Pleiotropic effects of sphingolipids in skeletal muscle

Cellular and Molecular Life Sciences

Volumn 65, Issue 23, 2008, Pages 3725-3736

  Bruni, P ^a   Donati, C ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Insulin responsiveness; Muscle regeneration; Skeletal muscle; Sphingolipids; Sphingosine 1 phosphate

Indexed keywords

CERAMIDE; GANGLIOSIDE; INSULIN; SPHINGOLIPID; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE;

CELL DIFFERENTIATION; CELL PROLIFERATION; EXCITATION CONTRACTION COUPLING; LIPID METABOLISM; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE FATIGUE; MUSCLE REGENERATION; PLEIOTROPY; REVIEW; SKELETAL MUSCLE; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; INSULIN; MUSCLE CONTRACTION; MUSCLE, SKELETAL; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; STEM CELLS;

EID: 57349160599     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8236-6     Document Type: Review

References (94)

1. Zeidan, Y. H., Hannun, Y. A. (2007) Translational aspects of sphingolipid metabolism. Trends. Mol. Med. 13, 327-336.
2. Wigmore, P. M., Evans, D. J. (2002) Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. Int. Rev. Cytol. 216, 175-232.
3. Dhawan, J., Rando, T. A. (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell. Biol. 15, 666-673.
4. Le Grand, F., Rudnicki, M. A. (2007) Skeletal muscle satellite cells and adult myogenesis. Curr. Opin. Cell. Biol. 19, 628-33.
5. Lahiri, S., Futerman, A. H. (2007) The metabolism and function of sphingolipids and glycosphingolipids. Cell. Mol. Life. Sci. 64, 2270-2284.
6. Zheng, W., Kollmeyer, J., Symolon, H., Momin, A., Munter, E., Wang, E., Kelly, S., Allegood, J. C., Liu, Y., Peng, Q., Ramaraju, H., Sullards, M. C., Cabot, M., Merrill, A. H. Jr. (2006) Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism and roles in membrane structure, dynamics, signalling and autophagy. Biochim. Biophys. Acta. 1758, 1864-1884.
7. Morales, A., Lee, H., Goñi, F. M., Kolesnick, R., Fernandez-Checa, J. C. (2007) Sphingolipids and cell death. Apoptosis. 12, 923-939.
8. Venable, M. E., Lee, J. Y., Smyth, M. J., Bielawska, A., Obeid, L. M. (1995) Role of ceramide in cellular senescence. J. Biol. Chem. 270, 30701-30708.
9. Hannun, Y. A., Luberto, C. (2000) Ceramide in the eukaryotic stress response. Trends Cell. Biol. 10, 73-80.
10. Futerman, A. H., Stieger, B., Hubbard, A. L. and Pagano, R. E. (1990) Sphingomyelin synthesis in rat liver occurs predominantly at the cis and medial cisternae of the Golgi apparatus. J. Biol. Chem. 265, 8650-8657.
11. Jeckel, D., Karrenbauer, A., Birk, R., Schmidt, R. R. and Wieland, F. (1990) Sphingomyelin is synthesized in the cis Golgi. FEBS Lett. 261, 155-157.
12. Marchesini, N., Hannun, Y. A. (2004) Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem. Cell. Biol. 82, 27-44.
13. Valaperta, R., Chigorno, V., Basso, L., Prinetti, A., Bresciani, R., Preti, A., Miyagi, T., Sonnino, S. (2006) Plasma membrane production of ceramide from ganglioside GM3 in human fibroblasts. FASEB J. 20, 1227-1229.
14. Kitatani, K., Idkowiak-Baldys, J., Hannun, Y. A. (2008) The sphingolipid salvage pathway in ceramide metabolism and signalling. Cell. Signal. 20, 1010-1018.
15. Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P. G., Coso, O. A., Gutkind, S., Spiegel, S. (1996) Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 381, 800-803.
16. Gomez-Brouchet, A., Pchejetski, D., Brizuela, L., Garcia, V., Altié, M. F., Maddelein, M. L., Delisle, M. B., Cuvillier, O. (2007) Critical role for sphingosine kinase-1 in regulating survival of neuroblastoma cells exposed to amyloid-beta peptide. Mol. Pharmacol. 72, 341-349.
