Defective acidification in human breast tumor cells and implications for chemotherapy

Journal of Experimental Medicine

Volumn 187, Issue 10, 1998, Pages 1583-1598

  Altan, Nihal ^a   Chen, Yu ^a   Schindler, Melvin ^b   Simon, Sanford M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b Michigan State University   (United States)

Author keywords

Breast cancer; Chemotherapy; Multidrug resistance; pH; Secretion

Indexed keywords

ANTHRACYCLINE ANTIBIOTIC AGENT; BAFILOMYCIN A1; DOXORUBICIN; MONENSIN; VINCA ALKALOID;

ACIDIFICATION; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CELL ORGANELLE; CELL PH; CELLULAR DISTRIBUTION; DRUG DISTRIBUTION; ENDOSOME; HUMAN; HUMAN CELL; LYSOSOME; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; TUMOR CELL LINE;

ANTI-BACTERIAL AGENTS; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL COMPARTMENTATION; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; FEMALE; HUMANS; HYDROGEN-ION CONCENTRATION; IONOPHORES; MACROLIDES; MONENSIN; TUMOR CELLS, CULTURED;

EID: 0032543207     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.10.1583     Document Type: Article

References (76)

1. Biedler, J.L., and H. Riehm. 1970. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic, and cytogenetic studies. Cancer Res. 30:1174-1184.
2. Simon, S.M., and M. Schindler. 1994. Cell biological mechanisms of multidrug resistance in tumors. Proc. Natl. Acad. Sci. USA 91:3497-3504.
3. Ling, V. 1975. Drug resistance and membrane alteration in mutants of mammalian cells. Can. J. Genet. Cytol. 17:503-515.
4. Gottesman, M.M., and I. Pastan. 1993. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62:385-427.
5. Cole, S.P.C., G. Bhardwaj, J.H. Gerlach, J.E. Mackie, C.E. Grant, K.C. Almquist, A.J. Stewart, E.U. Kurz, A.M.V. Duncan, and R.G. Deeley. 1992. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science. 258:1650-1654.
6. De la Torre, M., X.-Y. Hao, R. Larsson, P. Nygren, T. Tsuruo, B. Mannervik, and J. Bergh. 1993. Characterization of four doxorubicin adapted human breast cancer cell lines with respect to chemotherapeutic drug sensitivity, drug resistance associated membrane proteins and glutathione transferases. Anticancer Res. 13:1425-1430.
7. Posada, J.A., E.M. McKeegan, K.F. Worthington, M.J. Morin, S. Jaken, and T.R. Tritton. 1989. Human multidrug resistant KB cells overexpress protein kinase C: involvement in drug resistance. Cancer Commun. 1:285-292.
8. Beck, W.T. 1990. Mechanisms of multidrug resistance in human tumor cells. The roles of P-glycoprotein, DNA topoisomerase II, and other factors. Cancer Treat. Rev. 17(Suppl. A):11-20.
9. Ma, L., and M.S. Center. 1992. The gene encoding vacuolar H(+)-ATPase subunit C is overexpressed in multidrug-resistant HL60 cells. Biochem. Biophys. Res. Commun. 182:675-681.
10. Hindenburg, A.A., J.E. Gervasoni, Jr., S. Krishna, V.J. Stewart, M.L.J. Rosado, K. Bhalla, M.A. Baker, and R.N. Taub. 1989. Intracellular distribution and pharmacokinetics of daunorubicin in anthracycline-sensitive and -resistant HL-60 cells. Cancer Res. 49:4607-4614.
11. Gervasoni, J.E., Jr., S.Z. Fields, S. Krishna, M.A. Baker, M. Rosado, K. Thuraisamy, A.A. Hindenburg, and R.N. Taub. 1991. Subcellular distribution of daunorubicin in P-glycoprotein-positive and -negative drug-resistant cells using laser-assisted confocal microscopy. Cancer Res. 51:4955-4963.
12. Weaver, J.L., P.S. Pine, A. Aszalos, P.V. Schoenlein, S.J. Currier, R. Padmanabhan, and M.M. Gottesman. 1991. Laser scanning and confocal microscopy of daunorubicin, doxorubicin, and rhodamine 123 in multidrug-resistant cells. Exp. Cell Res. 196:323-329.
13. Coley, H.M., W.B. Amos, P.R. Twentyman, and P. Workman. 1993. Examination by laser scanning confocal fluorescence imaging microscopy of the subcellular localisation of anthracyclines in parent and multidrug resistant cell lines. Br. J. Cancer. 67:1316-1323.
