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Apoptosis of human carcinoma cells in the presence of potential anti-cancer drugs: III. Treatment of Colo-205 and SKBR3 cells with: cis-platin, Tamoxifen, Melphalan, Betulinic acid, L-PDMP, L-PPMP, and GD3 ganglioside

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Abstract

Breast cancer is the most common type of cancer, predominantly among women over 20, whereas colo-rectal cancer occurs in both men and women over the age of 50. Chemotherapy of both cancers affect rapidly growing normal as well as cancer cells. Cancer cells are non-apoptotic. Seven anti-cancer agents (cis-platin, Tamoxifen, Melphalan, Betulinic acid, D-PDMP, L-PPMP, and GD3) have been tested with human breast (SKBR3) and colon (Colo-205) carcinoma cells for their apoptotic effect and found to be positive by several assay systems. Colo-205 cells were obtained from ATCC, and the SKBR3 cells were a gift from the Cleveland Clinic. All of these six agents killed those two cell lines in a dose-dependent manner. In the early apoptotic stage (6 h), these cells showed only a flopping of phosphatidylserine on the outer lamella of the plasma membranes as evidenced by the binding of a novel fluorescent dye PSS-380. After 24 h of the treatment, those apoptotic cells showed damage of the plasma as well as the nuclear membrane as evidenced by binding of propidium iodide to the nuclear DNA. DNA laddering assay viewed further breakdown of DNA by 1% agarose gel electrophoresis analysis. It is concluded that during apoptosis the signaling by Mitochondrial Signaling Pathway (MSP) is stimulated by some of these agents. Caspase 3 was activated with the concomitant appearance of its p17 polypeptide as viewed by Westernblot analyses. Incorporation of radioactivity from [U-14C]-L-serine in total sphingolipid mixture was observed between 2 and 4 micromolar concentrations of most of the agents except cis-platin. However, apoptosis in carcinoma cells in the presence of cis-platin is induced by a caspase 3 activation pathway without any increase in synthesis of ceramide. Published in 2004..

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References

  1. Wyllie AH, Apoptosis: Cell death in tissue regulation. J Pathol 153, 313–6 (1987).

    PubMed  Google Scholar 

  2. Arends MJ, Wyllie AH, Apoptosis: Mechanisms and roles in pathology. Int Rev Exp Pathol 3 2, 223–54 (1991).

    PubMed  Google Scholar 

  3. Pisha E, Chai H, Lee IS, Chagwedera TE, Farnsworth NR, Cordell GA, Beecher CW, Fong HH, Kinghorn AD, Brown DM, et al., Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis. Nat Med 1, 1046–51 (1995).

    Article  PubMed  Google Scholar 

  4. Ritke MK, Rusnak JM, Lazo JS, Allan WP, Dive C, Heer S, Yalowich JC, Differential induction of etoposide-mediated apop-tosis in human leukemia HL-60 and K562 cells. Mol Pharmacol 4 6, 605–11 (1994).

    PubMed  Google Scholar 

  5. Schmidt ML, Kuzmanoff KL, Ling-Indeck L, Pezzuto JM, Be-tulinic acid induces apoptosis in human neuroblastoma cell lines.Eur J Cancer 33, 2007–10 (1997).

    Article  PubMed  Google Scholar 

  6. Couldwell WT, Hinton DR, He S, Chen TC, Sebat I, Weiss MH, Law RE, Protein kinase C inhibitors induce apoptosis in human malignant glioma cell lines. FEBS Lett 345, 43–6 (1994).

    Article  PubMed  Google Scholar 

  7. Issandou M, Faucher C, Bayard F, Darbon JM, Opposite effects of tamoxifen on in vitroprotein kinase C activity and endogenous protein phosphorylation in intact MCF-7 cells. Cancer Res 50, 5845–50 (1990).