17. Mitra, P., Oskeritzian, C. A., Payne, S. G., Beaven, M. A., Milstien, S., Spiegel, S. (2006) Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc. Natl. Acad. Sci. U S A. 103, 16394-16399.
18. Birgbauer E, Chun J. (2006) New developments in the biological functions of lysophospholipids. Cell Mol Life Sci. 63, 2695-2701.
19. Donati C, Bruni P. (2006) Sphingosine 1-phosphate regulates cytoskeleton dynamics: implications in its biological response. Biochim. Biophys. Acta. 1758, 2037-2048.
20. Lee M. J., Thangada S, Claffey K. P, Ancellin N, Liu C. H., Kluk M, Volpi M, Sha'afi RI, Hla T. (1999) Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell. 99, 301-312.
21. Arikawa K, Takuwa N, Yamaguchi H, Sugimoto N, Kitayama J, Nagawa H, Takehara K, Takuwa Y. (2003) Ligand-dependent inhibition of B16 melanoma cell migration and invasion via endogenous S1P2 G protein-coupled receptor. Requirement of inhibition of cellular RAC activity. J. Biol. Chem. 278, 32841-32851.
22. Yoshida, N., Yoshida, S., Koishi, K., Masuda, K., Nabeshima, Y. (1998) Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates 'reserve cells'. J. Cell. Sci. 111, 769-779.
23. Nagata, Y., Kobayashi, H., Umeda, M., Ohta, N., Kawashima, S., Zammit, P. S., Matsuda, R. (2006) Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells. J. Histochem. Cytochem. 54, 375-384.
24. Volonte, D., Liu, Y., Galbiati, F. (2005) The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J. 19, 237-239.
25. Nagata, Y., Partridge, T. A., Matsuda, R., Zammit, P. S. (2006) Entry of muscle satellite cells into the cell cycle requires sphingolipid signalling. J. Cell. Biol. 174, 245-253.
26. Kim, H.. J., Lee, Y., Chang, E. J., Kim, H. M., Hong, S. P., Lee, Z. H., Ryu, J., Kim, H. H. (2007) Suppression of osteoclastogenesis by N,N-dimethyl-D-erythro-sphingosine: a sphingosine kinase inhibition-independent action. Mol. Pharmacol. 72, 418-428.
27. Tatsumi, R., Anderson, J. E., Nevoret, C. J., Halevy, O., Allen, R. E. (1998) HGF/SFis present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol. 194, 114-128.
28. Kästner, S., Elias, M. C., Rivera, A. J., Yablonka-Reuveni, Z. (2000) Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J. Histochem- Cytochem. 48, 1079-1096.
29. Ratajczak, M. Z., Majka, M., Kucia, M., Drukala, J., Pietrzkowski, Z., Peiper, S., Janowska-Wieczorek, A. (2003) Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells. 21, 363-371.
30. Meacci, E., Vasta, V., Donati, C., Farnararo, M., Bruni, P. (1999) Receptor-mediated activation of phospholipase D by sphingosine 1-phosphate in skeletal muscle C2C12 cells. A role for protein kinase C. FEBS Lett. 457, 184-188.
31. Meacci, E., Donati, C., Cencetti, F., Romiti, E., Bruni, P. (2000) Permissive role of protein kinase C alpha but not protein kinase C delta in sphingosine 1-phosphate-induced Rho A activation in C2C12 myoblasts. FEBS Lett. 482, 97-101.
32. Meacci, E., Cencetti, F., Formigli, L., Squecco, R., Donati, C., Tiribilli, B., Quercioli, F., Zecchi Orlandini, S., Francini, F., Bruni, P. (2002) Sphingosine 1-phosphate evokes calcium signals in C2C12 myoblasts via Edg3 and Edg5 receptors. Biochem. J. 362, 349-357.
33. Meacci, E., Cencetti, F., Donati, C., Nuti, F., Farnararo, M., Kohno, T., Igarashi, Y., Bruni, P. (2003) Down-regulation of EDG5/S1P2 during myogenic differentiation results in the specific uncoupling of sphingosine 1-phosphate signalling to phospholipase D. Biochim. Biophys. Acta. 1633, 133-142.
