Insulin-like growth factor 1 signaling regulates cytosolic sialidase Neu2 expression during myoblast differentiation and hypertrophy

FEBS Journal

Volumn 273, Issue 16, 2006, Pages 3709-3721

  Fanzani, Alessandro ^a   Colombo, Francesca ^a   Giuliani, Roberta ^a   Preti, Augusto ^a   Marchesini, Sergio ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

Author keywords

AKT; Gangliosides; IGF 1; Myoblast; Neu2 sialidase

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; SIALIDASE; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOSOL; ENZYME ACTIVATION; GENE OVEREXPRESSION; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; CYTOSOL; ENZYME INHIBITORS; HYPERTROPHY; INSULIN-LIKE GROWTH FACTOR I; MICE; MYOBLASTS; NEURAMINIDASE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 33746728251     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05380.x     Document Type: Article

References (50)

1. Franzini-Armstrong C & Fischman DA (1994) Myology: Basic and Clinical, 2nd edn, Vol. 1. McGraw-Hill, New York.
2. Florini JR, Ewton DZ & Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocrine Rev 17, 481-517.
3. DeVol DL, Rotwein P, Sadow JL, Novakofski J & Bechtel PJ (1990) Activation of insulin-like growth factor gene expression during work-induced skeletal muscle growth. Am J Physiol 259, E89-E95.
4. Coleman ME, DeMayo F, Yin KC, Lee HM, Geske R, Montgomery C & Schwartz RJ (1995) Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 270, 12109-12116.
5. Musarò A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, Barton ER, Sweeney HL & Rosenthal N (2001) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27, 195-200.
6. Rabinovsky ED, Gelir E, Gelir S, Lui H, Kattash M, DeMayo FJ, Shenaq SM & Schwartz RJ (2003) Targeted expression of IGF-1 transgene to skeletal muscle accelerates muscle and motor neuron regeneration. FASEB J 17, 53-55.
7. Rosenthal SM & Cheng ZQ (1995) Opposing early and late effects of insulin-like growth factor I on differentiation and the cell cycle regulatory retinoblastoma protein in skeletal myoblasts. Proc Natl Acad Sci USA 92, 10307-10311.
8. Engert JC, Berglund EB & Rosenthal N (1996) Proliferation precedes differentiation in IGF-I-stimulated myogenesis. J Cell Biol 135, 431-440.
9. Coolican SA, Samuel DS, Ewton DZ, McWade FJ & Florini JR (1997) The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 272, 6653-6662.
10. Lai KM, Gonzalez M, Poueymirou WT, Kline WO, Na E, Zlotchenko E, Stitt TN, Economides AN, Yancopoulos GD & Glass DJ (2004) Conditional activation of akt in adult skeletal muscle induces rapid hypertrophy. Mol Cell Biol 24, 9295-9304.
11. Scott PH, Brunn GJ, Kohn AD, Roth RA & Lawrence JC Jr (1998) Evidence of insulin-stimulated phosphorylation and activation of the mammalian target of rapamycin mediated by a protein kinase B signaling pathway. Proc Natl Acad Sci USA 95, 7772-7777.
12. Nave BT, Ouwens M, Withers DJ, Alessi DR & Shepherd PR (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344, 427-431.
13. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD & Glass DJ (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.
14. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ et al. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
15. Vinogradova MV, Michaud L, Mezentsev AV, Lukong KE, El-Alfy M, Morales CR, Potier M & Pshezhetsky AV (1998) Molecular mechanism of lysosomal sialidase deficiency in galactosialidosis involves its rapid degradation. Biochem J 330, 641-650.
16. Thomas GH (2001) In The Metabolic and Molecular Bases of Inherited Disease (Scriver CR, Beaudet AL, Sly WS & Valle D, eds), Vol. III, 8th edn, pp. 3507-3534. McGraw-Hill, New York.
17. D'Azzo A, Andria G, Strisciuglio P & Galjaard H (2001) In The Metabolic and Molecular Bases of Inherited Disease (Scriver CR, Beaudet AL, Sly WS & Valle D, eds), Vol. III, 8th edn, pp. 3811-3826. McGraw-Hill, New York.
18. Monti E, Bassi MT, Papini N, Riboni M, Manzoni M, Venerando B, Croci G, Preti A, Ballabio A, Tettamanti G et al. (2000) Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem J 349, 343-351.
19. Monti E, Bassi MT, Bresciani R, Civini S, Croci GL, Papini N, Riboni M, Zanchetti G, Ballabio A, Preti A et al. (2004) Molecular cloning and characterization of NEU4, the fourth member of the human sialidase gene family. Genomics 83, 445-453.
20. Miyagi T, Konno K, Emori Y, Kawasaki H, Suzuki K, Yasui A & Tsuik S (1993) Molecular cloning and expression of cDNA encoding rat skeletal muscle cytosolic sialidase. J Biol Chem 268, 26435-26440.
21. Sato K & Miyagi T (1996) Involvement of an endogenous sialidase in skeletal muscle cell differentiation. Biochem Biophys Res Commun 221, 826-830.
22. Fanzani A, Giuliani R, Colombo F, Zizioli D, Presta M, Preti A & Marchesini S (2003) Overexpression of cytosolic sialidase Neu2 induces myoblast differentiation in C2C12 cells. FEBS Lett 547, 183-188.