14. Rutherford, A.V., and M.C. Willingham. 1993. Ultrastructural localization of daunomycin in multidrug-resistant cultured cells with modulation of the multidrug transporter. J. Histochem. Cytochem. 41:1573-1577.
15. Burns, J.H. 1972. Anal. Profiles Drug Subst. 1:463-480.
16. Beijnen, J.H. 1988. Anal. Profiles Drug Subst. 17:221-258.
17. Mayer, L.D., M.B. Bally, and P.R. Cullis. 1986. Uptake of adriamycin into large unilamellar vesicles in response to a pH gradient. Biochim. Biophys. Acta 857:123-126.
18. Dalmark, M., and H.H. Storm. 1981. A Fickian diffusion transport process with features of transport catalysis. Doxorubicin transport in human red blood cells. J. Gen. Physiol. 78:349-364.
19. Dalmark, M., and E.K. Hoffmann. 1983. Doxorubicin (Adriamycin) transport in Ehrlich ascites tumour cells: comparison with transport in human red blood cells. Scand. J. Clin. Lab. Invest. 43:241-248.
20. Beck, W.T. 1987. The cell biology of multiple drug resistance. Biochem. Pharmacol. 36:2879-2887.
21. Schindler, M., S. Grabski, E. Hoff, and S.M. Simon. 1996. Defective pH regulation of acidic compartments in human breast cancer cells (MCF-7) is normalized in adnamycin-resistant cells (MCF-7adr). Biochemistry. 35:2811-2817.
22. Keizer, H.G., and H. Joenje. 1989. Increased cytosolic pH in multidrug-resistant human lung tumor cells: effect of verapamil. J. Natl. Cancer Inst. 81:706-709.
23. Thiebaut, F., S.J. Currier, J. Whitaker, R.P. Haugland, M.M. Gottesman, I. Pastan, and M.C. Willingham. 1990. Activity of the multidrug transporter results in alkalinization of the cytosol: measurement of cytosolic pH by microinjection of a pH-sensitive dye. J. Histochem. Cytochem. 38:685-690.
24. Hoffman, M.M., L.Y. Wei, and P.D. Roepe. 1996. Are altered pHi and membrane potential in hu MDR 1 transtectants sufficient to cause MDR protein-mediated multidrug resistance? J. Gen. Physiol. 108:295-313.
25. Simon, S.M., D. Roy, and M. Schindler. 1994. Intracellular pH and the control of multidrug resistance. Proc. Natl. Acad. Sci. USA. 91:1128-1132.
26. Millot, C., J.M. Millot, H. Morjani, A. Desplaces, and M. Manfait. 1997. Characterization of acidic vesicles in multidrug-resistant and sensitive cancer cells by acridine orange staining and confocal microspectrofluorometry. J. Histochem. Cytochem. 45:1255-1264.
27. Tycko, B., and F.R. Maxfield. 1982. Rapid acidification of endocytic vesicles containing α2-macroglobulin. Cell. 28:643-651.
28. Yamashiro, D.J., and F.R. Maxfield. 1987. Acidification of morphologically distinct endosomes in mutant and wild-type Chinese hamster ovary cells. J. Cell Biol. 105:2723-2733.
29. Augenbraun, E., F.R. Maxfield, R. St. Jules, W. Setlik, and E. Holtzman. 1993. Properties of acidified compartments in hippocampal neurons. Eur. J. Cell Biol. 61:34-43.
30. Pagano, R.E., O.C. Martin, H.C. Kang, and R.P. Haugland. 1991. A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J. Cell Biol. 113:1267-1279.
31. Ghosh, R.N., and F.R. Maxfield. 1995. Evidence for non-vectorial, retrograde transferrin trafficking in the early endosomes of HEp2 cells. J. Cell Biol. 128:549-561.
32. Schmid, S., R. Fuchs, M. Kielian, A. Helenius, and I. Mellman. 1989. Acidification of endosome subpopulations in wild-type Chinese hamster ovary cells and temperature-sensitive acidification-defective mutants. J. Cell Biol. 108:1291-1300.
33. Lukacs, G.L., O.D. Rotstein, and S. Grinstein. 1990. Phagosomal acidification is mediated by a vacuolar-rype H(+)-ATPase in murine macrophages. J. Biol. Chem. 265:21099-21107.
34. McNeil, P.L., R.F. Murphy, F. Lanni, and D.L. Taylor. 1984. A method for incorporating macromolecules into adherent cells. J. Cell Biol. 98:1556-1564.