34. Donati, C., Meacci, E., Nuti, F., Becciolini, L., Farnararo, M., Bruni, P. (2005) Sphingosine 1-phosphate regulates myogenic differentiation: a major role for S1P2 receptor. FASEB J. 19, 449-451.
35. Squecco, R., Sassoli, C., Nuti, F., Martinesi, M., Chellini, F., Nosi, D., Zecchi-Orlandini, S., Francini, F., Formigli, L., Meacci, E. (2006) Sphingosine 1-phosphate induces myoblast differentiation through Cx43 protein expression: a role for a gap junction-dependent and -independent function. Mol. Biol. Cell. 17, 4896-4910.
36. Formigli, L., Meacci, E., Sassoli, C., Squecco, R., Nosi, D., Chellini, F., Naro, F., Francini, F., Zecchi-Orlandini, S. (2007) Cytoskeleton/stretch- activated ion channel interaction regulates myogenic differentiation of skeletal myoblasts. J. Cell. Physiol. 211, 296-306.
37. Meacci, E., Nuti, F., Donati, C., Cencetti, F., Farnararo, M., Bruni, P. (2008) Sphingosine kinase activity is required for myogenic differentiation of C2C12 myoblasts. J. Cell. Physiol. 214, 210-220.
38. Olivera, A., Kohama, T., Edsall, L., Nava, V., Cuvillier, O., Poulton, S., Spiegel, S. (1999) Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J. Cell. Biol. 147, 545-558.
39. Donati, C., Nincheri, P., Cencetti, F., Rapizzi, E., Farnararo, M., Bruni, P. (2007) Tumor necrosis factor-alpha exerts promyogenic action in C2C12 myoblasts via sphingosine kinase/S1P2 signaling. FEBS Lett. 581, 4384-4388.
40. Rapizzi, E., Donati, C., Cencetti, F., Nincheri, P., Bruni, P. (2008) Sphingosine 1-phosphate differentially regulates proliferation of C2C12 reserve cells and myoblasts. Mol. Cell. Biochem. 314, 193-199.
41. Donati, C., Cencetti, F., Nincheri, P., Bernacchioni, C., Brunelli, S., Clementi, E., Cossu, G., Bruni, P. (2007) Sphingosine 1-phosphate mediates proliferation and survival of mesoangioblasts. Stem Cells. 25, 1713-1719.
42. Sampaolesi, M., Torrente, Y., Innocenzi, A., Tonlorenzi, R., D'Antona, G., Pellegrino, M. A., Barresi, R., Bresolin, N., De Angelis, M. G., Campbell, K. P., Bottinelli, R., Cossu, G. (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science. 301, 487-492.
43. Sampaolesi, M., Blot, S., D'Antona, G., Granger, N., Tonlorenzi, R., Innocenzi, A., Mognol, P., Thibaud, J. L., Galvez, B. G., Barthélé my, I., Perani, L., Mantero, S., Guttinger, M., Pansarasa, O., Rinaldi, C., Cusella De Angelis, M. G., Torrente, Y., Bordignon, C., Bottinelli, R., Cossu, G. (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature. 444, 574-579.
44. Becciolini, L., Meacci, E., Donati, C., Cencetti, F., Rapizzi, E., Bruni, P. (2006) Sphingosine 1-phosphate inhibits cell migration in C2C12 myoblasts. Biochim. Biophys. Acta. 1761, 43-51.
45. Suzuki, J., Yamazaki, Y., Li, G., Kaziro, Y., Koide, H. (2000) Involvement of Ras and Ral in chemotactic migration of skeletal myoblasts. Mol. Cell. Biol. 20, 4658-4665.
46. Lepley, D., Paik, J. H., Hla, T., Ferrer, F. (2005) The G protein-coupled receptor S1P2 regulates Rho/Rho kinase pathway to inhibit tumor cell migration. Cancer Res. 65, 3788-3795.
47. Bondesen, B. A., Jones, K. A., Glasgow, W. C., Pavlath, G. K. (2007) Inhibition of myoblast migration by prostacyclin is associated with enhanced cell fusion. FASEB J. 21, 3338-3345.
48. Pettus, B. J., Bielawski, J., Porcelli, A. M., Reames, D. L., Johnson, K. R., Morrow, J., Chalfant, C. E., Obeid, L. M., Hannun, Y. A. (2003) The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J. 17, 1411-1421.
