Neurostatin blocks glioma cell cycle progression by inhibiting EGFR activation

Molecular and Cellular Neuroscience

Volumn 46, Issue 1, 2011, Pages 89-100

  Valle Argos, Beatriz ^a   Gómez Nicola, Diego ^a,b   Nieto Sampedro, Manuel ^a,b  

^a INSTITUTO CAJAL   (Spain)

^b HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

Author keywords

Cell cycle; EGFR; Gangliosides; Glioma; Neurostatin

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN A; CYCLIN B; CYCLIN D1; CYCLIN D3; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; EPIDERMAL GROWTH FACTOR RECEPTOR; GANGLIOSIDE GD 1B; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROSTATIN; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; GLIOMA CELL; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LOW DRUG DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; CELL CYCLE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYCLINS; FEMALE; GLIOMA; GLYCOSPHINGOLIPIDS; HUMANS; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSPLANTATION, HETEROLOGOUS;

EID: 78650892976     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.08.009     Document Type: Article

References (95)

1. Abad-Rodriguez J., Bernabe M., Romero-Ramirez L., Vallejo-Cremades M., Fernandez-Mayoralas A., Nieto-Sampedro M. Purification and structure of neurostatin, an inhibitor of astrocyte division of mammalian brain. J. Neurochem. 2000, 74:2547-2556.
2. Abad-Rodriguez J., Vallejo-Cremades M., Nieto-Sampedro M. Control of glial number: purification from mammalian brain extracts of an inhibitor of astrocyte division. Glia 1998, 23:156-168.
3. Bhattacharya S., Ray R.M., Johnson L.R. Prevention of TNF-alpha-induced apoptosis in polyamine-depleted IEC-6 cells is mediated through the activation of ERK1/2. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 286:G479-G490.
4. Birkle S., Zeng G., Gao L., Yu R.K., Aubry J. Role of tumor-associated gangliosides in cancer progression. Biochimie 2003, 85:455-463.
5. Bremer E.G., Schlessinger J., Hakomori S. Ganglioside-mediated modulation of cell growth. Specific effects of GM3 on tyrosine phosphorylation of the epidermal growth factor receptor. J. Biol. Chem. 1986, 261:2434-2440.
6. Brezak M.C., Kasprzyk P.G., Galcera M.O., Lavergne O., Prevost G.P. CDC25 inhibitors as anticancer agents are moving forward. Anticancer Agents Med. Chem. 2008, 8:857-862.
7. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., Frisch S., Reed J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998, 282:1318-1321.
8. Choi H.J., Chung T.W., Kang S.K., Lee Y.C., Ko J.H., Kim J.G., Kim C.H. Ganglioside GM3 modulates tumor suppressor PTEN-mediated cell cycle progression-transcriptional induction of p21(WAF1) and p27(kip1) by inhibition of PI-3K/AKT pathway. Glycobiology 2006, 16:573-583.
9. Chuang C.F., Ng S.Y. Functional divergence of the MAP kinase pathway. ERK1 and ERK2 activate specific transcription factors. FEBS Lett. 1994, 346:229-234.
10. Costello J.F., Plass C., Arap W., Chapman V.M., Held W.A., Berger M.S., Su Huang H.J., Cavenee W.K. Cyclin-dependent kinase 6 (CDK6) amplification in human gliomas identified using two-dimensional separation of genomic DNA. Cancer Res. 1997, 57:1250-1254.
11. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997, 91:231-241.
12. Deng X., Ruvolo P., Carr B., May W.S. Survival function of ERK1/2 as IL-3-activated, staurosporine-resistant Bcl2 kinases. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1578-1583.
13. Diehl J.A., Cheng M., Roussel M.F., Sherr C.J. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 1998, 12:3499-3511.
14. Egan S.E., Giddings B.W., Brooks M.W., Buday L., Sizeland A.M., Weinberg R.A. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature 1993, 363:45-51.
