Multidrug Resistance: A Novel Class of Membrane-Associated Transport Proteins is Identified

References

• Moscow J. A., Cowan K. H. Multidrug resistance. J Natl Cancer Inst 1988; 80: 14–20
   PubMed Web of Science ®Google Scholar
• Endim J. A., Ling V. The biochemistry of P-glywprotein-mediated multidrug resistance. Annu Rev Biochem 1989; 58: 137–171
   PubMed Web of Science ®Google Scholar
• Bider J. L., Riehm H. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic and cytogenetic studies. Cancer Res 1970; 30: 1174–1184
   PubMed Web of Science ®Google Scholar
• Ling V., Thompson L. H. Reduced permeability in CHO cells as a mechanism for resistance to colchicine. J Cell Physiol 1974; 83: 103–111
   PubMed Web of Science ®Google Scholar
• Fojo A., Akiyama S., Gottesman M. M., et al. Reduced drug accumulation in multiply drug resistant human KB carcinoma cell lines. Cancer Res 1985; 45: 3002–3007
   PubMed Web of Science ®Google Scholar
• Lemontt J. F., Azzaria M., Gros P. Increased mdr gene expression and decreased drug accumulation in multidrug-resistant human melanoma cells. Cancer Res 1988; 48: 6348–6353
   PubMed Web of Science ®Google Scholar
• Dano K. Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochem Biophys Acta 1973; 323: 446–483
   Google Scholar
• Skovsgaard T. Mechanism of cross-resistance between vincristine and daunorubicin in Ehrlich ascites tumor cells. Cancer Res 1978; 39: 4722–4721
   Google Scholar
• Juliano R. L., Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochem Biophys Acta 1976; 455: 152–162
   PubMed Web of Science ®Google Scholar
• Beck W. T., Mueller T. J., Tanzer L. R. Altered surface membrane glycoproteins in vinca alkaloid-resistant human leukemic lymphoblasts. Cancer Res 1979; 39: 2070–2076
   PubMed Web of Science ®Google Scholar
• Gros P., Ben-Neriah Y., Croop J. M., et al. Isolation and expression of a complementary DNA that confers multidrug resistance. Nature 1986; 323: 728–731
   PubMed Web of Science ®Google Scholar
• Ueda K., Cardarelli C., Gotteaman M. M., et al. Expression of a full-length cDNA clone for the human mdr1 gene confers resistance to colchichc, doxorubicin and vinblastine. Roc Natl Acad Sci (USA) 1987; 84: 3004–3008
   PubMed Web of Science ®Google Scholar
• Hammond J., Johnstone R. UT, Gros P. Enhanced efflux of 3H-vinblastine from Chinese hamster ovary cells transfecled with a full-length complementary DNA clone for the mouse mdr1 gene. Cancer Res 1989; 49: 3867–3871
   PubMed Web of Science ®Google Scholar
• Schurr E., Raymond M., Bell J., et al. Characterization of the multidrug resistance protein expressed in cell clones stably transfected with the mouse mdr1 cDNA. Cancer Res 1989; 49: 2729–2734
   PubMed Web of Science ®Google Scholar
• Greenberger L. M., Lothstein L., Williams S. S., et al. Distinct P-glyooprotein precursors are ovgproduced in independently isolated drug-resistant cell lines. Proc Natl Acad Sci (USA) 1988; 85: 3762–3766
   PubMed Web of Science ®Google Scholar
• Cornwell M. M., Tsunu T., Goamnan M. M., et al. ATP-biding properties of P-glycoprotein from multidrug resistant KB cells. FASEB J 1987; 1: 51–54
   PubMed Web of Science ®Google Scholar
• Cornwell M. M., Safa A. R., Felsted R., et al. Membrane vesicles from multidrug resistant cancer cells contain a specific 150–170 kDa protein detected by photoaffinity labelling. Roc Natl Acad Sci (USA) 1986; 83: 3847–3850
   PubMed Web of Science ®Google Scholar