49. Ikeda, Y., Ohashi, K., Shibata, R., Pimentel, D. R., Kihara, S., Ouchi, N., Walsh, K. (2008) Cyclooxygenase-2 induction by adiponectin is regulated by a sphingosine kinase-1 dependent mechanism in cardiac myocytes. FEBS Lett. 582, 1147-1150.
50. Johann, A. M., Weigert, A., Eberhardt, W., Kuhn, A. M., Barra, V., Von Knethen, A., Pfeilschifter, J. M., Brüne, B. (2008) Apoptotic cell-derived sphingosine-1-phosphate promotes HuR-dependent cyclooxygenase-2 mRNA stabilization and protein expression. J. Immunol. 180, 1239-1248.
51. Meadows, K. A., Holly, J. M-, Stewart, C. E. (2000) Tumor necrosis factor-alpha-induced apoptosis is associated with suppression of insulin-like growth factor binding protein-5 secretion in differentiating murine skeletal myoblasts. J. Cell. Physiol. 183, 330-337.
52. Mebarek, S., Komati, H., Naro, F., Zeiller, C., Alvisi, M., Lagarde, M., Prigent, A. F., Némoz, G. (2007) Inhibition of de novo ceramide synthesis upregulates phospholipase D and enhances myogenic differentiation. J. Cell. Sci. 120, 407-416.
53. Strle, K., Broussard, S. R., McCusker, R. H., Shen, W. H., Johnson, R. W., Freund, G. G-, Dantzer, R., Kelley, K. W. (2004) Proinflammatory cytokine impairment of insulin-like growth factor I-induced protein synthesis in skeletal muscle myoblasts requires ceramide. Endocrinology. 145, 4592-4602.
54. Hyde, R., Hajduch, E., Powell, D. J., Taylor, P. M., Hundal, H. S. (2005) Ceramide down-regulates System A amino acid transport and protein synthesis in rat skeletal muscle cells. FASEB J. 19, 461-463.
55. Hait, N. C., Oskeritzian, C. A., Paugh, S. W., Milstien, S., Spiegel, S. (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim. Biophys. Acta. 1758, 2016-2026.
56. Leskawa, K. C., Hogan, E. L. (1990) Regulation of glycolipid synthesis during differentiation of clonal murine muscle cells. Mol Cell Biochem. 96, 163-173.
57. Cambron, L. D., Leskawa, K. C. (1994) Glycosphingolipids during skeletal muscle cell differentiation: comparison of normal and fusion-defective myoblasts. Mol. Cell. Biochem. 130, 173-185.
58. Fanzani, A., Giuliani, R., Colombo, F., Zizzoli, D., Presta, M., Preti, A., Marchesini, S. (2003) Overexpression of cytosolic sialidase Neu2 induces myoblast differentiation in C2C12 cells. FEBS Lett. 547, 183-188.
59. Betto, R., Teresi, A., Fachechi-Cassano, G., Salviati, G., Sabbadini, R. A. (1992) Sphingosine inhibits calcium release from sarcoplasmic reticulum membranes. Adv. Exp. Med. Biol. 311, 403-404.
60. Ghosh, N., Sabbadini, R., Chatterjee, S. (1998) Identification, partial purification, and localization of a neutral sphingomyelinase in rabbit skeletal muscle: neutral sphingomyelinase in skeletal muscle. Mol. Cell. Biochem. 189, 161-168.
61. Sabbadini R, McNutt W, Jenkins G, Betto R, Salviati G. (1993) Sphingosine is endogenous to cardiac and skeletal muscle. Biochem. Biophys. Res. Commun. 193, 752-728.
62. Sabbadini, R. A., Danieli-Betto, D., Betto, R. (1999) The role of sphingolipids in the control of skeletal muscle function: a review. Ital. J. Neurol. Sci. 20, 423-430.
63. Bencini, C., Squecco, R., Piperio, C., Formigli, L., Meacci, E., Nosi, D., Tiribilli, B., Vassalli, M., Quercioli, F., Bruni, P., Zecchi Orlandini, S., Francini, F. (2003) Effects of sphingosine 1-phosphate on excitation- contraction coupling in mammalian skeletal muscle. J. Muscle Res. Cell. Motil. 24, 539-554.
