There is more to a lipid than just being a fat: Sphingolipid-Guided differentiation of oligodendroglial lineage from embryonic stem cells

Neurochemical Research

Volumn 36, Issue 9, 2011, Pages 1601-1611

  Bieberich, Erhard ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Apoptosis; Ceramide; Differentiation; Embryonic stem cells; Oligodendrocyte precursors; Sphingosine 1 phosphate

Indexed keywords

CELL MARKER; CERAMIDE; CERAMIDE DERIVATIVE; FINGOLIMOD; N OLEOYL SERINOL; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN O4; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CERAMIDES; HUMANS; IMMUNOSUPPRESSIVE AGENTS; LYSOPHOSPHOLIPIDS; MICE; MOLECULAR STRUCTURE; OLIGODENDROGLIA; PROPYLENE GLYCOLS; RECEPTORS, LYSOSPHINGOLIPID; SPHINGOLIPIDS; SPHINGOSINE; STEM CELLS;

CITRUS MAXIMA;

EID: 80755163629     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-010-0338-5     Document Type: Article

References (122)

1. Strathmann FG, Wang X, Mayer-Proschel M (2007) Identification of two novel glial-restricted cell populations in the embryonic telencephalon arising from unique origins. BMC Dev Biol 7:33
2. Bjorklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O (2002) Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA 99:2344-2349 (Pubitemid 34169063)
3. Bieberich E, Silva J, Wang G, Krishnamurthy K, Condie BG (2004) Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol 167:723-734 (Pubitemid 39565152)
4. Brustle O, Jones KN, Learish RD, Karram K, Choudhary K, Wiestler OD, Duncan ID, McKay RD (1999) Embryonic stem cell-derived glial precursors: A source of myelinating transplants. Science 285:754-756
5. Duncan ID (2005) Oligodendrocytes and stem cell transplantation: Their potential in the treatment of leukoencephalopathies. J Inherit Metab Dis 28:357-368 (Pubitemid 40723869)
6. Perez-Bouza A, Glaser T, Brustle O (2005) ES cell-derived glial precursors contribute to remyelination in acutely demyelinated spinal cord lesions. Brain Pathol 15:208-216 (Pubitemid 41161176)
7. Hu BY, Du ZW, Zhang SC (2009) Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc 4:1614-1622
8. Kiel ME, Chen CP, Sadowski D, McKinnon RD (2008) Stem cell-derived therapeutic myelin repair requires 7% cell replacement. Stem Cells 26:2229-2236
9. Maire CL, Buchet D, Kerninon C, Deboux C, Baron-Van Evercooren A, Nait-Oumesmar B (2009) Directing human neural stem/precursor cells into oligodendrocytes by overexpression of Olig2 transcription factor. J Neurosci Res 87:3438-3446
10. Goldman JE, Hirano M, Yu RK, Seyfried TN (1984) GD3 ganglioside is a glycolipid characteristic of immature neuroectodermal cells. J Neuroimmunol 7:179-192
11. Yu RK (1994) Development regulation of ganglioside metabolism. Prog Brain Res 101:31-44 (Pubitemid 24084736)
12. Suetake K, Liour SS, Tencomnao T, Yu RK (2003) Expression of gangliosides in an immortalized neural progenitor/stem cell line. J Neurosci Res 74:769-776 (Pubitemid 37475457)
13. Cochran FB, Ledeen RW, Yu RK (1982) Gangliosides and proteins in developing chicken brain myelin. Brain Res 282:27-32 (Pubitemid 13151074)
14. Yu RK, Macala LJ, Taki T, Weinfield HM, Yu FS (1988) Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem 50:1825-1829
15. Yu RK, Macala LJ, Farooq M, Sbaschnig-Agler M, Norton WT, Ledeen RW (1989) Ganglioside and lipid composition of bulkisolated rat and bovine oligodendroglia. J Neurosci Res 23:136-141 (Pubitemid 19178874)
