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Apoptosis of human breast carcinoma cells in the presence of cis-platin and L-/D-PPMP: IV. Modulation of replication complexes and glycolipid: Glycosyltransferases

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Abstract

Apoptosis of human breast carcinoma cells (SKBR-3, MCF-7, and MDA-468) has been observed after treatment of these cells with anti-cancer drug cis-platin and glycosphingolipid biosynthesis inhibitor L- and D-PPMP, respectively. These drugs initiated apoptosis in a dose-dependent manner as measured by phenotypic morphological changes, by binding of a fluorescent phophatidyl serine-specific dye (PSS-380) onto the outer leaflet of the cell membranes, and by activation of caspases, −3, −8, and −9. It was observed that in two hours very little apoptotic process had started but predominant biochemical changes occurred after 6 h. DNA degradation started after 24 hours of drug treatment. However, very little is known about the stability of the ‘`Replication Complexes’’ during the apoptotic process. DNA helicases are motor proteins that catalyze the melting of genomic DNA during its replication, repair, and recombination processes. Previously, DNA helicase-III was characterized as a component of the replication complexes isolated from embryonic chicken brains as well as breast and colon carcinoma cells. Helicase activities were measured by a novel method (ROME assay), and DNA polymerase-α activities were determined by regular chain extension of the nicked ACT-DNA, by determining values obtained from +/− aphidicolin-treated incubation mixtures. In all three breast carcinoma cell lines, a common trend was observed: a decrease of activities of DNA polymerase-α and Helicase III. A sharp decrease of activities of the glycolipid sialyltransferases: SAT-2 (CMP-NeuAc; GD3 α2-8 sialyltransferase) and SAT-4 (CMP-NeuAc: GM1a α2-3 sialyltransferase) was observed in the apoptotic carcinoma cells treated with L-PPMP compared with cis-platin.

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References

  1. Wyllie, A.H.: Apoptosis: cell death in tissue regulation. J. Pathol. 153, 313–316 (1987)

    Article  CAS  PubMed  Google Scholar 

  2. Arends, M.J., Wyllie, A.H.: Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32, 223–254 (1991)

    CAS  PubMed  Google Scholar 

  3. Wajant, H.: The Fassignaling pathway: more than a paradigm. Science, 296, 1635–6 (2002)

    Article  CAS  PubMed  Google Scholar 

  4. Strasser, A., O’Connor, L., Dixit, V.M.: Apoptosis signaling. Annu. Rev. Biochem. 69, 217–245 (2000)

    Article  CAS  PubMed  Google Scholar 

  5. Couldwell, W.T., Hinton, D.R., He, S., Chen, T.C., Sebat, I., Weiss, M.H., Law, R.E.: Protein kinaseC inhibitors induce apoptosis in human malignant glioma cell lines. FEBS Lett. 345, 43–46 (1994)

    Article  CAS  PubMed  Google Scholar 

  6. Issandou, M., Faucher, C., Bayard, F., Darbon, J.M.: Opposite effectsof tamoxifen on in vitro protein kinase C activity and endogenous protein phosphorylation in intact MCF-7 cells. Cancer Res. 50, 5845–5850 (1990)

    CAS  PubMed  Google Scholar 

  7. Pisha, E., Chai, H., Lee, I.S., Chagwedera, T.E., Farnsworth, N.R., Cordell, G.A., Beecher, C.W., Fong, H.H., Kinghorn, A.D., Brown, D.M., 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  CAS  PubMed  Google Scholar 

  8. Ritke, M.K., Rusnak, J.M., Lazo, J.S., Allan, W.P., Dive, C., Heer, S., Yalowich, J.C.: Differential inductionof etoposide-mediated apoptosis in human leukemia HL-60 and K562 cells. Mol. Pharmacol. 46, 605–611 (1994)

    CAS  PubMed  Google Scholar 

  9. Schmidt, M.L., Kuzmanoff, K.L., Ling-Indeck, L., Pezzuto, J.M.: Betulinic acid induces apoptosis in human neuroblastoma cell lines. Eur. J. Cancer 33, 2007–2010 (1997)

    Article  CAS  PubMed  Google Scholar 

  10. Cifone, M.G., Roncaioli, P., De Maria, R., Camarda, G., Santoni, A., Ruberti, G., Testi, R.: Multiple pathwaysoriginate at the Fas/APO-1 (CD95) receptor: sequential involvement of phosphatidylcholine-specific phospholipase C and acidic sphingomyelinase in the propagation of the apoptotic signal. Embo. J. 14, 5859–5868 (1995)