    PubMed  Google Scholar 

  8. Devita VT, Hellman S, Rosenberg SA, Biologic Therapy of Cancer, 2nd edition (1995).

  9. Ashkenazi A, Dixit VM, Death receptors, signaling and modulation.Science 281, 1305–8 (1998).

    Article  PubMed  Google Scholar 

  10. Basu S, Ma R, Mikulla B, Bradley M, Moulton C, Basu M, Banerjee S, Inokuchi J, Apoptosis of human carcinoma cells in the presence of inhibitors of glycosphingolipid biosynthesis: I.Treatment of Colo-205 and SKBR3 cells with isomers of PDMP and PPMP. Glycoconj J 2 0(3), 157–68 (2003).

    Article  Google Scholar 

  11. Ma R, Koulov A, Basu M, Banerjee S, Goodson H, Basu S, Apopto-sis of Colon and Breast Carcinoma Cells in the Presence of Added Disialosyl Gangliosides: II.Treatment of Colo-205 and SKBR3 Cells with GD3 and GD1b. in Glycoconjugates and Cell Signal-ing, Issue-3; Glycoconj J 20(5), 319–33 (2004).

    Article  PubMed  Google Scholar 

  12. Ray S, Kelley TJ, Fan L, Basu S, Characterization of DNA Pol-alpha/ Primase Complex From Embryonic Chicken Brain. India J Biochem Biophys 31, 226–35 (1994).

    Google Scholar 

  13. Boyle PJ, Ma R, Moulton C, Vranish J, Banerjee S, Tuteja N, Basu M, Basu S, Changes in the helicase activity of the replication complex during apoptosis of breast and colon carcinoma cells.FASEB J 18(8), page-C289.

  14. Gao X, Fisher SG, Emami B, Risk of second primary cancer in the contralateral breast in women treated for early-stage breast cancer: a population-based study. Int J Radiat Oncol Biol Phys 56, 1038–45 (2003).

    Article  PubMed  Google Scholar 

  15. Wingo PA, Jamison PM, Young JL, Gargiullo P, Population-Based Statistics for Women Diagnosed with Inflammatory Breast Cancer (United States). Cancer Causes Control 15, 321–8 (2004).

    Article  PubMed  Google Scholar 

  16. Salami S, Karami-Tehrani F, Biochemical studies of apoptosis induced by tamoxifen in estrogen receptor positive and negative breast cancer cell lines. Clin Biochem 36, 247–53 (2003).

    Article  PubMed  Google Scholar 

  17. Hawkin RA, Arends MJ, Ritchie AA, Langdon S, Miller WR, Tamoxifen increases apoptosis but does not influence markers of proliferation in an MCF-7 xenograft model of breast cancer. Breast 9, 96–106 (2000).

    Article  PubMed  Google Scholar 

  18. Simeone AM, Ekmekcioglu S, Broemeling LD, Grimm EA, Tari AM, A novel mechanism by which N-(4-hydroxyphenyl)retinamide inhibits breast cancer cell growth: the production of nitric oxide. Mol Cancer Ther 1, 1009–17 (2002).

    PubMed  Google Scholar 

  19. Majumdar SK, Valdellon JA, Brown KA, In vitroInvestigations on the toxicity and cell death induced by tamoxifen on two non-breast cancer cell types. J Biomed Biotechnol 1, 99–107 (2001).

    Article  PubMed  Google Scholar 

  20. Tavassoli M, Soltaninia J, Rudnicka J, Mashanyare D, Johnson N, Gaken J, Tamoxifen inhibits the growth of head and neck cancer cells and sensitizes these cells to cis-platin induced-apoptosis: Role of TGF-beta1. Carcinogenesis 23, 1569–75 (2002).

    Article  PubMed  Google Scholar 

  21. Simard M, Zhang W, Hinton DR, Chen TC, Weiss MH, Su YZ, Gopalakrishna R, Law RE, Couldwell WT, Tamoxifen-induced growth arrest and apoptosis in pituitary tumor cells in vitrovia a protein kinase C-independent pathway. Cancer Lett 185, 131–8 (2002).