16. Zeng G, Gao L, Freischutz B, Tokuda A, Yu RK (1998) Developmental expression of rat brain GD3-and GT3-synthases. Ann N Y Acad Sci 845:430
17. Ngamukote S, Yanagisawa M, Ariga T, Ando S, Yu RK (2007) Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem 103:2327-2341 (Pubitemid 350173557)
18. Liour SS, Yu RK (2002) Differential effects of three inhibitors of glycosphingolipid biosynthesis on neuronal differentiation of embryonal carcinoma stem cells. Neurochem Res 27:1507-1512 (Pubitemid 36014162)
19. Nakatani Y, Yanagisawa M, Suzuki Y, Yu RK (2010) Characterization of GD3 ganglioside as a novel biomarker of mouse neural stem cells. Glycobiology 20:78-86
20. Liour SS, Kapitonov D, Yu RK (2000) Expression of gangliosides in neuronal development of P19 embryonal carcinoma stem cells. J Neurosci Res 62:363-373
21. Liour SS, Kraemer SA, Dinkins MB, Su CY, Yanagisawa M, Yu RK (2006) Further characterization of embryonic stem cell-derived radial glial cells. Glia 53:43-56 (Pubitemid 43076211)
22. Wang G, Silva J, Krishnamurthy K, Tran E, Condie BG, Bieberich E (2005) Direct binding to ceramide activates protein kinase Czeta before the formation of a pro-apoptotic complex with PAR-4 in differentiating stem cells. J Biol Chem 280:26415-26424 (Pubitemid 41022238)
23. Bieberich E, Freischutz B, Suzuki M, Yu RK (1999) Differential effects of glycolipid biosynthesis inhibitors on ceramideinduced cell death in neuroblastoma cells. J Neurochem 72:1040-1049 (Pubitemid 29085018)
24. Bieberich E, Kawaguchi T, Yu RK (2000) N-acylated serinol is a novel ceramide mimic inducing apoptosis in neuroblastoma cells. J Biol Chem 275:177-181 (Pubitemid 30038969)
25. Bieberich E, MacKinnon S, Silva J, Yu RK (2001) Regulation of apoptosis during neuronal differentiation by ceramide and b-series complex gangliosides. J Biol Chem 276:44396-44404
26. Bieberich E, MacKinnon S, Silva J, Noggle S, Condie BG (2003) Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J Cell Biol 162:469-479 (Pubitemid 36988555)
27. Bieberich E (2004) Integration of glycosphingolipid metabolism and cell-fate decisions in cancer and stem cells: Review and hypothesis. Glycoconj J 21:315-327 (Pubitemid 39434560)
28. Krishnamurthy K, Wang G, Silva J, Condie BG, Bieberich E (2007) Ceramide regulates atypical PKC{zeta}/{lambda}-mediated cell polarity in primitive ectoderm cells: A novel function of sphingolipids in morphogenesis. J Biol Chem 282:3379-3390 (Pubitemid 47084368)
29. Krishnamurthy K, Dasgupta S, Bieberich E (2007) Development and characterization of a novel anti-ceramide antibody. J Lipid Res 48:968-975 (Pubitemid 46557902)
30. Bieberich E (2008) Smart drugs for smarter stem cells: Making SENSe (sphingolipid-enhanced neural stem cells) of ceramide. Neurosignals 16:124-139 (Pubitemid 351263220)
31. Bieberich E (2008) Ceramide signaling in cancer and stem cells. Future Lipidol 3:273-300 (Pubitemid 352015401)
32. Wang G, Krishnamurthy K, Chiang YW, Dasgupta S, Bieberich E (2008) Regulation of neural progenitor cell motility by ceramide and potential implications for mouse brain development. J Neurochem 106:718-733
33. Wang G, Silva J, Dasgupta S, Bieberich E (2008) Long-chain ceramide is elevated in presenilin 1 (PS1M146 V) mouse brain and induces apoptosis in PS1 astrocytes. Glia 56:449-456 (Pubitemid 351212953)
34. Wang G, Krishnamurthy K, Umapathy NS, Verin AD, Bieberich E (2009) The carboxyl-terminal domain of atypical protein kinase Czeta binds to ceramide and regulates junction formation in epithelial cells. J Biol Chem 284:14469-14475
