The opposite effects of doxorubicin on bone marrow stem cells versus breast cancer stem cells depend on glucosylceramide synthase

International Journal of Biochemistry and Cell Biology

Volumn 44, Issue 11, 2012, Pages 1770-1778

  Bhinge, Kaustubh N ^a   Gupta, Vineet ^a   Hosain, Salman B ^a   Satyanarayanajois, Seetharama D ^a   Meyer, Sharon A ^a   Blaylock, Benny ^a   Zhang, Qian Jin ^b   Liu, Yong Yu ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^b XAVIER UNIVERSITY OF LOUISIANA   (United States)

Author keywords

Bone marrow; Breast cancer stem cells; Doxorubicin; Glucosylceramide synthase; Myelosuppression

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CERAMIDE GLUCOSYLTRANSFERASE; DOXORUBICIN; PACLITAXEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER STEM CELL; CELL COUNT; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GLYCOSYLATION; HEMATOPOIETIC STEM CELL; LEUKOCYTE COUNT; MOUSE; NONHUMAN; PROTEIN EXPRESSION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOOD CELL COUNT; BONE MARROW CELLS; BREAST NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; FEMALE; GLUCOSYLTRANSFERASES; HUMANS; MICE; NEOPLASTIC STEM CELLS; PACLITAXEL; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

MUS;

EID: 84864473400     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.06.010     Document Type: Article

References (56)

1. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proceedings of the National Academy of Sciences of the United States of America 100 2003 3983 3988
2. R. Bartsch, and G.G. Steger The role of supportive therapy in the era of modern adjuvant treatment - current and future tools Breast Care (Basel) 4 2009 167 176
3. S.N. Brimble, E.S. Sherrer, E.W. Uhl, E. Wang, S. Kelly, and A.H. Merrill Jr. The cell surface glycosphingolipids SSEA-3 and SSEA-4 are not essential for human ESC pluripotency Stem Cells 25 2007 54 62
4. F.W. Busch, U. Schmittele, and G. Ehninger Toxicity of novel anthracycline derivatives towards normal myeloid bone marrow progenitor cells (CFU-GM) is not increased by verapamil Blut 60 1990 219 222
5. A.M. Calcagno, C.D. Salcido, J.P. Gillet, C.P. Wu, J.M. Fostel, and M.D. Mumau Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics Journal of the National Cancer Institute 102 2010 1637 1652
6. P.J. Carey Drug-induced myelosuppression: diagnosis and management Drug Safety 26 2003 691 706
7. R. Clarke, S. Currier, O. Kaplan, E. Lovelace, V. Boulay, and M.M. Gottesman Effect of P-glycoprotein expression on sensitivity to hormones in MCF-7 human breast cancer cells Journal of the National Cancer Institute 84 1992 1506 1512
8. D. Daniel, and J. Crawford Myelotoxicity from chemotherapy Seminars in Oncology 33 2006 74 85
9. M. Dean, T. Fojo, and S. Bates Tumour stem cells and drug resistance Nature Reviews Cancer 5 2005 275 284
10. L.A. Doyle, W. Yang, L.V. Abruzzo, T. Krogmann, Y. Gao, and A.K. Rishi A multidrug resistance transporter from human MCF-7 breast cancer cells Proceedings of the National Academy of Sciences of the United States of America 95 1998 15665 15670
11. C.M. Fillmore, and C. Kuperwasser Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy Breast Cancer Research 10 2008 R25
12. G. Gasparini, M. Barbareschi, C. Doglioni, P.D. Palma, F.A. Mauri, and P. Boracchi Expression of bcl-2 protein predicts efficacy of adjuvant treatments in operable node-positive breast cancer Clinical Cancer Research 1 1995 189 198
13. M.C. Giarratana, L. Kobari, H. Lapillonne, D. Chalmers, L. Kiger, and T. Cynober Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells Nature Biotechnology 23 2005 69 74
14. A.M. Gonzalez-Angulo, F. Morales-Vasquez, and G.N. Hortobagyi Overview of resistance to systemic therapy in patients with breast cancer Advances in Experimental Medicine and Biology 608 2007 1 22
15. M.A. Goodell, K. Brose, G. Paradis, A.S. Conner, and R.C. Mulligan Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo Journal of Experimental Medicine 183 1996 1797 1806
16. V. Gupta, G.A. Patwardhan, Q.J. Zhang, M.C. Cabot, S.M. Jazwinski, and Y.Y. Liu Direct quantitative determination of ceramide glycosylation in vivo: a new approach to evaluate cellular enzyme activity of glucosylceramide synthase Journal of Lipid Research 51 2010 866 874
17. V. Gupta, Q.J. Zhang, and Y.Y. Liu Evaluation of anticancer agents using flow cytometry analysis of cancer stem cells Methods in Molecular Biology 716 2011 179 191
18. S.I. Hakomori Structure and function of glycosphingolipids and sphingolipids: recollections and future trends Biochimica et Biophysica Acta 1780 2008 325 346
19. J.F. Herman, L.S. Mangala, and K. Mehta Implications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells Oncogene 25 2006 3049 3058
20. L.E. Hood Chemotherapy in the elderly: supportive measures for chemotherapy-induced myelotoxicity Clinical Journal of Oncology Nursing 7 2003 185 190
21. S. Ichikawa, and Y. Hirabayashi Glucosylceramide synthase and glycosphingolipid synthesis Trends in Cell Biology 8 1998 198 202
22. W. Janni, D. Rjosk, B. Strobl, F. Bergauer, F. Linka, and T. Dimpfl Chemotherapy-associated myelosuppression in gynecological oncology Gynakologisch-Geburtshilfliche Rundschau 41 2001 166 173
23. J.J. Jimenez, H.S. Huang, M. Hindahl, F.C. Pearson, and A.A. Yunis Protection from chemotherapy-induced neutropenia by ImuVert American Journal of the Medical Sciences 303 1992 83 85
24. I. Klimanskaya, Y. Chung, S. Becker, S.J. Lu, and R. Lanza Human embryonic stem cell lines derived from single blastomeres Nature 444 2006 481 485
25. Y. Kobayashi, K. Seino, S. Hosonuma, T. Ohara, H. Itamochi, and S. Isonishi Side population is increased in paclitaxel-resistant ovarian cancer cell lines regardless of resistance to cisplatin Gynecologic Oncology 121 2011 390 394
26. N. Kroger, W. Achterrath, S. Hegewisch-Becker, K. Mross, and A.R. Zander Current options in treatment of anthracycline-resistant breast cancer Cancer Treatment Reviews 25 1999 279 291
27. C. Lagadec, E. Vlashi, L. Della Donna, C. Dekmezian, and F. Pajonk Radiation-induced reprogramming of breast cancer cells Stem Cells 30 2012 833 844
28. H.E. Lee, J.H. Kim, Y.J. Kim, S.Y. Choi, S.W. Kim, and E. Kang An increase in cancer stem cell population after primary systemic therapy is a poor prognostic factor in breast cancer British Journal of Cancer 104 2011 1730 1738
29. Y.J. Liang, H.H. Kuo, C.H. Lin, Y.Y. Chen, B.C. Yang, and Y.Y. Cheng Switching of the core structures of glycosphingolipids from globo- and lacto- to ganglio-series upon human embryonic stem cell differentiation Proceedings of the National Academy of Sciences of the United States of America 107 2010 22564 22569