    Article  PubMed  Google Scholar 

  22. Brandt S, Heller H, Schuster KD, Grote J, Tamoxifen induces sup-pression of cell viability and apoptosis in the human hepatoblas-toma cell line HepG2 via down-regulation of telomerase activity.Liver Int 2 4, 46–54 (2004).

    Article  PubMed  Google Scholar 

  23. Zartman JK, Foreman NK, Donson AM, Fleitz JM, Measurement of tamoxifen-induced apoptosis in glioblastoma by cyto-metric bead analysis of active caspase-3. J Neurooncol 67, 3–7 (2004).

    Article  PubMed  Google Scholar 

  24. Tseng SH, Wang CH, Lin SM, Chen CK, Huang HY, Chen Y, Acti-vation of c-Jun N-terminal kinase 1 and caspase 3 in the tamoxifen-induced apoptosis of rat glioma cells. J Cancer Res Clin Oncol 130(5), 285–93 (2004).

    Article  PubMed  Google Scholar 

  25. Gauduchon J, Gouilleux F, Maillard S, Marsaud V, Renoir MJ, Sola B, The selective estrogen receptor modulator 4-hydroxy tamoxifen induces G1 arrest and apoptosis of multiple myeloma cell lines. Ann N Y Acad Sci 1010, 321–5 (2003).

    Article  PubMed  Google Scholar 

  26. Basu S, Ma R, Basu M, Goodson H, Smith B and Banerjee S, Glycosphingolipid metabolism and signaling in apoptotic cancer cells. In Sphingolipid Metabolizing Enzymes, edited by Haldar DK, Das SK, Research Signpost (in press/2004).

  27. Seki K, Yoshikawa H, Shiiki K, Hamada Y, Akamatsu N, Tasaka K, Cisplatin (CDDP) specifically induces apoptosis via sequen-tial activation of caspase-8,-3 and-6 in osteosarcoma. Cancer Chemother Pharmacol 45, 199–206 (2000).

    Article  PubMed  Google Scholar 

  28. Henkels KM, Turchi JJ, Cisplatin-induced apoptosis proceeds by caspase-3-dependent and-independent pathways in cisplatin-resistant and-sensitive human ovarian cancer cell lines. Cancer Res 59, 3077–83 (1999).

    PubMed  Google Scholar 

  29. Kelley TJ, Moghaddas S, Bose R, Basu S, Inhibition of immunopurified DNA polymerase-alpha from PA-3 prostate tumor cells by platinum (II) antitumor drugs, Cancer Biochem Biophys 13, 135–46 (1993).

    PubMed  Google Scholar 

  30. Bose R, Li D, Kennedy M, Basu S, Facile Formation of cis-platin Nanopeptide Complex of Human DNA Polymerase-alpha Origin. J Chem Soc Commun Royal Soc Chem 1731–32 (1995).

  31. Bose RN, Li D, Yang WW, Basu S, NMR structures of a non-apeptide from DNA binding domain of human polymerase-alpha determined by iterative complete-relaxation-matrix approach. J Biomol Struct Dyn 16, 1075–85 (1999).

    PubMed  Google Scholar 

  32. Basu S, Basu M, (Volume Co-editors), Liposomes methods and protocols in Methods in Molecular Biol (Series Editor: Walker JM) Humana Press, New York (2001).

    Google Scholar 

  33. Cichewicz RH, Kouzi SA, Chemistry, biological activity, and chemotherapeutic potential of betulinic acid for the prevention and treatment of cancer and HIV infection, Med Res Rev 24, 90–114 (2004).

    Article  PubMed  Google Scholar 

  34. Eiznhamer DA, Xu ZQ, Betulinic acid: a promising anticancer candidate, IDrugs 7, 359–73 (2004).

    PubMed  Google Scholar 

  35. Tan Y, Yu R, Pezzuto JM, Betulinic acid-induced programmed cell death in human melanoma cells involves mitogen-activated protein kinase activation, Clin Cancer Res 9, 2866–75 (2003).

