid 41242632)
30. Tedesco, F. S., Dellavalle, A., Diaz-Manera, J., Messina, G., and Cossu, G. (2010) Repairing skeletal muscle. Regenerative potential of skeletal muscle stem cells. J. Clin. Invest. 120, 11-19
31. Goetsch, S. C., Hawke, T. J., Gallardo, T. D., Richardson, J. A., and Garry, D. J. (2003) Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol. Genomics 14, 261-271 (Pubitemid 37345234)
32. Bulfield, G., Siller, W. G., Wight, P. A., and Moore, K. J. (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. U.S.A. 81, 1189-1192 (Pubitemid 14171480)
33. Hoffman, E. P., Brown, R. H., Jr., and Kunkel, L. M. (1987) Dystrophin. The protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928
34. Coulton, G. R., Morgan, J. E., Partridge, T. A., and Sloper, J. C. (1988) The mdx mouse skeletal muscle myopathy. I. A histological, morphometric and biochemical investigation. Neuropathol. Appl. Neurobiol. 14, 53-70
35. McArdle, A., Edwards, R. H., and Jackson, M. J. (1994) Time course of changes in plasma membrane permeability in the dystrophin-deficient mdx mouse. Muscle Nerve 17, 1378-1384 (Pubitemid 24362809)
36. Harada, H., and Takahashi, M. (2007) CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and -2. J. Biol. Chem. 282, 5597-5607 (Pubitemid 47093756)
37. Gushulak, L., Hemming, R., Martin, D., Seyrantepe, V., Pshezhetsky, A., and Triggs-Raine, B. (2012) Hyaluronidase 1 and β-hexosaminidase have redundant functions in hyaluronan and chondroitin sulfate degradation. J. Biol. Chem. 287, 16689-16697
38. Martin, D. C., Atmuri, V., Hemming, R. J., Farley, J., Mort, J. S., Byers, S., Hombach-Klonisch, S., Csoka, A. B., Stern, R., and Triggs-Raine, B. L. (2008) A mouse model of human mucopolysaccharidosis IX exhibits osteoarthritis. Hum. Mol. Genet. 17, 1904-1915 (Pubitemid 351865839)
39. Grant, B. D., and Donaldson, J. G. (2009) Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608
40. Doherty, K. R., Demonbreun, A. R., Wallace, G. Q., Cave, A., Posey, A. D., Heretis, K., Pytel, P., and McNally, E. M. (2008) The endocytic recycling protein EHD2 interacts with myoferlin to regulate myoblast fusion. J. Biol. Chem. 283, 20252-20260
41. Kim, M. H., Kay, D. I., Rudra, R. T., Chen, B. M., Hsu, N., Izumiya, Y., Martinez, L., Spencer, M. J., Walsh, K., Grinnell, A. D., and Crosbie, R. H. (2011) Myogenic Akt signaling attenuates muscular degeneration, promotes myofiber regeneration and improves muscle function in dystrophin-deficient mdx mice. Hum. Mol. Genet. 20, 1324-1338
42. Zanou, N., Schakman, O., Louis, P., Ruegg, U. T., Dietrich, A., Birnbaumer, L., and Gailly, P. (2012) Trpc1 ion channel modulates phosphatidylinositol 3-kinase/Akt pathway during myoblast differentiation and muscle regeneration. J. Biol. Chem. 287, 14524-14534
43. Bradbury, E. J., Moon, L. D., Popat, R. J., King, V. R., Bennett, G. S., Patel, P. N., Fawcett, J. W., and McMahon, S. B. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (Pubitemid 34406764)
44. Silver, J., and Miller, J. H. (2004) Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146-156 (Pubitemid 38160289)