35. Yanai J, Doetchman T, Laufer N, Maslaton J, Mor-Yosef S, Safran A, Shani M, Sofer D (1995) Embryonic cultures but not embryos transplanted to the mouse's brain grow rapidly without immunosuppression. Int J Neurosci 81:21-26
36. Wakitani S, Takaoka K, Hattori T, Miyazawa N, Iwanaga T, Takeda S, Watanabe TK, Tanigami A (2003) Embryonic stem cells injected into the mouse knee joint form teratomas and subsequently destroy the joint. Rheumatology (Oxford) 42:162-165 (Pubitemid 36131582)
37. Teramoto K, Hara Y, Kumashiro Y, Chinzei R, Tanaka Y, Shimizu-Saito K, Asahina K, Teraoka H, Arii S (2005) Teratoma formation and hepatocyte differentiation in mouse liver transplanted with mouse embryonic stem cell-derived embryoid bodies. Transplant Proc 37:285-286 (Pubitemid 40459762)
38. Swijnenburg RJ, Tanaka M, Vogel H, Baker J, Kofidis T, Gunawan F, Lebl DR, Caffarelli AD, de Bruin JL, Fedoseyeva EV, Robbins RC (2005) Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 112:I166-I172 (Pubitemid 41266669)
39. Sanchez-Pernaute R, Studer L, Ferrari D, Perrier A, Lee H, Vinuela A, Isacson O (2005) Long-term survival of dopamine neurons derived from parthenogenetic primate embryonic stem cells (cyno-1) after transplantation. Stem Cells 23:914-922 (Pubitemid 41170947)
40. Kim D, Gu Y, Ishii M, Fujimiya M, Qi M, Nakamura N, Yoshikawa T, Sumi S, Inoue K (2003) In vivo functioning and transplantable mature pancreatic islet-like cell clusters differentiated from embryonic stem cell. Pancreas 27:e34-e41
41. Fujikawa T, Oh SH, Pi L, Hatch HM, Shupe T, Petersen BE (2005) Teratoma formation leads to failure of treatment for type I diabetes using embryonic stem cell-derived insulin-producing cells. Am J Pathol 166:1781-1791 (Pubitemid 40734401)
42. Fong SP, Tsang KS, Chan AB, Lu G, Poon WS, Li K, Baum LW, Ng HK (2007) Trophism of neural progenitor cells to embryonic stem cells: Neural induction and transplantation in a mouse ischemic stroke model. J Neurosci Res 85:1851-1862 (Pubitemid 47051474)
43. Choi D, Oh HJ, Chang UJ, Koo SK, Jiang JX, Hwang SY, Lee JD, Yeoh GC, Shin HS, Lee JS, Oh B (2002) In vivo differentiation of mouse embryonic stem cells into hepatocytes. Cell Transplant 11:359-368 (Pubitemid 34855516)
44. Bielby RC, Boccaccini AR, Polak JM, Buttery LD (2004) In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 10:1518-1525 (Pubitemid 39557855)
45. Arnhold S, Klein H, Semkova I, Addicks K, Schraermeyer U (2004) Neurally selected embryonic stem cells induce tumor formation after long-term survival following engraftment into the subretinal space. Invest Ophthalmol Vis Sci 45:4251-4255 (Pubitemid 39564646)
46. Baker M (2009) Stem cells: Fast and furious. Nature 458:962-965
47. Leor J, Gerecht S, Cohen S, Miller L, Holbova R, Ziskind A, Shachar M, Feinberg MS, Guetta E, Itskovitz-Eldor J (2007) Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart 93:1278-1284 (Pubitemid 47492921)
48. Blum B, Benvenisty N (2008) The tumorigenicity of human embryonic stem cells. Adv Cancer Res 100:133-158 (Pubitemid 351932182)
49. Lee AS, Tang C, Cao F, Xie X, van der Bogt K, Hwang A, Connolly AJ, Robbins RC, Wu JC (2009) Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8:2608-2612
50. Fong CY, Gauthaman K, Bongso A (2010) Teratomas from pluripotent stem cells: A clinical hurdle. J Cell Biochem 111:769-781
51. Kuznetsov SA, Cherman N, Robey PG (2010) In vivo bone formation by progeny of human embryonic stem cells. Stem Cells Dev. doi:10.1089/scd.2009.0501