15. Ekstrand A.J., Sugawa N., James C.D., Collins V.P. Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:4309-4313.
16. Emlet D.R., Moscatello D.K., Ludlow L.B., Wong A.J. Subsets of epidermal growth factor receptors during activation and endocytosis. J. Biol. Chem. 1997, 272:4079-4086.
17. Ettenberg S.A., Keane M.M., Nau M.M., Frankel M., Wang L.M., Pierce J.H., Lipkowitz S. cbl-b inhibits epidermal growth factor receptor signaling. Oncogene 1999, 18:1855-1866.
18. Feldkamp M.M., Lala P., Lau N., Roncari L., Guha A. Expression of activated epidermal growth factor receptors, Ras-guanosine triphosphate, and mitogen-activated protein kinase in human glioblastoma multiforme specimens. Neurosurgery 1999, 45:1442-1453.
19. Fleming T.P., Saxena A., Clark W.C., Robertson J.T., Oldfield E.H., Aaronson S.A., Ali I.U. Amplification and/or overexpression of platelet-derived growth factor receptors and epidermal growth factor receptor in human glial tumors. Cancer Res. 1992, 52:4550-4553.
20. Fotedar R., Fotedar A. Cell cycle control of DNA replication. Prog. Cell Cycle Res. 1995, 1:73-89.
21. Friedman H. What is "hope" for a patient with a deadly brain tumor?. Cerebrum: DANA Forum Brain Sci. 2003, 5:7-18.
22. Furnari F.B., Fenton T., Bachoo R.M., Mukasa A., Stommel J.M., Stegh A., Hahn W.C., Ligon K.L., Louis D.N., Brennan C., Chin L., DePinho R.A., Cavenee W.K. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007, 21:2683-2710.
23. Gomez-Nicola D., Doncel-Perez E., Nieto-Sampedro M. Regulation by GD3 of the proinflammatory response of microglia mediated by interleukin-15. J. Neurosci. Res. 2006, 83:754-762.
24. Gomez-Nicola D., Valle-Argos B., Nieto-Sampedro M. Blockade of IL-15 activity inhibits microglial activation through the NFkappaB, p38, and ERK1/2 pathways, reducing cytokine and chemokine release. Glia 2010, 58:264-276.
25. Gomez-Nicola D., Valle-Argos B., Pita-Thomas D.W., Nieto-Sampedro M. Interleukin 15 expression in the CNS: Blockade of its activity prevents glial activation after an inflammatory injury. Glia 2008, 56:494-505.
26. Gomez-Nicola D., Valle-Argos B., Suardiaz M., Taylor J.S., Nieto-Sampedro M. Role of IL-15 in spinal cord and sciatic nerve after chronic constriction injury: regulation of macrophage and T-cell infiltration. J. Neurochem. 2008, 107:1741-1752.
27. Gregory M.A., Qi Y., Hann S.R. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J. Biol. Chem. 2003, 278:51606-51612.
28. Haga Y., Hatanaka K., Hakomori S.I. Effect of lipid mimetics of GM3 and lyso-GM3 dimer on EGF receptor tyrosine kinase and EGF-induced signal transduction. Biochim. Biophys. Acta 2008, 1780:393-404.
29. Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 1996, 56:5309-5318.
30. Henson J.W., Schnitker B.L., Correa K.M., von D.A., Fassbender F., Xu H.J., Benedict W.F., Yandell D.W., Louis D.N. The retinoblastoma gene is involved in malignant progression of astrocytomas. Ann. Neurol. 1994, 36:714-721.
31. Huang P.H., Xu A.M., White F.M. Oncogenic EGFR signaling networks in glioma. Sci. Signal. 2009, 2:re6.
32. James C.D., Carlbom E., Dumanski J.P., Hansen M., Nordenskjold M., Collins V.P., Cavenee W.K. Clonal genomic alterations in glioma malignancy stages. Cancer Res. 1988, 48:5546-5551.
33. Kanu O.O., Mehta A., Di C., Lin N., Bortoff K., Bigner D.D., Yan H., Adamson D.C. Glioblastoma multiforme: a review of therapeutic targets. Expert Opin. Ther. Targets 2009, 13:701-718.
34. Kapoor G.S., O'Rourke D.M. Mitogenic signaling cascades in glial tumors. Neurosurgery 2003, 52:1425-1434.
35. Kapoor G.S., O'Rourke D.M. Receptor tyrosine kinase signaling in gliomagenesis: pathobiology and therapeutic approaches. Cancer Biol. Ther. 2003, 2:330-342.