    PubMed  Google Scholar 

  36. Kwon HJ, Shim JS, Kim JH, Cho HY, Yum YN, Kim SH, Yu J, Betulinic Acid Inhibits Growth Factor-induced in vitroAngiogenesis via the Modulation of Mitochondrial Function in Endothelial Cells, Jpn J Cancer Res 93, 417–25 (2002).

    PubMed  Google Scholar 

  37. Devita VT, Hellman S, Rosenberg SA, Biologic Therapy of Can-ce r, 2nd edition (1995).

  38. Malisan F, Testi R, GD3 in cellular ageing and apoptosis. Exp Gerontol 37, 1273–82 (2002).

    Article  PubMed  Google Scholar 

  39. Paris R, Morales A, Coll O, Sanchez-Reyes A, Garcia-Ruiz C, Fernandez-Checa JC, Ganglioside GD3 sensitizes human hep-atoma cells to cancer therapy. J Biol Chem 27 7, 49870–6 (2002).

    Article  PubMed  Google Scholar 

  40. Watanabe R, Ohyama C, Aoki H, Takahashi T, Satoh M, Saito S, Hoshi S, Ishii A, Saito M, Arai Y, Ganglioside GM3 overexpression induces apoptosis and reduces malignant potential in murine bladder cancer. Cancer Res 62, 3850–4 (2002).

    PubMed  Google Scholar 

  41. Simon BM, Malisan F, Testi R, Nicotera P, Leist M, Disialogan-glioside GD3is released by microglia and induces oligodendrocyte apoptosis. Cell Death Differ 9, 758–67 (2002).

    Article  PubMed  Google Scholar 

  42. Copani A, Melchiorri D, Caricasole A, Martini F, Sale P, Carnevale R, Gradini R, Sortino MA, Lenti L, De Maria R, Nicoletti F, Beta-amyloid-induced synthesis of the ganglioside GD3 is a requisite for cell cycle reactivation and apoptosis in neurons. J Neurosci 2 2, 3963–8 (2002).

    PubMed  Google Scholar 

  43. Kristal BS, Brown AM, Apoptogenic ganglioside GD3 directly induces the mitochondrial permeability transition. J Biol Chem 274, 23169–75 (1999).

    Article  PubMed  Google Scholar 

  44. Scorrano L, Petronilli V, Di Lisa F, Bernardi P, Commitment to apoptosis by GD3 ganglioside depends on opening of the mito-chondrial permeability transition pore. J Biol Chem 274, 22581–5 (1999).

    Article  PubMed  Google Scholar 

  45. Rippo MR, Malisan F, Ravagnan L, Tomassini B, Condo I, Costan-tini P, Susin SA, Rufini A, Todaro M, Kroemer G, Testi R, GD3 ganglioside directly targets mitochondria in a bcl-2-controlled fashion. Faseb J 14, 2047–54 (2000).

    Article  PubMed  Google Scholar 

  46. Kristal BS, Brown AM, Ganglioside GD3, the mitochondrial per-meability transition, and apoptosis. Ann NY Acad Sci 893, 321–4 (1999).

    PubMed  Google Scholar 

  47. Morales A, Colell A, Mari M, Garcia-Ruiz, Fernandez-Checa JC, Glycosphingolipids and mitochondria: role in apoptosis and dis-ease. Glycoconj J 20(5) (in press/2004).

  48. Kaufman B, Basu S, Roseman S, Isolation of glucosylceramides from yeast (Hansenula ciferri). J Biol Chem 246, 4266–71 (1971).

    PubMed  Google Scholar 

  49. Dickson RC, Lester RL, Metabolism and selected functions of sphingolipids in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1438, 305–21 (1999).

    PubMed  Google Scholar 

  50. Ohashi Y, Tanaka T, Akashi S, Morimoto S, Kishimoto Y, Nagai Y, Squid nerve sphingo-myelin containing an unusual sphingoid base. J Lipid Res 41, 1118–24 (2000).