52. Wang NK, Tosi J, Kasanuki JM, Chou CL, Kong J, Parmalee N, Wert KJ, Allikmets R, Lai CC, Chien CL, Nagasaki T, Lin CS, Tsang SH (2010) Transplantation of reprogrammed embryonic stem cells improves visual function in a mouse model for retinitis pigmentosa. Transplantation 89:911-919
53. Bartke N, Hannun YA (2009) Bioactive sphingolipids: Metabolism and function. J Lipid Res 50(Suppl):S91-S96
54. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139-150 (Pubitemid 351158911)
55. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758:2016-2026 (Pubitemid 44879368)
56. Futerman AH, Hannun YA (2004) The complex life of simple sphingolipids. EMBO Rep 5:777-782 (Pubitemid 39199166)
57. Merrill AH Jr, Schmelz EM, Dillehay DL, Spiegel S, Shayman JA, Schroeder JJ, Riley RT, Voss KA, Wang E (1997) Sphingolipids- the enigmatic lipid class: Biochemistry, physiology, and pathophysiology. Toxicol Appl Pharmacol 142:208-225 (Pubitemid 27051415)
58. Edsall LC, Pirianov GG, Spiegel S (1997) Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J Neurosci 17:6952-6960 (Pubitemid 27427874)
59. Fyrst H, Saba JD (2010) An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat Chem Biol 6:489-497
60. Bieberich E, Hu B, Silva J, MacKinnon S, Yu RK, Fillmore H, Broaddus WC, Ottenbrite RM (2002) Synthesis and characterization of novel ceramide analogs for induction of apoptosis in human cancer cells. Cancer Lett 181:55-64 (Pubitemid 34310662)
61. Osinde M, Mullershausen F, Dev KK (2007) Phosphorylated FTY720 stimulates ERK phosphorylation in astrocytes via S1P receptors. Neuropharmacology 52:1210-1218 (Pubitemid 46546406)
62. Coelho RP, Payne SG, Bittman R, Spiegel S, Sato-Bigbee C (2007) The immunomodulator FTY720 has a direct cytoprotective effect in oligodendrocyte progenitors. J Pharmacol Exp Ther 323:626-635 (Pubitemid 350005137)
63. Saini HS, Coelho RP, Goparaju SK, Jolly PS, Maceyka M, Spiegel S, Sato-Bigbee C (2005) Novel role of sphingosine kinase 1 as a mediator of neurotrophin-3 action in oligodendrocyte progenitors. J Neurochem 95:1298-1310 (Pubitemid 41779255)
64. Hojjati MR, Li Z, Jiang XC (2005) Serine palmitoyl-CoA transferase (SPT) deficiency and sphingolipid levels in mice. Biochim Biophys Acta 1737:44-51 (Pubitemid 41550382)
65. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL (2005) Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 25:11113-11121 (Pubitemid 41747151)
66. Zhou H, Summers SA, Birnbaum MJ, Pittman RN (1998) Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J Biol Chem 273:16568-16575 (Pubitemid 28311444)
67. Jung CG, Kim HJ, Miron VE, Cook S, Kennedy TE, Foster CA, Antel JP, Soliven B (2007) Functional consequences of S1P receptor modulation in rat oligodendroglial lineage cells. Glia 55:1656-1667 (Pubitemid 47612852)
68. Hsieh HL, Wu CB, Sun CC, Liao CH, Lau YT, Yang CM (2006) Sphingosine-1-phosphate induces COX-2 expression via PI3 K/ Akt and p42/p44 MAPK pathways in rat vascular smooth muscle cells. J Cell Physiol 207:757-766
69. Wong RC, Tellis I, Jamshidi P, Pera M, Pebay A (2007) Antiapoptotic effect of sphingosine-1-phosphate and platelet-derived growth factor in human embryonic stem cells. Stem Cells Dev 16:989-1001
70. Arboleda G, Morales LC, Benitez B, Arboleda H (2009) Regulation of ceramide-induced neuronal death: Cell metabolism meets neurodegeneration. Brain Res Rev 59:333-346