    CAS  PubMed  Google Scholar 

  11. Bharti, A.C., Singh, S.M.: Induction ofapoptosis in bone marrow cells by gangliosides produced by a T cell lymphoma. Immunol. Lett. 72, 39–48 (2000)

    Article  CAS  PubMed  Google Scholar 

  12. Colell, A., Morales, A., Fernandez-Checa, J.C., Garcia-Ruiz, C.: Ceramide generatedby acidic sphingomyelinase contributes to tumor necrosis factor-alpha-mediated apoptosis in human colon HT-29 cells through glycosphingolipids formation. Possible role of ganglioside GD3. FEBS Lett. 526, 135–141 (2002)

    Article  CAS  PubMed  Google Scholar 

  13. Malisan, F., Testi, R.: GD3 in cellular ageing and apoptosis. Exp. Gerontol. 37, 1273–1282 (2002)

    Article  CAS  PubMed  Google Scholar 

  14. Paris, R., Morales, A., Coll, O., Sanchez-Reyes, A., Garcia-Ruiz, C., Fernandez-Checa, J.C.: Ganglioside GD3 sensitizes human hepatoma cells to cancer therapy. J. Biol. Chem. 277, 49870–49876 (2002)

    Article  CAS  PubMed  Google Scholar 

  15. Watanabe, R., Ohyama, C., Aoki, H., Takahashi, T., Satoh, M., Saito, S., Hoshi, S., Ishii, A., Saito, M., Arai, Y.: Ganglioside G(M3) overexpression induces apoptosis and reduces malignant potential in murine bladder cancer. Cancer Res. 62, 3850–3854 (2002)

    CAS  PubMed  Google Scholar 

  16. Simon, B.M., Malisan, F., Testi, R., Nicotera, P., Leist, M.: Disialoganglioside GD3 is released by microglia and induces oligodendrocyte apoptosis. Cell. Death. Differ. 9, 758–767 (2002)

    Article  CAS  PubMed  Google Scholar 

  17. Copani, A., Melchiorri, D., Caricasole, A., Martini, F., Sale, P., Carnevale, R., Gradini, R., Sortino, M.A., 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. 22, 3963–3968 (2002)

    CAS  PubMed  Google Scholar 

  18. Kristal, B.S., Brown, A.M.: Apoptogenic gangliosideGD3 directly induces the mitochondrial permeability transition. JBiol. Chem. 274, 23169–23175 (1999)

    Article  CAS  Google Scholar 

  19. Scorrano, L., Petronilli, V., Di Lisa, F., Bernardi, P.: Commitment toapoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore. J. Biol. Chem. 274, 22581–22585 (1999)

    Article  CAS  PubMed  Google Scholar 

  20. Rippo, M.R., Malisan, F., Ravagnan, L., Tomassini, B., Condo, I., Costantini, P., Susin, S.A., Rufini, A., Todaro, M., Kroemer, G., Testi, R.: GD3 ganglioside directly targets mitochondria in a bcl-2-controlled fashion. Faseb. J. 14, 2047–2054 (2000)

    Article  CAS  PubMed  Google Scholar 

  21. Kristal, B.S., Brown, A.M.: Ganglioside GD3, the mitochondrial permeability transition, and apoptosis. Ann. N. Y. Acad. Sci. 893, 321–324 (1999)

    Article  CAS  PubMed  Google Scholar 

  22. Morales, A., Colell, A., Mari, M., Garcia-Ruiz, C., Fernandez-Checa, J.C.: Glycosphingolipids andmitochondria: role in apoptosis and disease. Glycoconj. J. 20, 579–588 (2004)

    Article  CAS  PubMed  Google Scholar 

  23. Ma, R., Koulov, A., Moulton, C., Basu, M., Banerjee, S., Goodson, H., Basu, S.: Apoptosis ofhuman breast carcinoma cells in the presence of disialosyl gangliosides: II. Treatment of SKBR3 cells with GD3 and GD1b gangliosides. Glycoconj. J. 20, 319–330 (2004)

    Article  CAS  PubMed  Google Scholar 

  24. Hannun, Y.A., Luberto, C., Argraves, K.M.: Enzymes ofsphingolipid metabolism: from modular to integrative signaling. Biochemistry 40, 4893–4903 (2001)

    Article  CAS  PubMed  Google Scholar 

  25. Pettus, B.J., Chalfant, C.E., Hannun, Y.A.: Ceramide inapoptosis: an overview and current perspectives. Biochim. Biophys. Acta. 1585, 114–125 (2002)