36. Kawada M., Yamagoe S., Murakami Y., Suzuki K., Mizuno S., Uehara Y. Induction of p27Kip1 degradation and anchorage independence by Ras through the MAP kinase signaling pathway. Oncogene 1997, 15:629-637.
37. Kitagawa M., Higashi H., Jung H.K., Suzuki-Takahashi I., Ikeda M., Tamai K., Kato J., Segawa K., Yoshida E., Nishimura S., Taya Y. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 1996, 15:7060-7069.
38. Lauren J., Gunji Y., Alitalo K. Is angiopoietin-2 necessary for the initiation of tumor angiogenesis?. Am. J. Pathol. 1998, 153:1333-1339.
39. Lavoie J.N., L'Allemain G., Brunet A., Muller R., Pouyssegur J. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J. Biol. Chem. 1996, 271:20608-20616.
40. Levkowitz G., Waterman H., Ettenberg S.A., Katz M., Tsygankov A.Y., Alroy I., Lavi S., Iwai K., Reiss Y., Ciechanover A., Lipkowitz S., Yarden Y. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 1999, 4:1029-1040.
41. Li W., Nishimura R., Kashishian A., Batzer A.G., Kim W.J., Cooper J.A., Schlessinger J. A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 1994, 14:509-517.
42. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109.
43. Lui V.W., Grandis J.R. EGFR-mediated cell cycle regulation. Anticancer Res. 2002, 22:1-11.
44. Maddika S., Ande S.R., Panigrahi S., Paranjothy T., Weglarczyk K., Zuse A., Eshraghi M., Manda K.D., Wiechec E., Los M. Cell survival, cell death and cell cycle pathways are interconnected: implications for cancer therapy. Drug Resist. Updat. 2007, 10:13-29.
45. Martens T., Laabs Y., Gunther H.S., Kemming D., Zhu Z., Witte L., Hagel C., Westphal M., Lamszus K. Inhibition of glioblastoma growth in a highly invasive nude mouse model can be achieved by targeting epidermal growth factor receptor but not vascular endothelial growth factor receptor-2. Clin. Cancer Res. 2008, 14:5447-5458.
46. Martinvalet D., Dykxhoorn D.M., Ferrini R., Lieberman J. Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death. Cell 2008, 133:681-692.
47. Medema R.H., Kops G.J., Bos J.L., Burgering B.M. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 2000, 404:782-787.
48. Miletic H., Niclou S.P., Johansson M., Bjerkvig R. Anti-VEGF therapies for malignant glioma: treatment effects and escape mechanisms. Expert Opin. Ther. Targets 2009, 13:455-468.
49. Miljan E.A., Bremer E.G. Regulation of growth factor receptors by gangliosides. Sci. STKE 2002, RE15.
50. Miljan E.A., Meuillet E.J., Mania-Farnell B., George D., Yamamoto H., Simon H.G., Bremer E.G. Interaction of the extracellular domain of the epidermal growth factor receptor with gangliosides. J. Biol. Chem. 2002, 277:10108-10113.
51. Mirkin B.L., Clark S.H., Zhang C. Inhibition of human neuroblastoma cell proliferation and EGF receptor phosphorylation by gangliosides GM1, GM3, GD1A and GT1B. Cell Prolif. 2002, 35:105-115.
52. Mishima K., Johns T.G., Luwor R.B., Scott A.M., Stockert E., Jungbluth A.A., Ji X.D., Suvarna P., Voland J.R., Old L.J., Huang H.J., Cavenee W.K. Growth suppression of intracranial xenografted glioblastomas overexpressing mutant epidermal growth factor receptors by systemic administration of monoclonal antibody (mAb) 806, a novel monoclonal antibody directed to the receptor. Cancer Res. 2001, 61:5349-5354.
53. Mittnacht S., Lees J.A., Desai D., Harlow E., Morgan D.O., Weinberg R.A. Distinct sub-populations of the retinoblastoma protein show a distinct pattern of phosphorylation. EMBO J. 1994, 13:118-127.
54. Mohanam S., Chintala S.K., Go Y., Bhattacharya A., Venkaiah B., Boyd D., Gokaslan Z.L., Sawaya R., Rao J.S. In vitro inhibition of human glioblastoma cell line invasiveness by antisense uPA receptor. Oncogene 1997, 14:1351-1359.