35. 2-terminal repeats associate with mouse macrophage lysosomes. J. Cell Biol. 136:1059-1070.
36. Vickers, P.J., R.B. Dickson, R. Shoemaker, and K.H. Cowan. 1988. A multidrug-resistant MCF-7 human breast cancer cell line which exhibits cross-resistance to antiestrogens and hormone-independent tumor growth in vivo. Mol. Endocrinol. 2:886-892.
37. Rabkin, S.W., and P. Sunga. 1987. The effect of doxorubicin (adriamycin) on cytoplasmic microtubule system in cardiac cells. J. Mol. Cell. Cardiol. 19:1073-1083.
38. Zunino, F., R. Gambetta, A. Di Marco, A. Velcich, A. Zaccara, F. Quadrifoglio, and V. Crescenzi. 1977. The interaction of adriamycin and its beta anomer with DNA. Biochim. Biophys. Acta. 476:38-46.
39. Harris, A.L., and D. Hochhauser. 1992. Mechanisms of multidrug resistance in cancer treatment. Acta Oncol. 31:205-213.
40. + pump in parallel to a chloride conductance. J. Cell Biol. 97:1303-1308.
41. Mellman, I., R. Fuchs, and A. Helenius. 1986. Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55:663-700.
42. Kim, J.H., C.A. Lingwood, D.B. Williams, W. Furuya, M.F. Manolson, and S. Grinstein. 1996. Dynamic measurement of the pH ot the Golgi complex in living cells using retrograde transport ot the verotoxin receptor. J. Cell Biol. 134:1387-1399.
43. Presley, J.F., S. Mayor, K.W. Dunn, L.S. Johnson, T.E. McGraw, and F.R. Maxfield. 1993. The End2 mutation in CHO cells slows the exit ot transferrin receptors from the recycling compartment but bulk membrane recycling is unaffected. J. Cell Biol. 122:1231-1241.
44. McGraw, T.E., K.W. Dunn, and F.R. Maxfield. 1993. Isolation of a temperature-sensitive variant Chinese hamster ovary cell line with a morphologically altered endocytic recycling compartment. J. Cell Physiol. 155:579-594.
45. Lipsky, N.G., and R.E. Pagano. 1985. A vital stain for the Golgi apparatus. Science. 228:745-747.
46. Chen, J.W., T.E. Murphy, M.C. Willingham, I. Pastan, and J.T. August. 1985. Identification of two lysosomal membrane glycoproteins. J. Cell Biol. 101:85-95.
47. Vigevani, A., and M.J. Williamson. 1980. Anal. Profiles Drug Subst. 9:245-274.
48. Mayer, L.D., L.C.L. Tai, M.B. Bally, G.N. Mitilenes, R.S. Ginsberg, and P.R. Cullis. 1990. Characterization of liposomal systems containing doxorubicin entrapped in response to pH gradients. Biochim. Biophys. Acta 1025:143-151.
49. Barasch, J., M.D. Gershon, E.A. Nunez, H. Tamir, and Q. Al-Awqati. 1988. Thyrotropin induces the acidification of the secretory granules of parafollicular cells by increasing the chloride conductance of the granular membrane. J. Cell Biol. 107:2137-2147.
50. Zelenin, A.V. 1993. Acridine orange as a probe for molecular and cell biology. In Fluorescent and Luminescent Probes for Biological Activity. W.T. Mason, editor. Academic Press, Inc., San Diego. 83-99.
51. Berglindh, T., D.R. Dibona, S. Ito, and G. Sachs. 1980. Probes of parietal cell function. Am. J. Physiol. 238:G165-G176.
52. Allen, R.D., and A.K. Fok. 1983. Nonlysosomal vesicles (acidosomes) are involved in phagosome acidification in Paramecium. J. Cell Biol. 97:566-570.
53. Kreis, T.E., R. Matteoni, M. Hollinshead, and J. Tooze. 1989. Secretory granules and endosomes show saltatory movement biased to the anterograde and retrograde directions, respectively, along microtubules in AtT20 cells. Eur. J. Cell Biol. 49:128-139.
54. Fagotto, F., and F.R. Maxfield. 1994. Changes in yolk platelet pH during Xenopus laevis development correlate with yolk utilization. A quantitative confocal microscopy study. J. Cell Sci. 107:3325-3337.
55. Soule, H.D., T.M. Maloney, S.R. Wolman, W.D.J. Peterson, R. Brenz, C.M. McGrath, J. Russo, R.J. Pauley, R.F. Jones, and S.C. Brooks. 1990. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50:6075-6086.