23. Musarò A & Rosenthal N (1999) Maturation of the myogenic program is induced by postmitotic expression of insulin-like growth factor I. Mol Cell Biol 19, 3115-3124.
24. James PL, Stewart CE & Rotwein P (1996) Insulin-like growth factor binding protein-5 modulates muscle differentiation through an insulin-like growth factor-dependent mechanism. J Cell Biol 133, 683-693.
25. Tringali C, Papini N, Fusi P, Croci G, Borsani G, Preti A, Tortora P, Tettamanti G, Venerando B & Monti E (2004) Properties of recombinant human cytosolic sialidase HsNEU2. The enzyme hydrolyzes monomerically dispersed GM1 ganglioside molecules. J Biol Chem 279, 3169-3179.
26. Lee L, Abe A & Shayman JA (1999) Improved inhibitors of glucosylceramide synthase. J Biol Chem 274, 14662-14669.
27. Jones JI & Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16, 3-34.
28. Baker J, Liu JP, Robertson EJ & Efstratiadis A (1993) A Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75, 73-82.
29. Louvi A, Accili D & Efstratiadis A (1997) A growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev Biol 189, 33-48.
30. Takahashi A, Kureishi Y, Yang J, Luo Z, Guo K, Mukhopadhyay D, Ivashchenko Y, Branellec D & Walsh K (2002) Myogenic Akt signalling regulates blood vessel recruitment during myofiber growth. Mol Cell Biol 22, 4803-4814.
31. Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM & Schiaffino S (2002) A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci USA 99, 9213-9218.
32. von Manteuffel SR, Gingras AC, Ming XF, Sonenberg N & Thomas G (1996) 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc Natl Acad Sci USA 93, 4076-4080.
33. Hara K, Yonezawa K, Kozlowski MT, Sugimoto T, Andrabi K, Weng QP, Kasuga M, Nishimoto I & Avruch J (1997) Regulation of eIF-4E BP1 phosphorylation by mTOR. J Biol Chem 272, 26457-26463.
34. Cross DA, Alessi DR, Cohen P, Andjelkovich M & Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
35. James PL, Jones SB, Busby WH Jr, Clemmons DR & Rotwein P (1993) A highly conserved insulin-like growth factor-binding protein (IGFBP-5) is expressed during myoblast differentiation. J Biol Chem 268, 22305-22312.
36. Gillard BK, Heath JP, Thurmon LT & Marcus DM (1991) Association of glycosphingolipids with intermediate filaments of human umbilical vein endothelial cells. Exp Cell Res 192, 433-444.
37. Schauer R (1985) Sialic acids and their role as biological masks. Trends Biochem Sci 10, 357-360.
38. Tokuyama S, Moriya S, Taniguchi S, Yasui A, Miyazaki J, Orikasa S & Miyagi T (1997) Suppression of pulmonary metastasis in murine B16 melanoma cells by transfection of a sialidase cDNA. Int J Cancer 73, 410-415.
39. Meuillet EJ, Kroes R, Yamamoto H, Warner TG, Ferrari J, Mania-Farnell B, George D, Rebbaa A, Moskal JR & Bremer EG (1999) Sialidase gene transfection enhances epidermal growth factor receptor activity in an epidermoid carcinoma cell line. Cancer Res 59, 234-240.
40. Pilatte Y, Bignon J & Lambrè CR (1993) Sialic acids as important molecules in the regulation of the immune system: pathophysiological implications of sialidases in immunity. Glycobiology 3, 201-218.
41. Gillard BK, Thurmon LT & Marcus DM (1992) Association of glycosphingolipids with intermediate filaments of mesenchymal, epithelial, glial, and muscle cells. Cell Motil Cytoskeleton 21, 255-271.
42. Sonnino S, Ghidoni R, Marchesini S & Tettamanti G (1979) Cytosolic gangliosides: occurrence in calf brain as ganglioside-protein complexes. J Neurochem 33, 117-121.
43. Chan KF & Liu Y (1991) Ganglioside-binding proteins in skeletal and cardiac muscle. Glycobiology 1, 193-203.
44. Suzuki T, Park H, Hollingsworth N, Sternglanz R & Lennarz WJ (2000) PNG1, a yeast gene encoding a highly conserved peptide: N-glycanase. J Cell Biol 149, 1039-1052.
45. Suzuki T, Park H, Kwofie MA & Lennarz WJ (2001) Rad23 provides a link between the Png1 deglycosylating enzyme and the 26S proteasome in yeast. J Biol Chem 276, 21601-21607.
46. Albouz-Abo S, Turton R, Wilson JC & von Itzstein M (2005) An investigation of the activity of recombinant rat skeletal muscle cytosolic sialidase. FEBS Lett 579, 1034-1038.
47. Singleton JR & Feldman EL (2001) Insulin-like growth factor-I in muscle metabolism and myotherapies. Neurobiol Dis 8, 541-554.
48. Suzuki N, Aoki M, Hinuma Y, Takahashi T, Onodera Y, Ishigaki A, Kato M, Warita H, Tateyama M & Itoyama Y (2005) Expression profiling with progression of dystrophic change in dysferlin-deficient mice (SJL). Neurosci Res 52, 47-60.
49. Bittner RE, Anderson LV, Burkhardt E, Bashir R, Vafiadaki E, Ivanova S, Raffelsberger T, Maerk I, Hoger H, Jung M et al. (1999) Dysferlin deletion in SJL mice (SJL-Dysf) defines a natural model for limb girdle muscular dystrophy 2B. Nat Genet 23, 141-142.
50. Folch-Pi J, Lees M & Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497-509.