    CAS  PubMed  Google Scholar 

  26. Tilly, J.L., Kolesnick, R.N.: Sphingolipids, apoptosis, cancer treatments and the ovary: investigating a crime against female fertility. Biochim. Biophys. Acta. 1585, 135–138 (2002)

    CAS  PubMed  Google Scholar 

  27. Cuvillier, O.: Sphingosine inapoptosis signaling. Biochim. Biophys. Acta. 1585, 153–162 (2002)

    CAS  PubMed  Google Scholar 

  28. Radin, N.S.: Killing tumoursby ceramide-induced apoptosis: a critique of available drugs. Biochem. J. 371, 243–256 (2003)

    Article  CAS  PubMed  Google Scholar 

  29. Bieberich, E., Hu, B., Silva, J., MacKinnon, S., Yu, R.K., Fillmore, H., Broaddus, W.C., Ottenbrite, R.M.: Synthesis andcharacterization of novel ceramide analogs for induction of apoptosis in human cancer cells. Cancer Lett. 181, 55–64 (2002)

    Article  CAS  PubMed  Google Scholar 

  30. Okazaki, T., Bell, R.M., Hannun, Y.A.: Sphingomyelin turnoverinduced by vitamin D3 in HL-60 cells. Role in cell differentiation. J. Biol. Chem. 264, 19076–19080 (1989)

    CAS  PubMed  Google Scholar 

  31. Okazaki, T., Bielawska, A., Bell, R.M., Hannun, Y.A.: Role ofceramide as a lipid mediator of 1 alpha, 25-dihydroxyvitamin D3-induced HL-60 cell differentiation. J. Biol. Chem. 265, 15823–15831 (1990)

    CAS  PubMed  Google Scholar 

  32. Basu, S., Ma, R., Mikulla, B., Bradley, M., Moulton, C., Basu, M., Banerjee, S., Inokuchi, J.: Apoptosis ofhuman 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. 20, 157–168 (2004)

    Article  CAS  PubMed  Google Scholar 

  33. Kolesnick, R.N.: Sphingomyelin andderivatives as cellular signals. Prog. Lipid. Res. 30, 1–38 (1991)

    Article  CAS  PubMed  Google Scholar 

  34. Basu, M., Kelly, P., Girzadas, M., Li, Z., Basu, S.: Properties ofanimal ceramide glycanases. Methods. Enzymol. 311, 287–297 (2000)

    CAS  PubMed  Google Scholar 

  35. Dastgheib, S., Basu, S.S., Li, Z., Basu, M., Basu, S.: Analyses ofglycosphingolipids using clam, Mercenaria mercenaria, ceramide glycanase. Methods. Enzymol. 312, 196–205 (2000)

    CAS  PubMed  Google Scholar 

  36. Basu, M., Kelly, P., O’Donnell, P., Miguel, M., Bradley, M., Sonnino, S., Banerjee, S., Basu, S.: Ceramide glycanaseactivities in human cancer cells. Biosci. Rep. 19, 449–460 (1999)

    Article  CAS  PubMed  Google Scholar 

  37. Spiegel, S., Milstien, S.: Functions ofa new family of sphingosine-1-phosphate receptors. Biochim. Biophys. Acta. 1484, 107–116 (2000)

    CAS  PubMed  Google Scholar 

  38. Igarashi, Y.: Functional rolesof sphingosine, sphingosine 1-phosphate, and methylsphingosines: in regard to membrane sphingolipid signaling pathways. J. Biochem. (Tokyo) 122, 1080–1087 (1997)

    CAS  Google Scholar 

  39. Kerr, J.F., Wyllie, A.H., Currie, A.R., Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26, 239–257 (1972)

    CAS  PubMed  Google Scholar 

  40. Cohen, G., Sun, X., Fearnhead, H., MacFarlane, M., Brown, D., Snowden, R., Dinsale, D.: Formation oflarge molecular weight fragments of DNA is a key committed step of apoptosis in thymocytes. J. Immunol., 153, 507–516 (1994)

    CAS  PubMed  Google Scholar 

  41. Martin, S., Reutelingsperger, C., McGahon, A., Rader, J., Schie, R.v., LaFace, D., Green, D.: Early redistributionof plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545–1556 (1995)