55. Mohanam S., Sawaya R.E., Yamamoto M., Bruner J.M., Nicholson G.L., Rao J.S. Proteolysis and invasiveness of brain tumors: role of urokinase-type plasminogen activator receptor. J. Neurooncol. 1994, 22:153-160.
56. Mori M., Uchida M., Watanabe T., Kirito K., Hatake K., Ozawa K., Komatsu N. Activation of extracellular signal-regulated kinases ERK1 and ERK2 induces Bcl-xL up-regulation via inhibition of caspase activities in erythropoietin signaling. J. Cell. Physiol. 2003, 195:290-297.
57. Moriyama T., Kataoka H., Seguchi K., Tsubouchi H., Koono M. Effects of hepatocyte growth factor (HGF) on human glioma cells in vitro: HGF acts as a motility factor in glioma cells. Int. J. Cancer 1996, 66:678-685.
58. Nakatsuji Y., Miller R.H. Selective cell-cycle arrest and induction of apoptosis in proliferating neural cells by ganglioside GM3. Exp. Neurol. 2001, 168:290-299.
59. New D.C., Wong Y.H. CC chemokine receptor-coupled signalling pathways. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao 2003, 35:779-788. (Shanghai).
60. Nieto-Sampedro M. Astrocyte mitogen inhibitor related to epidermal growth factor receptor. Science 1988, 240:1784-1786.
61. Nieto-Sampedro M., Broderick J.T. A soluble brain molecule related to epidermal growth factor receptor is a mitogen inhibitor for astrocytes. J. Neurosci. Res. 1989, 22:28-35.
62. Noll E.N., Lin J., Nakatsuji Y., Miller R.H., Black P.M. GM3 as a novel growth regulator for human gliomas. Exp. Neurol. 2001, 168:300-309.
63. Nyati M.K., Morgan M.A., Feng F.Y., Lawrence T.S. Integration of EGFR inhibitors with radiochemotherapy. Nat. Rev. Cancer 2006, 6:876-885.
64. Ohgaki H., Dessen P., Jourde B., Horstmann S., Nishikawa T., Di Patre P.L., Burkhard C., Schuler D., Probst-Hensch N.M., Maiorka P.C., Baeza N., Pisani P., Yonekawa Y., Yasargil M.G., Lutolf U.M., Kleihues P. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 2004, 64:6892-6899.
65. Pardee A.B. G1 events and regulation of cell proliferation. Science 1989, 246:603-608.
66. Rasband W.S. ImageJ 1.38x. 1997-2008: ImageJ 2008, U.S.National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/,1997-2007.
67. Rebbaa A., Chou P.M., Bremer E.G. Modulation of growth factor response in brain tumors by complex carbohydrates. Bull. Cancer 2004, 91:E15-E60.
68. Rebbaa A., Hurh J., Yamamoto H., Kersey D.S., Bremer E.G. Ganglioside GM3 inhibition of EGF receptor mediated signal transduction. Glycobiology 1996, 6:399-406.
69. Reich R., Thompson E.W., Iwamoto Y., Martin G.R., Deason J.R., Fuller G.C., Miskin R. Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res. 1988, 48:3307-3312.
70. Reifenberger G., Reifenberger J., Ichimura K., Meltzer P.S., Collins V.P. Amplification of multiple genes from chromosomal region 12q13-14 in human malignant gliomas: preliminary mapping of the amplicons shows preferential involvement of CDK4, SAS, and MDM2. Cancer Res. 1994, 54:4299-4303.
71. Rivard N., L'Allemain G., Bartek J., Pouyssegur J. Abrogation of p27Kip1 by cDNA antisense suppresses quiescence (G0 state) in fibroblasts. J. Biol. Chem. 1996, 271:18337-18341.
72. Rojas M., Yao S., Lin Y.Z. Controlling epidermal growth factor (EGF)-stimulated Ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J. Biol. Chem. 1996, 271:27456-27461.
73. Romero-Ramirez L., Nieto-Sampedro M. Inhibiting human astrocytoma growth: structure-activity relationships in neurostatin related glycolipids. J. Med. Chem. 2004, 47:4983-4984.
74. Rusnati M., Tanghetti E., Urbinati C., Tulipano G., Marchesini S., Ziche M., Presta M. Interaction of fibroblast growth factor-2 (FGF-2) with free gangliosides: biochemical characterization and biological consequences in endothelial cell cultures. Mol. Biol. Cell 1999, 10:313-327.