71. Bourbon NA, Sandirasegarane L, Kester M (2002) Ceramideinduced inhibition of Akt is mediated through protein kinase Czeta: Implications for growth arrest. J Biol Chem 277: 3286-3292 (Pubitemid 34953194)
72. Stoica BA, Movsesyan VA, Lea PM 4th, Faden AI (2003) Ceramide-induced neuronal apoptosis is associated with dephosphorylation of Akt, BAD, FKHR, GSK-3beta, and induction of the mitochondrial-dependent intrinsic caspase pathway. Mol Cell Neurosci 22:365-382 (Pubitemid 36407599)
73. Osawa Y, Uchinami H, Bielawski J, Schwabe RF, Hannun YA, Brenner DA (2005) Roles for C16-ceramide and sphingosine 1-phosphate in regulating hepatocyte apoptosis in response to tumor necrosis factor-alpha. J Biol Chem 280: 27879-27887 (Pubitemid 41076905)
74. Fernandez-Marcos PJ, Abu-Baker S, Joshi J, Galvez A, Castilla EA, Canamero M, Collado M, Saez C, Moreno-Bueno G, Palacios J, Leitges M, Serrano M, Moscat J and Diaz-Meco MT (2009) Simultaneous inactivation of Par-4 and PTEN in vivo leads to synergistic NF-{kappa}B activation and invasive prostate carcinoma. Proc Natl Acad Sci USA
75. Lee TJ, Lee JT, Kim SH, Choi YH, Song KS, Park JW, Kwon TK (2008) Overexpression of Par-4 enhances thapsigargininduced apoptosis via down-regulation of XIAP and inactivation of Akt in human renal cancer cells. J Cell Biochem 103:358-368
76. Diaz-Meco MT, Abu-Baker S (2009) The Par-4/PTEN connection in tumor suppression. Cell Cycle 8:2518-2522
77. Lee TJ, Jang JH, Noh HJ, Park EJ, Choi KS, Kwon TK (2010) Overexpression of Par-4 sensitizes TRAIL-induced apoptosis via inactivation of NF-kappaB and Akt signaling pathways in renal cancer cells. J Cell Biochem 109:885-895
78. Sun B, Lu C, Zhou GP, Xing CY (2010) Suppression of Par-4 protects human renal proximal tubule cells from apoptosis induced by oxidative stress. Nephron Exp Nephrol 117:e53-e61
79. Goswami A, Ranganathan P, Rangnekar VM (2006) The phosphoinositide 3-kinase/Akt1/Par-4 axis: A cancer-selective therapeutic target. Cancer Res 66:2889-2892
80. Hancock CR, Wetherington JP, Lambert NA, Condie BG (2000) Neuronal differentiation of cryopreserved neural progenitor cells derived from mouse embryonic stem cells. Biochem Biophys Res Commun 271:418-421 (Pubitemid 30444741)
81. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 59:89-102 (Pubitemid 26325462)
82. Ruhparwar A, Bara C, Kofidis T, Ruebesamen N, Karck M, Martin U, Haverich A (2006) In vivo detection of integration of grafted cells after myocardial transplantation. Zentralbl Chir 131:420-424 (Pubitemid 44785653)
83. Ruhparwar A, Kofidis T, Ruebesamen N, Karck M, Haverich A, Martin U (2005) Intra-vital fluorescence microscopy for intramyocardial graft detection following cell transplantation. Int J Cardiovasc Imaging 21:569-574 (Pubitemid 41435160)
84. Xian HQ, McNichols E, St Clair A, Gottlieb DI (2003) A subset of ES-cell-derived neural cells marked by gene targeting. Stem Cells 21:41-49 (Pubitemid 36120364)
85. Xian H, Gottlieb DI (2004) Dividing Olig2-expressing progenitor cells derived from ES cells. Glia 47:88-101 (Pubitemid 38879709)
86. Paugh SW, Payne SG, Barbour SE, Milstien S, Spiegel S (2003) The immunosuppressant FTY720 is phosphorylated by sphingosine kinase type 2. FEBS Lett 554:189-193 (Pubitemid 37324838)
87. Loveridge C, Tonelli F, Leclercq T, Lim KG, Long JS, Berdyshev E, Tate RJ, Natarajan V, Pitson SM, Pyne NJ, Pyne S (2010) The sphingosine kinase 1 inhibitor 2-(P-hydroxyanilino)- 4-(P-chlorophenyl)thiazole induces proteasomal degradation of sphingosine kinase 1 in mammalian cells. J Biol Chem. doi: 10.1074/jbc.M110.127993