    PubMed  Google Scholar 

  51. Carter HE, Hendry RA, Mojima S, Stanacer NF, Biochim Biophys Acta 4 5, 402 (1960).

    Article  PubMed  Google Scholar 

  52. Lester RL, Dickson RC, Sphingolipids with inositolphosphate-containing head groups. Adv Lipid Res 26, 253–74 (1993).

    PubMed  Google Scholar 

  53. Sperling P, Heinz E, Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim Biophys Acta 1632, 1–15 (2003).

    PubMed  Google Scholar 

  54. Okazaki T, Bell RM, Hannun YA, Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation. J Biol Chem 264, 19076–80 (1989).

    PubMed  Google Scholar 

  55. Okazaki T, Bielawska A, Bell RM, Hannun YA, Role of ceramide as a lipid mediator of 1 alpha,25-dihydroxyvitamin D3-induced HL-60 cell differentiation. J Biol Chem 26 5, 15823–31 (1990).

    PubMed  Google Scholar 

  56. Pettus BJ, Chalfant CE, Hannun YA, Ceramide in apoptosis: an overview and current perspectives. Biochim Biophys Acta 1585, 114–25 (2002).

    PubMed  Google Scholar 

  57. Tilly JL, Kolesnick RN, Sphingolipids, apoptosis, cancer treatments and the ovary: investigating a crime against female fertility. Biochim Biophys Acta 1585, 135–8 (2002).

    PubMed  Google Scholar 

  58. Cuvillier O, Sphingosine in apoptosis signaling. Biochim Biophys Acta 1585, 153–62 (2002).

    PubMed  Google Scholar 

  59. Radin NS, Killing tumours by ceramide-induced apoptosis: A critique of available drugs. Biochem J 371, 243–56 (2003).

    Article  PubMed  Google Scholar 

  60. Bieberich E, Hu B, Silva J, MacKinnon S, Yu RK, Fillmore H, Broaddus WC, Ottenbrite RM, Synthesis and characterization of novel ceramide analogs for induction of apoptosis in human cancer cells. Cancer Lett 18 1, 55–64 (2002).

    Article  PubMed  Google Scholar 

  61. Basu M, Kelly P, Girzadas M, Li Z, Basu S, Properties of animal ceramide glycanases, Methods Enzymol 311, 287–97 (2000).

    PubMed  Google Scholar 

  62. glycosphingolipids using clam (cercenaria mercenaria) ceramide glycanase. In Methods in Enzymology, edited by Merrill AH, Jr., Hannun YA (Academic Press, NY, 2000), vol. 321, no. B, pp. 196–205.

  63. Basu M, Kelly P, O'Donnell P, Miguel M, Bradley M, Sonnino S, Banerjee S, Basu S, Ceramide glycanase activities in human cancer cells, Biosci Rep 19, 449–60 (1999).

    Article  PubMed  Google Scholar 

  64. Ito M, Yamagata T, Purification and characterization of glycosphingolipid-specific endoglycosidases (endoglycocerami-dases) from a mutant strain of Rhodococcus sp. Evidence for three molecular species of endoglycoceramidase with different speci-ficities, J Biol Chem 264, 9510–9 (1989).

    PubMed  Google Scholar 

  65. Li SC, DeGasperi R, Muldrey JE, Li YT, A unique glycosphingolipid-splitting enzyme (ceramide-glycanase from leech) cleaves the linkage between the oligosaccharide and the ceramide, Biochem Biophys Res Commun 141, 346–52 (1986).

    PubMed  Google Scholar 

  66. Spiegel S, Milstien S, Functions of a new family of sphingosine-1-phosphate receptors, Biochim Biophys Acta 1484, 107–16 (2000).

    PubMed  Google Scholar 

  67. Igarashi Y, Functional roles of sphingosine, sphingosine 1-phosphate, and methylsphingosines: In regard to membrane sph-ingolipid signaling pathways, J Biochem (Tokyo) 122, 1080–7 (1997).