75. Salcini A.E., McGlade J., Pelicci G., Nicoletti I., Pawson T., Pelicci P.G. Formation of Shc-Grb2 complexes is necessary to induce neoplastic transformation by overexpression of Shc proteins. Oncogene 1994, 9:2827-2836.
76. Sampson J.H., Crotty L.E., Lee S., Archer G.E., Ashley D.M., Wikstrand C.J., Hale L.P., Small C., Dranoff G., Friedman A.H., Friedman H.S., Bigner D.D. Unarmed, tumor-specific monoclonal antibody effectively treats brain tumors. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7503-7508.
77. Sawaya R.E., Yamamoto M., Gokaslan Z.L., Wang S.W., Mohanam S., Fuller G.N., McCutcheon I.E., Stetler-Stevenson W.G., Nicolson G.L., Rao J.S. Expression and localization of 72kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin. Exp. Metastasis 1996, 14:35-42.
78. Schulze W.X., Deng L., Mann M. Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 2005, 1:2005.
79. Sherr C.J. Cancer cell cycles. Science 1996, 274:1672-1677.
80. Sherr C.J. G1 phase progression: cycling on cue. Cell 1994, 79:551-555.
81. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999, 13:1501-1512.
82. Shi M., Yan S.G., Xie S.T., Wang H.N. Tip30-induced apoptosis requires translocation of Bax and involves mitochondrial release of cytochrome c and Smac/DIABLO in hepatocellular carcinoma cells. Biochim. Biophys. Acta 2008, 1783:263-274.
83. Shin I., Yakes F.M., Rojo F., Shin N.Y., Bakin A.V., Baselga J., Arteaga C.L. PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat. Med. 2002, 8:1145-1152.
84. Sun P., Wang X.Q., Lopatka K., Bangash S., Paller A.S. Ganglioside loss promotes survival primarily by activating integrin-linked kinase/Akt without phosphoinositide 3-OH kinase signaling. J. Invest. Dermatol. 2002, 119:107-117.
85. Tate M.C., Aghi M.K. Biology of angiogenesis and invasion in glioma. Neurotherapeutics 2009, 6:447-457.
86. Treisman R. Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 1996, 8:205-215.
87. Valle-Argos B., Gomez-Nicola D., Nieto-Sampedro M. Glioma growth inhibition by neurostatin and O-But GD1b. Neuro Oncol. 2010, Jul 8. [Epub ahead of print].
88. Valle-Argos B., Gomez-Nicola D., Nieto-Sampedro M. Synthesis and characterization of neurostatin-related compounds with high inhibitory activity of glioma growth. Eur. J. Med. Chem. 2010, 45:2034-2043.
89. Van Brocklyn J., Bremer E.G., Yates A.J. Gangliosides inhibit platelet-derived growth factor-stimulated receptor dimerization in human glioma U-1242MG and Swiss 3T3 cells. J. Neurochem. 1993, 61:371-374.
90. Weber J.D., Raben D.M., Phillips P.J., Baldassare J.J. Sustained activation of extracellular-signal-regulated kinase 1 (ERK1) is required for the continued expression of cyclin D1 in G1 phase. Biochem. J. 1997, 326(Pt 1):61-68.
91. Wild-Bode C., Weller M., Wick W. Molecular determinants of glioma cell migration and invasion. J. Neurosurg. 2001, 94:978-984.
92. Williams M.A., McCluer R.H. The use of Sep-Pak C18 cartridges during the isolation of gangliosides. J. Neurochem. 1980, 35:266-269.
93. Xiong Y., Zhang H., Beach D. Subunit rearrangement of the cyclin-dependent kinases is associated with cellular transformation. Genes Dev. 1993, 7:1572-1583.
94. Yamini B., Yu X., Pytel P., Galanopoulos N., Rawlani V., Veerapong J., Bickenbach K., Weichselbaum R.R. Adenovirally delivered tumor necrosis factor-alpha improves the antiglioma efficacy of concomitant radiation and temozolomide therapy. Clin. Cancer Res. 2007, 13:6217-6223.
95. Zurita A.R., Maccioni H.J., Daniotti J.L. Modulation of epidermal growth factor receptor phosphorylation by endogenously expressed gangliosides. Biochem. J. 2001, 355:465-472.