88. Berdyshev EV, Gorshkova I, Skobeleva A, Bittman R, Lu X, Dudek SM, Mirzapoiazova T, Garcia JG, Natarajan V (2009) FTY720 inhibits ceramide synthases and up-regulates dihydrosphingosine 1-phosphate formation in human lung endothelial cells. J Biol Chem 284:5467-5477
89. Tonelli F, Lim KG, Loveridge C, Long J, Pitson SM, Tigyi G, Bittman R, Pyne S, Pyne NJ (2010) FTY720 and (S)-FTY720 vinylphosphonate inhibit sphingosine kinase 1 and promote its proteasomal degradation in human pulmonary artery smooth muscle, breast cancer and androgen-independent prostate cancer cells. Cell Signal 22:1536-1542
90. Lahiri S, Park H, Laviad EL, Lu X, Bittman R, Futerman AH (2009) Ceramide synthesis is modulated by the sphingosine analog FTY720 via a mixture of uncompetitive and noncompetitive inhibition in an Acyl-CoA chain length-de pend ent manner. J Biol Chem 284:16090-16098
91. Kasai N, Yu RK (1983) The monoclonal antibody A2B5 is specific to ganglioside GQ1c. Brain Res 277:155-158 (Pubitemid 13021233)
92. Kim SU, Moretto G, Lee V, Yu RK (1986) Neuroimmunology of gangliosides in human neurons and glial cells in culture. J Neurosci Res 15:303-321 (Pubitemid 16118992)
93. Rao MS, Mayer-Proschel M (1997) Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 188:48-63 (Pubitemid 27360086)
94. Rao MS, Noble M, Mayer-Proschel M (1998) A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA 95:3996-4001 (Pubitemid 28173242)
95. Herrera J, Yang H, Zhang SC, Proschel C, Tresco P, Duncan ID, Luskin M, Mayer-Proschel M (2001) Embryonic-derived glialrestricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp Neurol 171:11-21 (Pubitemid 32848441)
96. Noble M, Proschel C, Mayer-Proschel M (2004) Getting a GR(i)P on oligodendrocyte development. Dev Biol 265:33-52 (Pubitemid 38028512)
97. Levi G, Gallo V, Ciotti MT (1986) Bipotential precursors of putative fibrous astrocytes and oligodendrocytes in rat cerebellar cultures express distinct surface features and "neuron-like" gamma-aminobutyric acid transport. Proc Natl Acad Sci USA 83:1504-1508 (Pubitemid 16016158)
98. Schnitzer J, Schachner M (1982) Cell type specificity of a neural cell surface antigen recognized by the monoclonal antibody A2B5. Cell Tissue Res 224:625-636 (Pubitemid 12055444)
99. Abney ER, Williams BP, Raff MC (1983) Tracing the development of oligodendrocytes from precursor cells using monoclonal antibodies, fluorescence-activated cell sorting, and cell culture. Dev Biol 100:166-171 (Pubitemid 14238261)
100. Raff MC, Abney ER, Miller RH (1984) Two glial cell lineages diverge prenatally in rat optic nerve. Dev Biol 106:53-60 (Pubitemid 15209360)
101. Saneto RP, de Vellis J (1985) Characterization of cultured rat oligodendrocytes proliferating in a serum-free, chemically defined medium. Proc Natl Acad Sci USA 82:3509-3513 (Pubitemid 15030714)
102. Lubetzki C, Goujet-Zalc C, Gansmuller A, Monge M, Brillat A, Zalc B (1991) Morphological, biochemical, and functional characterization of bulk isolated glial progenitor cells. J Neurochem 56:671-680 (Pubitemid 21902013)
103. Kalyani A, Hobson K, Rao MS (1997) Neuroepithelial stem cells from the embryonic spinal cord: Isolation, characterization, and clonal analysis. Dev Biol 186:202-223 (Pubitemid 27319570)
104. Amat JA, Farooq M, Ishiguro H, Norton WT (1998) Cells of the oligodendrocyte lineage proliferate following cortical stab wounds: An in vitro analysis. Glia 22:64-71 (Pubitemid 28038044)