• Safa A. R., Glover C. J., Meyers M. B., et al. Vinblastine photoaffinity labelling of a high molecular weight membrane glycoprotein specific for multidrug-resistant cells. J Biol chem 1986; 261: 6137–6140
   PubMed Web of Science ®Google Scholar
• Safa A. R., Metha N. D., Agresti M. Photoaffinity labelling in multidrug resistant cells with photoactive analogs of colchicine. Biochem Biophys Res Comm 1989; 162: 1402–1408
   PubMed Web of Science ®Google Scholar
• Hamada H., Tsuruo T. Purification of the 170-to 180-kilodalton membrane glycoprotein associated with multidrug resistance. J Biol Chem 1988; 263: 1454–1458
   PubMed Web of Science ®Google Scholar
• Epstein J., Xiao H., Oba B. K. P-glycoprotein expression in plasma-cell myeloma is associated with resistance to VAD. Blood 1989; 47: 913–917
   Google Scholar
• Dalton W. S., Gmgan T. M., Meltzer P. S., et al. Drug resistance in multiple myeloma and non-Hodgkin's lymphoma: Detection of P-glycqmtein and potential circumvention by addition of verapamil to chemotherapy. J Clin Oncol 1989; 7: 415–424
   PubMed Web of Science ®Google Scholar
• Salmon S. E., Gmgan T. M., Miller T., et al. Prediction of doxorubicin resistance in vitro in myeloma, lymphoma, and breast cancer by P-glycoprotein staining. J Natl Cancer Inst 1989; 81: 696–701
   PubMed Web of Science ®Google Scholar
• Ito Y., Tanimoto M., Kumazawa T., et al. Increased P-glycoprotein expression and multidrug resistant gene mdr1 amplification are frequently found in fresh acute leukemic cells. Cancer 1989; 63: 1534–1538
   PubMed Web of Science ®Google Scholar
• Rothenberg M. L., Mickley L. A., Cole D. E., et al. Expression of the mdrI/P-170 gene in patients with acute lymphoblastic leukemia. Blood 1989; 74: 1388–1395
   PubMed Web of Science ®Google Scholar
• Carulli G., Petrini M., Marini A., et al. P-glycoprotein in acute nonlymphoblastic leukemia and in the blastic crisis of myeloid leukemia. Engl J Med 1989; 319: 797–798
   Web of Science ®Google Scholar
• Ma D. DF, Davey R. A., Hannan D. H., et al. Detection of a multidrug resistant phenotype in acute non-lymphoblastic leukemia. Lancet 1987; 1: 135–137
   PubMed Web of Science ®Google Scholar
• Goldstein L. J., Galski H., Fojo A., et al. Expression of a multidrug resistance gene in human cancers. J Natl Cancer Inst 1989; 81: 116–124
   PubMed Web of Science ®Google Scholar
• Kakehi Y., Kanamaru H., Yoshida O., et al. Measurement of multidrug-resistance messenger RNA in urogenital cancers; elevated expression in renal cell carcinoma is associated with intrinsic drug resistance. J Urol 1988; 139: 862–865
   PubMed Web of Science ®Google Scholar
• Fojo A. T., Shen D. W., Mickley L. A., et al. Intrinsic drug resistance in human kidney cancer is associated with expression of a human multidrug resistance gene. J Clin Oncol 1987; 5: 1922–1927
   PubMed Web of Science ®Google Scholar
• Kanamaru H., Kakehi Y., Yoshida O., et al. MDR1 RNA levels in human renal cell carcinomas: Correlation with grade and prediction of reversal of doxorubicin resistance by quinidine in tumor explants. J Natl Cancer Inst 1989; 81: 844–849
   PubMed Web of Science ®Google Scholar
• Bell D. R., Gerlach J. H., Kartner N., et al. Detection of P-glycoprotein in ovarian cancer: A molecular marker associated with multidrug resistance. J Clin Oncol 1985; 3: 311–315
   PubMed Web of Science ®Google Scholar
• Bourhis J., Goldstein L. J., Riou G., et al. Expression of a human multidrug resistance gene in ovarian carcinomas. Cancer Res 1989; 49: 5062–5065
   PubMed Web of Science ®Google Scholar