    Article  CAS  PubMed  Google Scholar 

  42. Martin, S., Green, D.: Protease activationduring apoptosis: death by a thousand cuts? Cell. 82, 349–352 (1995)

    Article  CAS  PubMed  Google Scholar 

  43. Wyllie, A.: Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555–556 (1980)

    Article  CAS  PubMed  Google Scholar 

  44. Liu, X., Zou, H., Slaughter, C., Wang, X.: DFF, a heterodimeric protein that functions downstream of Caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175–184 (1997)

    Article  CAS  PubMed  Google Scholar 

  45. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., Nagata, S., A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43–50 (1998)

    Article  CAS  PubMed  Google Scholar 

  46. Halenbeck, R., MacDonald, H., Roulston, A., Chen, T., Conroy, L., Williams, L., CPAN, a human nuclease regulated by the caspase-sensitive inhibitor DFF45. Curr. Biol. 8, 537–540 (1998)

    Article  CAS  PubMed  Google Scholar 

  47. Seki, K., Yoshikawa, H., Shiiki, K., Hamada, Y., Akamatsu, N., Tasaka, K.: Cis-platin (CDDP) specifically induces apoptosis via sequential activation of Caspase-8, -3 and -6 in osteosarcoma. Cancer Chemother Pharmacol. 45, 199–206 (2000)

    Article  CAS  PubMed  Google Scholar 

  48. Henkels, K.M., Turchi, J.J., Cis-platin-induced apoptosis proceeds by Caspase-3-dependent and – independent pathways in cis-platin-resistant and -sensitive human ovarian cancer cell lines. Cancer Res. 59, 3077–3083 (1999)

    CAS  PubMed  Google Scholar 

  49. 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-betal. Carcinogenesis 23, 1569–1575 (2002)

    Article  CAS  PubMed  Google Scholar 

  50. Rahmouni, A., Leng, M.: Reaction ofnucleic acids with cis-diamminedichloroplatinum (II): interstrand cross-links. Biochemistry 26, 7229–7234 (1987)

    Article  CAS  PubMed  Google Scholar 

  51. Kelley, T.J., Moghaddas, S., Bose, R., Basu, S.: Inhibition ofimmunopurified DNA polymerase-alpha from PA-3 prostate tumor cells by platinum (II) antitumor drugs. Cancer Biochem. Biophys. 13, 135–146 (1993)

    CAS  PubMed  Google Scholar 

  52. Bose, R., Li, D., Kennedy, M., Basu, S.: Facile Formationof cis-Platin Nonapeptide Complex of Human DNA Polymerase-alpha Origin. J. Chem. Soc. Commun. Royal Soc. Chem. 1731–1732 (1995)

  53. Bose, R.N., Li, D., Yang, W.W., Basu, S.: NMR structuresof a nonapeptide from DNA binding domain of human polymerase-alpha determined by iterative complete-relaxation-matrix approach. J. Biomol. Struct. Dyn. 16, 1075–1085 (1999)

    CAS  PubMed  Google Scholar 

  54. Hiraishi, K., Suzuki, K., Hakomori, S., Adachi, M., Le (y) antigen expression is correlated with apoptosis (programmed cell death). Glycobiology 3, 381–390 (1993)

    CAS  PubMed  Google Scholar 

  55. Basu, S., Ma, R., Boyle, P.J., Mikulla, B., Bradley, M., Smith, B., Basu, M., Banerjee, S.: Apoptosis ofhuman 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 (2004)

    Article  CAS  PubMed  Google Scholar 

  56. Boubelik, M., Floryk, D., Bohata, J., Draberova, L., Macak, J., Smid F, Draber, P.: Lex glycosphingolipids-mediated cell aggregation. Glycobiology 8, 139–146 (1998)

    Article  CAS  PubMed  Google Scholar 

  57. Koulov, A.V., Stucker, K.A., Lakshmi, C., Robinson, J.P., Smith, B.D.: Detection ofapoptotic cells using a synthetic fluorescent sensor for membrane surfaces that contain phosphatidylserine. Cell. Death. Differ. 10, 1357–1359 (2003)

    Article  CAS  PubMed  Google Scholar 

  58. Basu, M., De, T., Das, K.K., Kyle, J.W., Chon, H.C., Schaeper, R.J., Basu, S.: Glycolipids. Methods. Enzymol. 138, 575–607 (1987)

    CAS  PubMed  Google Scholar 

  59. Boyle, P.J.: Characterization of DNA Helicase-III in Replication Complexes Isolated from Embryonic Chicken Brain and Breast Carcinoma Cells, in Department of Chemistry and Biochemistry. 2005, University of Notre Dame: Notre Dame, IN