56. Murphy, R.F., S. Powers, and C.R. Cantor. 1984. Endosome pH tneasured in single cells by dual fluorescence flow cytometry: rapid acidification of insulin to pH 6. J. Cell Biol. 98:1757-1762.
57. Boscoboinik, D., R.S. Gupta, and R.M. Epand. 1990. Investigation of the relationship between altered intracellular pH and multidrug resistance in mammalian cells. Br. J. Cancer. 61:568-572.
58. Di Virgilio, F., T.H. Steinberg, and S.C. Silverstein. 1990. Inhibition of Fura-2 sequestration and secretion with organic anion transport blockers. Cell Calcium. 11:57-62.
59. Homolya, L., Z. Holló, U.A. Germann, I. Pastan, M.M. Gottesman, and B. Sarkadi. 1993. Fluorescent cellular indicators are extruded by the multidrug resistance protein. J. Biol. Chem. 268:21493-21496.
60. Seksek, O., and J. Bolard. 1996. Nuclear pH gradient in mammalian cells revealed by laser microspectrofluorimetry. J. Cell Sci. 109:257-262.
61. Tartakoff, A.M., and P. Vassalli. 1978. Comparative studies of intracellular transport of secretory proteins. J. Cell Biol. 79:694-707.
62. Maxfield, F.R. 1982. Weak bases and ionophores rapidly and reversibly raise the pH of endocytic vesicles in cultured mouse fibroblasts. J. Cell Biol. 95:676-681.
63. Dröse, S., and K. Altendorf. 1997. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 200:1-8.
64. Feldherr, C.M., E. Kallenbach, and N. Schultz. 1984. Movement of a karyophilic protein through the nuclear pores of oocytes. J. Cell Biol. 99:2216-2222.
65. Barasch, J., B. Kiss, A. Prince, L. Saiman, D. Gruenert, and Q. Al-Awqati. 1991. Defective acidification of intracellular organelles in cystic fibrosis. Nature. 352:70-73.
66. Al-Awqati, Q., J. Barasch, and D.W. Landry. 1989. Proton pumps and chloride channels in secretory vesicles. Soc. Gen. Physiol. Ser. 44:283-294.
67. Baldini, N., K. Scotlandi, M. Serra, T. Shikita, N. Zini, A. Ognibene, S. Santi, R. Ferracini, and N.M. Maraldi. 1995. Nuclear immunolocalization of P-glycoprotein in multidrug-resistant cell lines showing similar mechanisms of doxorubicin distribution. Eur. J. Cell Biol. 68:226-239.
68. Molinari, A., M. Cianfriglia, S. Meschini, A. Calcabrini, and G. Arancia. 1994. P-glycoprotein expression in the Golgi apparatus of multidrug-resistant cells. Int. J. Cancer 59:789-795.
69. Ehring, G.R., Y.V. Osipchuk, and M.D. Cahalan. 1994. Swelling-activated chloride channels in multidrug-sensitive and-resistant cells. J. Gen. Physiol. 104:1129-1161.
70. Gill, D.R., S.C. Hyde, C.F. Higgins, M.A. Valverde, G.M. Mintenig, and F.V. Sepúlveda. 1992. Separation of drug transport and chloride channel functions of the human multidrug resistance P-glycoprotein. Cell. 71:23-32.
71. Hainsworth, A.H., R.M. Henderson, M.E. Hickman, S.B. Hladky, T. Rowlands, P.R. Twentyman, and M.A. Barrand. 1996. Hypotonicity-induced anion fluxes in cells expressing the multidrug-resistance-associated protein, MRP. Pflugers Archiv. - Eur. J. Physiol. 432:234-240.
72. Hardy, S.P., H.R. Goodfellow, M.A. Valverde, D.R. Gill, F.V. Sepúlveda, and C.F. Higgins. 1995. Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels. EMBO (Eur. Mol. Biol. Organ.) J. 14:68-75.
73. Valverde, M.A., M. Díaz, F.V. Sepúlveda, D.R. Gill, S.C. Hyde, and C.F. Higgins. 1992. Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature. 355:830-833.
74. Dong, Y., G. Chen, G.E. Durán, K. Kouyama, A.C. Chao, B.I. Sikic, S.V. Gollapudi, S. Gupta, and P. Gardner. 1994. Volume-activated chloride current is not related to P-glycoprotein overexpression. Cancer Res. 54:5029-5032.
75. Mukhopadhyay, K., P.K. Parrack, and B. Bhattacharyya. 1990. The carboxy terminus of the alpha subunit of tubulin regulates its interaction with colchicine. Biochemistry. 29:6845-6850.
76. Ringel, I., and S.B. Horwitz. 1991. Effect of alkaline pH on taxol-microtubule interactions. J. Pharmacol. Exp. Ther. 259:855-860.