30. Y.Y. Liu, V. Gupta, G.A. Patwardhan, K. Bhinge, Y. Zhao, and J. Bao Glucosylceramide synthase upregulates MDR1 expression in the regulation of cancer drug resistance through cSrc and beta-catenin signaling Molecular Cancer 9 2010 145
31. Y.Y. Liu, T.Y. Han, A.E. Giuliano, and M.C. Cabot Expression of glucosylceramide synthase, converting ceramide to glucosylceramide, confers adriamycin resistance in human breast cancer cells Journal of Biological Chemistry 274 1999 1140 1146
32. Y.Y. Liu, T.Y. Han, A.E. Giuliano, and M.C. Cabot Ceramide glycosylation potentiates cellular multidrug resistance FASEB Journal 15 2001 719 730
33. Y.Y. Liu, G.A. Patwardhan, P. Xie, X. Gu, A.E. Giuliano, and M.C. Cabot Glucosylceramide synthase, a factor in modulating drug resistance, is overexpressed in metastatic breast carcinoma International Journal of Oncology 39 2011 425 431
34. Y.Y. Liu, J.Y. Yu, D. Yin, G.A. Patwardhan, V. Gupta, and Y. Hirabayashi A role for ceramide in driving cancer cell resistance to doxorubicin FASEB Journal 22 2008 2541 2551
35. M. Maugeri-Sacca, P. Vigneri, and R. De Maria Cancer stem cells and chemosensitivity Clinical Cancer Research 17 2011 4942 4947
36. K. Mehta High levels of transglutaminase expression in doxorubicin-resistant human breast carcinoma cells International Journal of Cancer 58 1994 400 406
37. K. Moore, and D. Crom Hematopoietic support with moderately myelosuppressive chemotherapy regimens: a nursing perspective Clinical Journal of Oncology Nursing 10 2006 383 388
38. Z. Nurgalieva, C.C. Liu, and X.L. Du Chemotherapy use and risk of bone marrow suppression in a large population-based cohort of older women with breast and ovarian cancer Medical Oncology 2010
39. G. Patwardhan, V. Gupta, J. Huang, X. Gu, and Y.Y. Liu Direct assessment of P-glycoprotein efflux to determine tumor response to chemotherapy Biochemical Pharmacology 80 2010 72 79
40. G.A. Patwardhan, and Y.Y. Liu Sphingolipids and expression regulation of genes in cancer Progress in Lipid Research 50 2011 104 114
41. G.A. Patwardhan, Q.J. Zhang, D. Yin, V. Gupta, J. Bao, and C.E. Senkal A new mixed-backbone oligonucleotide against glucosylceramide synthase sensitizes multidrug-resistant tumors to apoptosis PLoS One 4 2009 e6938
42. L. Repetto Incidence and clinical impact of chemotherapy induced myelotoxicity in cancer patients: an observational retrospective survey Critical Reviews in Oncology/Hematology 72 2009 170 179
43. D.S. Richardson, and S.A. Johnson Anthracyclines in haematology: preclinical studies, toxicity and delivery systems Blood Reviews 11 1997 201 223
44. C.W. Scharenberg, M.A. Harkey, and B. Torok-Storb The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors Blood 99 2002 507 512
45. A.D. Seidman Systemic treatment of breast cancer. Two decades of progress Oncology (Williston Park) 20 2006 983 990 discussion 991-982, 997-988
46. N. Shafee, C.R. Smith, S. Wei, Y. Kim, G.B. Mills, and G.N. Hortobagyi Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors Cancer Research 68 2008 3243 3250
47. M. Shiota, T. Heike, M. Haruyama, S. Baba, A. Tsuchiya, and H. Fujino Isolation and characterization of bone marrow-derived mesenchymal progenitor cells with myogenic and neuronal properties Experimental Cell Research 313 2007 1008 1023
48. G. Szakacs, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nature Reviews Drug Discovery 5 2006 219 234
49. T. Tanei, K. Morimoto, K. Shimazu, S.J. Kim, Y. Tanji, and T. Taguchi Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers Clinical Cancer Research 15 2009 4234 4241
50. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, and V.S. Marshall Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147
51. J.N. Timmer-Bonte, T.M. de Boo, H.J. Smit, B. Biesma, F.A. Wilschut, and S.A. Cheragwandi Prevention of chemotherapy-induced febrile neutropenia by prophylactic antibiotics plus or minus granulocyte colony-stimulating factor in small-cell lung cancer: a Dutch Randomized Phase III Study Journal of Clinical Oncology 23 2005 7974 7984
52. Y. Wang, V. Probin, and D. Zhou Cancer therapy-induced residual bone marrow injury-Mechanisms of induction and implication for therapy Curruent Cancer Therapy Reviews 2 2006 271 279
53. K. Weilbaecher, I. Weissman, K. Blume, and S. Heimfeld Culture of phenotypically defined hematopoietic stem cells and other progenitors at limiting dilution on Dexter monolayers Blood 78 1991 945 952
54. O.H. Yilmaz, M.J. Kiel, and S.J. Morrison SLAM family markers are conserved among hematopoietic stem cells from old and reconstituted mice and markedly increase their purity Blood 107 2006 924 930
55. S. Zhou, J.J. Morris, Y. Barnes, L. Lan, J.D. Schuetz, and B.P. Sorrentino Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo Proceedings of the National Academy of Sciences of the United States of America 99 2002 12339 12344
56. S. Zhou, J.D. Schuetz, K.D. Bunting, A.M. Colapietro, J. Sampath, and J.J. Morris The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype Nature Medicine 7 2001 1028 1034