105. Bansal R, Winkler S, Bheddah S (1999) Negative regulation of oligodendrocyte differentiation by galactosphingolipids. J Neurosci 19:7913-7924 (Pubitemid 30225789)
106. Gensert JM, Goldman JE (2001) Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter. J Neurobiol 48:75-86 (Pubitemid 32645825)
107. Wilson HC, Onischke C, Raine CS (2003) Human oligodendrocyte precursor cells in vitro: Phenotypic analysis and differential response to growth factors. Glia 44:153-165 (Pubitemid 37345625)
108. Dasgupta S, Everhart MB, Bhat NR, Hogan EL (1997) Neutral monoglycosylceramides in rat brain: Occurrence, molecular expression and developmental variation. Dev Neurosci 19:152-161 (Pubitemid 27110638)
109. Sells SF, Wood DP Jr, Joshi-Barve SS, Muthukumar S, Jacob RJ, Crist SA, Humphreys S, Rangnekar VM (1994) Commonality of the gene programs induced by effectors of apoptosis in androgen-dependent and -independent prostate cells. Cell Growth Differ 5:457-466 (Pubitemid 24251397)
110. Guo Q, Fu W, Xie J, Luo H, Sells SF, Geddes JW, Bondada V, Rangnekar VM, Mattson MP (1998) Par-4 is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer disease. Nat Med 4:957-962 (Pubitemid 28364038)
111. Azmi AS, Wang Z, Burikhanov R, Rangnekar VM, Wang G, Chen J, Wang S, Sarkar FH, Mohammad RM (2008) Critical role of prostate apoptosis response-4 in determining the sensitivity of pancreatic cancer cells to small-molecule inhibitorinduced apoptosis. Mol Cancer Ther 7:2884-2893
112. Zhao Y, Rangnekar VM (2008) Apoptosis and tumor resistance conferred by Par-4. Cancer Biol Ther 7:1867-1874
113. Wang G, Silva J, Krishnamurthy K, Bieberich E (2006) A novel isoform of prostate apoptosis response 4 (PAR-4) that co-distributes with F-actin and prevents apoptosis in neural stem cells. Apoptosis 11:315-325
114. Spiegel S, Milstien S (2003) Sphingosine-1-phosphate: An enigmatic signalling lipid. Nat Rev Mol Cell Biol 4:397-407 (Pubitemid 36565571)
115. Sim-Selley LJ, Goforth PB, Mba MU, Macdonald TL, Lynch KR, Milstien S, Spiegel S, Satin LS, Welch SP, Selley DE (2009) Sphingosine-1-phosphate receptors mediate neuromodulatory functions in the CNS. J Neurochem 110:1191-1202
116. Taha TA, Argraves KM, Obeid LM (2004) Sphingosine-1- phosphate receptors: Receptor specificity versus functional redundancy. Biochim Biophys Acta 1682:48-55 (Pubitemid 38670534)
117. Mao C, Obeid LM (2008) Ceramidases: Regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine- 1-phosphate. Biochim Biophys Acta 1781:424-434
118. Qin J, Berdyshev E, Goya J, Natarajan V, Dawson G (2010) Neurons and oligodendrocytes recycle sphingosine 1-phosphate to ceramide: Significance for apoptosis and multiple sclerosis. J Biol Chem 285:14134-14143
119. Coelho RP, Saini HS, Sato-Bigbee C (2010) Sphingosine-1- phosphate and oligodendrocytes: From cell development to the treatment of multiple sclerosis. Prostaglandins Other Lipid Mediat 91:139-144
120. Miron VE, Jung CG, Kim HJ, Kennedy TE, Soliven B, Antel JP (2008) FTY720 modulates human oligodendrocyte progenitor process extension and survival. Ann Neurol 63:61-71 (Pubitemid 351240552)
121. Miron VE, Schubart A, Antel JP (2008) Central nervous systemdirected effects of FTY720 (fingolimod). J Neurol Sci 274:13-17
122. Lee CW, Choi JW, Chun J (2010) Neurological S1P signaling as an emerging mechanism of action of oral FTY720 (Fingolimod) in multiple sclerosis. Arch Pharm Res 33:1567-1574