    PubMed  Google Scholar 

  68. Keenan TW, Morre DJ, Basu S, Ganglioside biosynthesis. Concentration of glycosphingolipid glycosyltransferases in Golgi apparatus from rat liver. J Biol Chem 249, 310–5 (1974).

    PubMed  Google Scholar 

  69. Basu S, Kaufman B, Roseman S, Enzymatic synthesis of glu-cocerebroside by a glucosyltransferase from embryonic chicken brain. J Biol Chem 248, 1388–94 (1973).

    PubMed  Google Scholar 

  70. Basu S, Das K, Basu M, Glycosyltransferases in Glycosph-ingolipid Biosynthesis. In Oligosaccharides in Chemistry and Biology-A Comprehensive Handbook, edited by Ernst B, Sinay P, Hart G (Wiley-VCH Verlag GmbH, Germany, 2000), pp. 329–47.

    Google Scholar 

  71. Colell A, Morales A, Fernandez-Checa JC, Garcia-Ruiz C, Ceramide generated by acidic sphingomyelinase contributes to tumor necrosis factor-alpha-mediated apoptosis in human colon HT-29 cells through glycosphingolipids formation. Possible role of gan-glioside GD3. FEBS Lett 526, 135–41 (2002).

    Article  PubMed  Google Scholar 

  72. Kannagi R, Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj J 14, 577–84 (1997).

    Article  PubMed  Google Scholar 

  73. Farmer RW, Richtsmeier WJ, Scher RL, Identification of sialyl Lewis-x in squamous cell carcinoma of the head and neck. Head Neck 20, 726–31 (1998).

    Article  PubMed  Google Scholar 

  74. Ugorski M., Laskowska A, Sialyl lewis A: A tumor-associated carbohydrate antigen involved in adhesion and metastatic potential of cancer cells. Acta Biochimica 49, 303–11 (2002).

    Google Scholar 

  75. Kaufman B, Basu S, Embryonic chicken brain sialyltransferases. Methods in Enzymol 8, 365–8 (1966).

    Google Scholar 

  76. Basu S, Basu M, Dastgheib S, Hawes JW, Biosynthesis and Regulation of Glycosphingolipids. Comprehensive Natural Products Chemistry, edited by Barton D, Nakanishi K, Meth-Cohen O, B. M. Pinto (Pergamon Press, New York, 1999), Vol. 3, pp. 107–28

    Google Scholar 

  77. Higashi H, Basu M, Basu S, Biosynthesis in vitroof disialosyl-neolactotetraosylceramide by a solubilized sialyltransferase from embryonic chicken brain, J Biol Chem 260, 824–8 (1985).

    PubMed  Google Scholar 

  78. Basu M, Hawes JW, Li Z, Ghosh S, Khan FA, Zhang BJ, Basu S, Biosynthesis in vitroof SA-Le x and SA-diLe x by alpha 1-3 fucosyltransferases from colon carcinoma cells and embryonic brain tissues. Glycobiology 1, 527–35 (1991).

    PubMed  Google Scholar 

  79. Basu M, Basu SS, Li Z, Tang H, Basu S, Biosynthesis and regulation of Le(x) and SA-Le(x) glycolipids in metastatic human colon carcinoma cells. Indian J Biochem Biophys 30, 324–32 (1993).

    PubMed  Google Scholar 

  80. Basu M, Khan FA, Das KK, Zhang BJ, Biosynthesis in vitroof core lacto-series glycosphingolipids by N-acetyl-D-glucosaminyltransferases from human colon carcinoma cells, Colo 205. Carbohydr Res 20 9, 261–77 (1991).

    Article  PubMed  Google Scholar 

  81. Basu M, Basu S, Stoffyn A, Stoffyn P, Biosynthesis in vitroof sialyl(alpha 2-3)neolactotetraosylceramide by a sialyltrans-ferase from embryonic chicken brain. J Biol Chem 257, 12765–9 (1982).