64. Danieli-Betto, D., Germinario, E., Esposito, A., Megighian, A., Midrio, M., Ravara, B., Damiani, E., Libera, L. D., Sabbadini, R. A., Betto, R. (2005) Sphingosine 1-phosphate protects mouse extensor digitorum longus skeletal muscle during fatigue. Am. J. Physiol Cell. Physiol. 288, C1367-C1373.
65. Meacci E, Cencetti F, Donati C, Nuti F, Becciolini L, Bruni P. (2004) Sphingosine kinase activity is required for sphingosine-mediated phospholipase D activation in C2C12 myoblasts. Biochem. J. 381, 655-663.
66. Zanin, M., Germinario, E., Dalla Libera, L., Sandonà, D., Sabbadini, R. A., Betto, R., Danieli-Betto, D. (2008) Trophic action of sphingosine 1-phosphate in denervated rat soleus muscle. Am. J. Physiol. Cell. Physiol. 294, C36-C46.
67. Dobrzyń, A., Zendzian-Piotrowska, M., Gorski, J. (2004) Effect of endurance training on the sphingomyelin-signalling pathway activity in the skeletal muscles of the rat. J. Physiol. Pharmacol. 55, 305-313.
68. Ohlson, L. O., Larsson, B., Svärdsudd, K., Welin, L., Eriksson, H., Wilhelmsen, L., Björntorp, P., Tibblin, G. (1985) The influence of body fat distribution on the incidence of diabetes mellitus. 13.5 years of follow-up of the participants in the study of men born in 1913. Diabetes. 34, 1055-1058.
69. McGarry, J. D. (2002) Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes. 51, 7-18.
70. Turinsky, J., O'Sullivan, D. M., Bayly, B. P. (1990) 1,2-Diacylglycerol and ceramide levels in insulin-resistant tissues of the rat in vivo. J. Biol. Chem. 265, 16880-16885.
71. Gorska, M., Dobrzyn, A., Zendzian-Piotrowska, M., Gorski, J. (2004) Effect of streptozotocin-diabetes on the functioning of the sphingomyelin- signalling pathway in skeletal muscles of the rat. Horm. Metab. Res. 36, 14-21.
72. Adams, J. M.2nd, Pratipanawatr, T., Berria, R., Wang, E., DeFronzo, R. A., Sullards, M. C., Mandarino, L. J. (2004) Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes. 53, 25-31.
73. Straczkowski M, Kowalska I, Nikolajuk A, Dzienis-Straczkowska S, Kinalska I, Baranowski M, Zendzian-Piotrowska M, Brzezinska Z, Gorski J. (2004) Relationship between insulin sensitivity and sphingomyelin signaling pathway in human skeletal muscle. Diabetes. 53, 1215-1221.
74. Straczkowski, M., Kowalska, I., Baranowski, M., Nikolajuk, A., Otziomek, E., Zabielski, P., Adamska, A., Blachnio, A., Gorski, J., Gorska, M. (2007) Increased skeletal muscle ceramide level in men at risk of developing type 2 diabetes. Diabetologia. 50, 2366-2373.
75. Hajduch, E., Balendran, A., Batty, I. H., Litherland, G. J., Blair, A. S., Downes, C. P., Hundal, H. S. (2001) Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells. Diabetologia. 44, 173-183.
76. Zhou, H., Summers, S. A., Birnbaum, M. J., Pittman, R. N. (1998) Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem. 273, 16568-16575.
77. Dobrzyń, A., Górski, J. (2002) Effect of acute exercise on the content of free sphinganine and sphingosine in different skeletal muscle types of the rat. Horm. Metab. Res. 34, 523-529.
78. Helge, J. W., Dobrzyn, A., Saltin, B., Gorski, J. (2004) Exercise and training effects on ceramide metabolismin human skeletal muscle. Exp. Physiol. 89, 119-127.
79. Planavila, A., Alegret, M., Snchez, R. M., Rodríguez-Calvo, R., Laguna, J. C., Vázquez-Carrera, M. (2005) Increased Akt protein expression is associated with decreased ceramide content in skeletal muscle of troglitazone-treated mice. Biochem. Pharmacol. 69, 1195-1204.