    Google Scholar 

  60. Mullen, O.L., Dodd, M.C., Minton, J.P.: Evaluation ofdye exclusion and colony inhibition techniques for detection of polyoma-specific, cell-mediated immunity. J. Natl. Cancer Inst. 54, 229–231 (1975)

    CAS  PubMed  Google Scholar 

  61. Porter, A.G., Janicke, R.U.: Emerging rolesof Caspase-3 in apoptosis. Cell. Death. Differ. 6, 99–104 (1999)

    Article  CAS  PubMed  Google Scholar 

  62. Kumar, S.: Mechanisms mediatingcaspase activation in cell death. Cell. Death. Differ. 6, 1060–1066 (1999)

    Article  CAS  PubMed  Google Scholar 

  63. Nunez, G., Benedict, M.A., Hu, Y., Inohara, N., Caspases: the proteases of the apoptotic pathway. Oncogene 17, 3237–3245 (1998)

    Article  PubMed  Google Scholar 

  64. Hearps, A.C., Burrows, J., Connor, C.E., Woods, G.M., Lowenthal, R.M., Ragg, S.J.: Mitochondrial cytochromec release precedes transmembrane depolarisation and Caspase-3 activation during ceramide-induced apoptosis of Jurkat T cells. Apoptosis 7, 387–394 (2002)

    Article  CAS  PubMed  Google Scholar 

  65. Chandra, J., Kaufmann, S.H.: Apoptotic pathways in cancer progression and treatment in Signal Transduction and Human Disease, 143–170 (2003); John Wiley and Sons, New Jersey Ekert, P.G., Silke, J., Vaux, D.L.: Caspase inhibitors. Cell. Death. Differ. 6, 1081–1086 (1999)

    Article  CAS  Google Scholar 

  66. Stennicke, H.R., Salvesen, G.S.: Catalytic propertiesof the caspases. Cell. Death. Differ. 6, 1054–1059 (1999)

    Article  CAS  PubMed  Google Scholar 

  67. Thornberry, N.A., Lazebnik, Y.: Caspases: enemies within. Science 281, 1312–1316 (1998)

    Article  CAS  PubMed  Google Scholar 

  68. Volckova, E., Dudones, L.P., Bose, R.N.: HPLC determinationof binding of cis-platin to DNA in the presence of biological thiols: implications of dominant platinum-thiol binding to its anticancer action. Pharm. Res. 19, 124–131 (2002)

    Article  CAS  PubMed  Google Scholar 

  69. Tuteja, N., Rahma, K., Tuteja, R., Ochem, A., Skopac, D., Falaschi, A.: DNA helicase III from HeLa cells: an enzyme that acts preferentially on partially unwound DNA duplexes. Nucleic Acids Res. 20, 5329–5337 (1992)

    CAS  PubMed  Google Scholar 

  70. Peyrone, M.: Ueber dieEinwirkung des Ammoniaks auf Platinchlorur. Ann. Chem. Pharm. 51, 1–29 (1844)

    Google Scholar 

  71. Rosenberg, B., Vancamp, L., Krigas, T.: Inhibition Of Cell Division In Escherichia Coli By Electrolysis Products From A Platinum Electrode. Nature 205, 698– 699 (1965)

    CAS  PubMed  Google Scholar 

  72. Rosenberg, B., VanCamp, L., Trosko, J.E., Mansour, V.H., Platinum compounds: a new class of potent antitumour agents. Nature 222, 385–386 (1969)

    CAS  PubMed  Google Scholar 

  73. Pinto, A.L., Lippard, S.J.: Binding ofthe antitumor drug cis-diamminedichloroplatinum (II) (cis-platin) to DNA. Biochim. Biophys. Acta. 780, 167–180 (1985)

    CAS  PubMed  Google Scholar 

  74. Bose, R.N., Li, D., Kennedy, M., Basu, S.: Facile Formationof cis-platin Nonapeptide Complex of Human DNA Polymerase-a Origin. J. Chem. Soc. Commun. Royal Soc. Chem. 1731–1732 (1995)

  75. Volckova, E., Evanics, F., Yang, W.W., Bose, R.N.: Unwinding of DNA polymerases by the antitumor drug, cis-diamminedichloroplatinum (II). Chem. Commun. (Camb), 1128–1129 (2003)

  76. Rossi, D., Gaidano, G.: Messengers ofcell death: apoptotic signaling in health and disease. Haematologica 88, 212–218 (2003)