• Merkel D. E., Fuqua S. AW, Tandon A. K., et al. Electrophoretic analysis of 248 clinical breast cancer specimens for P-glycoprotein overexpression or gene amplification. J Clin Oncol 1989; 7: 1129–1136
   PubMed Web of Science ®Google Scholar
• Cantwell B. MJ, Bozzino J. M., Corris P., et al. The multidrug resistant phenotype in clinical practice; evaluation of cross resistance to ifosfamide and mesna after VP16–213, doxorubicin and vincristine (VPAV) for small cell lung canpr. Eur J Cancer Clin Oncol 1988; 24: 123–129
   PubMedGoogle Scholar
• Lai S. L., Goldstein L. J., Gottesman M. M., et al. MDRl gene expression in lung cancer. J Natl Cancer Inst 1989; 81: 1144–1150
   PubMed Web of Science ®Google Scholar
• Gerlach J. H., Bell D. R., Karakousi S. C., et al. P-glycoprotein in human sarcoma: Evidence for multidrug resistance. J Clin Oncol 1987; 5: 1452–1460
   PubMed Web of Science ®Google Scholar
• Chan S. HL, Thorner P. S., Haddad G., et al. Immunohistochemical detection of P-glycoprotein: Prognostic correlation in soft tissue sarcoma of childhood. J Clin Oncol 1990; 8: 689–704
   PubMed Web of Science ®Google Scholar
• Chen U., Chin J. E., Ueda K., et al. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 1986; 47: 381–389
   PubMed Web of Science ®Google Scholar
• Van der Bliek A. M., Kooiman P. M., Schneider C., et al. Sequence of mdr3 cDNA encoding a human P-glycoprotein. Gene 1988; 71: 401–411
   PubMed Web of Science ®Google Scholar
• Gros P., Croop J., Housman D. E. Mammalian multidrug resistance gene: Complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 1986; 47: 371–380
   PubMed Web of Science ®Google Scholar
• Gtos P., Raymond M., Bell J., et al. Cloning and characterization of a second member of the mouse mdr gene family. Mol Cell Biol 1988; 8: 270–278
   Google Scholar
• Devault A., Gros P. Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol Cell Biol 1990; 10: 1652–1663
   PubMed Web of Science ®Google Scholar
• Ng W. F., Sarangi F., Zastawny R. K., et al. Identification of members of the P-glycoprotein multigene family. Mol Cell Biol 1989; 9: 1224–1232
   PubMed Web of Science ®Google Scholar
• Felmlee T., Pellett S., Welch R. A. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol 1985; 163: 94–105
   PubMed Web of Science ®Google Scholar
• Cangelosi F. A., Martkui G., Leigh J. A., et al. Role of Agrobacterium tumefaciens ChvA protein in export of beta-1,2-glum. J Bacteriol 1989; 171: 1609–1615
   PubMed Web of Science ®Google Scholar
• Stanfield S. W., Ielpi L., O'Brochta D., et al. The ndvA gene product of Rhizobium meliloti is required for beta-1,2-glucan production and has homology to the ATP-binding export protein HlyB. J Bacteriol 1988; 170: 3523–3530
   PubMed Web of Science ®Google Scholar
• Chen C. M., Misra T. K., Silver S., et al. Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J Biol Chem 1986; 261: 15030–15038
   PubMed Web of Science ®Google Scholar
• Stathdee C. A., Lo R. YC. Cloning nucleotide sequence and characterization of the gene encoding the secretion function of Pasteurella haemolyrica leukotoxin determinant. J Bacteriol 1989; 171: 916–928
   PubMed Web of Science ®Google Scholar
• Croop J. M., Raymond M., Haber D., et al. The three mouse multidrug resistance (mdr) genes are expressed in a tissue specific manner in normal mouse tissues. Mol Cell Biol 1989; 9: 1346–1350
   PubMed Web of Science ®Google Scholar