80. Summers, S. A.(2006) Ceramides in insulin resistance and lipotoxicity. Prog. Lipid Res. 45, 42-72.
81. Dobrowsky, R. T., Kamibayashi, C., Mumby, M. C., Hannun, Y. A. (1993) Ceramide activates heterotrimeric protein phosphatase 2A. J. Biol. Chem. 268, 15523-15530.
82. Stratford, S., Hoehn, K. L., Liu, F., Summers, S. A. (2004) Regulation of insulin action by ceramide: dual mechanisms linking ceramide accumulation to the inhibition of Akt/protein kinase B. J. Biol. Chem. 279, 36608-36615.
83. Schmitz-Peiffer, C., Craig, D. L., Biden, T. J. (1999) Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J. Biol. Chem. 274, 24202-24210.
84. Chavez, J. A., Summers, S. A. (2003) Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch. Biochem. Biophys. 419, 101-109.
85. Pickersgill, L., Litherland, G. J., Greenberg, A. S., Walker, M., Yeaman, S. J. (2007) Key role for ceramides in mediating insulin resistance in human muscle cells. J. Biol. Chem. 282, 12583-12589.
86. Holland, W. L., Brozinick, J. T., Wang, L. P., Hawkins, E. D., Sargent, K. M., Liu, Y., Narra, K., Hoehn, K. L., Knotts, T. A., Siesky, A., Nelson, D. H., Karathanasis, S. K., Fontenot, G. K., Birnbaum, M. J., Summers, S. A. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell. Metab. 5, 167-179.
87. Turpin, S. M., Lancaster, G. I., Darby, I., Febbraio, M. A., Watt, M. J. (2006) Apoptosis in skeletal muscle myotubes is induced by ceramides and is positively related to insulin resistance. Am. J. Physiol. Endocrinol. Metab. 291, E1341-E1350.
88. Ma, M. M., Chen, J. L., Wang, G. G., Wang, H., Lu, Y., Li, J. F., Yi, J., Yuan, Y. J., Zhang, Q. W., Mi, J., Wang, L.Sh., Duan, H. F., Wu, C. T. (2007) Sphingosine kinase 1 participates in insulin signalling and regulates glucose metabolism and homeostasis in KK/Ay diabetic mice. Diabetologia. 50, 891-900.
89. Taha, T. A., Kitatani, K., El-Alwani, M., Bielawski, J., Hannun, Y. A., Obeid, L. M. (2006) Loss of sphingosine kinase-1 activates the intrinsic pathway of programmed cell death: modulation of sphingolipid levels and the induction of apoptosis. FASEB J. 20, 482-484.
90. Yamashita, T., Hashiramoto, A., Haluzik, M., Mizukami, H., Beck, S., Norton, A., Kono, M., Tsuji, S., Daniotti, J. L., Werth, N., Sandhoff, R., Sandhoff, K., Proia, R. L. (2003) Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc. Natl. Acad. Sci. U S A. 100, 3445-3449.
91. Zhao, H., Przybylska, M., Wu, I. H., Zhang, J., Siegel, C., Komarnitsky, S., Yew, N. S., Cheng, S. H. (2007) Inhibiting glycosphingolipid synthesis improves glycemic control and insulin sensitivity in animal models of type 2 diabetes. Diabetes. 56, 1210-1218.
92. Safdar A, Yardley N. J., Snow R, Melov S, Tarnopolsky M. A. (2008) Global and targeted gene expression and protein content in skeletal muscle of young men following short-term creatine monohydrate supplementation. Physiol Genomics. 32, 219-228.
93. Vandenberghe, K., Goris, M., Van Hecke, P., Van Leemputte, M., Vangerven, L., Hespel, P. (1997) Long-term creatine intake is beneficial to muscle performance during resistance training. J. Appl. Physiol. 83, 2055-2263.
94. Volek, J. S., Duncan, N. D., Mazzetti, S. A., Staron, R. S., Putukian, M., Gómez, A. L., Pearson, D. R., Fink, W. J., Kraemer, W. J. (1999) Performance and muscle fiber adaptations to creatine supplementation and heavy resistance training. Med. Sci. Sports. Exerc. 31, 1147-1156