    CAS  PubMed  Google Scholar 

  77. Fredman, P., Nilsson, O., Svennerholm, L., Myrvold, H., Persson, B., Pettersson, S., Holmgren, J., Lindholm, L.: Colorectal carcinomashave a characteristic ganglioside pattern. Med. Biol. 61, 45–48 (1983)

    CAS  PubMed  Google Scholar 

  78. Wikstrand, C.J., Fredman, P., McLendon, R.R., Svennerholm, L., Bigner, D.D.: Altered expressionof ganglioside phenotypes of human gliomas in vivo and in vitro. Mol. Chem. Neuropathol. 21, 129–138 (1994)

    Article  CAS  PubMed  Google Scholar 

  79. Thomas, C.P., Buronfosse, A., Fertil, B., Portoukalian, J.: Surface expressionof GD3 disialogangliosides in human melanoma cells is correlated to both metastatic potential in vivo and radiosensitivity in vitro. C. R. Acad. Sci. III, 318, 1233–1238 (1995)

    CAS  PubMed  Google Scholar 

  80. Marquina, G., Waki, H., Fernandez, L.E., Kon, K., Carr, A., Valiente, O., Perez, R., Ando, S.: Gangliosides expressedin human breast cancer. Cancer Res. 56, 5165–5171 (1996)

    CAS  PubMed  Google Scholar 

  81. Magnani, J.L., Nilsson, B., Brockhaus, M., Zopf, D., Steplewski, Z., Koprowski, H., Ginsburg, V.: A monoclonalantibody-defined antigen associated with gastrointestinal cancer is a ganglioside containing sialylated lacto-N-fucopentaose II. J. Biol. Chem. 257, 14365–14369 (1982)

    CAS  PubMed  Google Scholar 

  82. Kannagi, R., Izawa, M., Koike, T., Miyazaki, K., Kimura, N.: Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci. 95, 377–384 (2004)

    Article  CAS  PubMed  Google Scholar 

  83. Zeisig, R., Stahn, R., Wenzel, K., Behrens, D., Fichtner, I.: Effect ofsialyl Lewis X-glycoliposomes on the inhibition of E-selectin-mediated tumour cell adhesion in vitro. Biochim. Biophys. Acta. 1660, 31–40 (2004)

    CAS  PubMed  Google Scholar 

  84. Magnani, J.L.: The discovery, biology, and drug development of sialyl Lea and sialyl Lex. Arch. Biochem. Biophys. 426, 122–131 (2004)

    Article  CAS  PubMed  Google Scholar 

  85. Basu S.: The serendipity of ganglioside biosynthesis: pathways to CARS and HY-CARS glycosyltrnsferases. Glycobiology 1, 469–475 (1991)

    CAS  PubMed  Google Scholar 

  86. Basu, M., Hawes, J., Li, Z., Ghosh, S., Khan, F.A., Zhang, B.J., Basu, S., Basu, M.: Biosynthesis in vitro of SA-LeX and SA-diLeX by al-3 fucosyltransferases from colon carcinoma and embryonic brain tissues. Glycobiology 1, 527–535 (1991)

    CAS  PubMed  Google Scholar 

  87. Basu, S., Basu, M., Dastgheib, S., Hawes, J.W.: Biosynthesis andregulation of glycosphingolipids in “Comprehensive Natural Products Chemistry” (eds. D. Barton, K. Nakanishi, O. Meth-Cohen, and B.M. Pinto), Vol-3. Pergamon Press, New York 107–128 (1999)

    Google Scholar 

  88. Basu, S., Kaufman, B., Roseman, S.: Conversion ofTay-Sachs ganglioside to monosialoganglioside by brain uridine diphosphoate D-galactose:glycolipid galactosyltransferase. J. Biol. Chem. 240, 4114–4117 (1965)

    Google Scholar 

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  1. Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN, 46556, USA

    Patrick J. Boyle, Rui Ma & Subhash Basu

  2. Plant and Molecular Biology, International Center for Genetic Engineering & Biotechnology (ICGEB), New Delhi, 110067, India

    Narendra Tuteja

  3. Department of Cancer Biology, Cleveland Clinic Foundation, Cleveland, OH, 44129, USA

    Sipra Banerjee

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  1. Patrick J. Boyle
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Boyle, P.J., Ma, R., Tuteja, N. et al. Apoptosis of human breast carcinoma cells in the presence of cis-platin and L-/D-PPMP: IV. Modulation of replication complexes and glycolipid: Glycosyltransferases. Glycoconj J 23, 175–187 (2006). https://doi.org/10.1007/s10719-006-7923-5

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