    PubMed  Google Scholar 

  82. Basu SS, Basu M, Li Z, Basu S, Characterization of two glycolipid: alpha 2-3sialyltransferases, SAT-3 (CMP-NeuAc:nLcOse4Cer al-pha 2-3sialyltransferase) and SAT-4 (CMP-NeuAc:GgOse4Cer al-pha 2-3sialyltransferase), from human colon carcinoma (Colo 205) cell line, Biochemistry 35, 5166–74 (1996).

    Article  PubMed  Google Scholar 

  83. Basu M, De T, Das KK, Kyle JW, Chon HC, Schaeper RJ, Basu S, Glycosyltransferases Involved in Glycolipid Biosynthesis. In Methods in Enzymol edited by Ginsburg V (Academic Press, New York, 1987), vol. 138, pp. 575–607.

    Google Scholar 

  84. Basu S, Basu M, Basu SS, Biological Specificity of Sialyl-transferases. In Biology of the Sialic Acid s, edited by Abraham Rosenberg, (Plenum Press, New York, 1995) pp. 69–94.

    Google Scholar 

  85. Basu M, Basu S, Enzymatic synthesis of a tetraglycosylceramide by a galactosyltransferase from rabbit bone marrow, J Biol Chem 247, 1489–95 (1972).

    PubMed  Google Scholar 

  86. Basu S, Basu M, Das KK, Daussin F, Schaeper RJ, Banerjee P, Khan FA, Suzuki I, Solubilized glycosyltransferases and biosyn-thesis in vitroof glycolipids, Biochimie 70, 1551–63 (1988).

    Article  PubMed  Google Scholar 

  87. Basu S, Basu M, Liposomes and Glycolipid Glycosyltransferases. In Liposomes Methods and Protocols in Methods in Molecular Biol edited by Basu S, Basu M, Walker JM (Humana Press, New York, 2002) pp. 107–30.

    Google Scholar 

  88. Das KK, Basu M, Basu S, A rapid preparative method for isola-tion of neutral and acidic glycosphingolipids by radial thin-layer chromatography. Anal Biochem 143, 125–34 (1984).

    PubMed  Google Scholar 

  89. Wang L, Ma R, Flavell RA, Choi ME, Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for activation of p38alpha and p38delta MAPK isoforms by TGF-beta 1 in murine mesangial cells. J Biol Chem 277, 47257–62 (2002).

    Article  PubMed  Google Scholar 

  90. Koulov AV, Stucker KA, Lakshmi C, Robinson JP, Smith BD, Detection of apoptotic cells using a synthetic fluorescent sensor for membrane surfaces that contain phosphatidylserine, Cell Death Differ 10, 1357–9 (2003).

    Article  PubMed  Google Scholar 

  91. Fadok VA, Bratton DL, Frasch SC, Warner ML, Henson PM, The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ 5, 551–62 (1998).

    Article  PubMed  Google Scholar 

  92. Eldadah BA, Yakovlev AG, Faden AI, Anewapproach for the elec-trophoretic detection of apoptosis, Nucleic Acids Res 2 4, 4092–3 (1996).

    Article  PubMed  Google Scholar 

  93. Gouaze V, Liu Y-Y, Yu JY, Prickett CS, Giuliano AF, Cabot MC, Blockers of glycolipid metabolism diminishes expression of the multidrug resistance gene (MDR1) and enhances cxhemotherapy sensitivity, FASEB J 18(8), C51.

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  1. Subhash Basu
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  2. Rui Ma
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Basu, S., Ma, R., Boyle, P.J. et al. Apoptosis of human carcinoma cells in the presence of potential anti-cancer drugs: III. Treatment of Colo-205 and SKBR3 cells with: cis-platin, Tamoxifen, Melphalan, Betulinic acid, L-PDMP, L-PPMP, and GD3 ganglioside. Glycoconj J 20, 563–577 (2003). https://doi.org/10.1023/B:GLYC.0000043293.46845.07

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