• Armi R. J., Croop J. M., Horwitz, et al. The gene encoding multidrug resistance is induced and expressed at high levels during pregnancy in the secretory epithelium of the uterus. Roc Natl Acad Sci (USA) 1988; 85: 4350–4354
   PubMed Web of Science ®Google Scholar
• Thiebaut F., Tsuruo T., Hamada H., et al. Cellular localization of the multidrug resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci (USA) 1987; 84: 7735–7738
   PubMed Web of Science ®Google Scholar
• Cordon-Cardo C., O'Brien J. P., Casals D., et al. Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Roc Natl Acad Sci (USA) 1989; 86: 695–698
   PubMed Web of Science ®Google Scholar
• Chin K. V., Tanaka S., Darlington G., et al. Heat shock and arsenite increase expression of the multidrug resistance (MDR1) gene in human red cell carcinoma cells. J Biol Chem 1990; 265: 221–226
   PubMed Web of Science ®Google Scholar
• Yang C. PH, DePinho S. G., Greenberger L. M., et al. Progesterone interacts with P-glycoprotein in multidrug resistant cells and in the endometrium of gravid uterus. J Biol chem 1989; 264: 782–788
   PubMed Web of Science ®Google Scholar
• Azzaria M., Schurr E., Gros P. Discrete mutations introduced in the predicted nucleotide-binding sites of the mdr1 gene abolish its abiity to confer multidrug resistance. Mol Cell Biol 1989; 9: 5289–5297
   PubMed Web of Science ®Google Scholar
• Hamada H., Hagiwara K. I., Nakajima T., et al. Phosphorylation of the 170,000 to 180,000 glycoprotein specific to multidrug-resistant tumor cells: Effects of veraparmil, trifluoperazine, and phorbol esters. Cancer Res 1987; 47: 2860–2865
   PubMed Web of Science ®Google Scholar
• Mellado W., Horwitz S. B. Phosphorylation of the multidrug resistance associated glycoprotein. Biochemistry 1987; 26: 6900–6904
   PubMed Web of Science ®Google Scholar
• O'Connor T. WE. Phorbol ester-induced loss of colchicine ultrasen-sitivity in chronic lymphocytic leukaemial lymphocytes. Leukemia Res 1985; 7: 885–895
   Google Scholar
• Ido M., Asao T., Sakurai M., et al. An inhibitor of protein kinase C, 1-(5-isoquinolinylsulfonyl)-2-methylpiperazine (H-7) inhibits TPA-induced reduction of vincristine uptake from P388 murine leukemic cells. Leukemia Res 1986; 10: 1063–1069
   PubMed Web of Science ®Google Scholar
• Ferguson P. J., Cheng Y. Transient protection of cultured human cells against anti-tumor agents by 12–0-tetradecanoylphorbol-13-acetate. Cancer Res 1987; 47: 433–441
   PubMed Web of Science ®Google Scholar
• Fine R. L., Patel J., Chabner B. A. Phorbol esters induce multidrug resistance in human breast cancer cells. Roc Natl Acad Sci (USA) 1988; 85: 582–586
   PubMed Web of Science ®Google Scholar
• Tsuruo T., Ida H., Tsukagoshi S., et al. Increased accumulation of vincristine and Adriarnycin in drug-resistant tumor cells following incubation with calcium antagonists and calmoddin inhibitors. Cancer Res 1982; 42: 4730–4733
   PubMed Web of Science ®Google Scholar
• Wise B. C., Kw I. F. Modes of inhibition of acylcamitim xlriamycin and trifluopirazine of cardiac phospholipid-sensitive calcium-dependent protein kinase. Biochem Phannacol 1983; 32: 1259–1265
   PubMedGoogle Scholar
• Safa A. R. Photoaffinity labeling of the multidrug resistance related P-glycoprotein with photoactive analogs of verapamil. Roc Natl Acad Sci (USA) 1988; 85: 7187–7191
   PubMed Web of Science ®Google Scholar
• Pearce H. L., Safa A., Bach N. J., et al. Essential features of the P-glycoprotein pharmacophore as defined by a series of reserpine analogs that modulate multidrug resistance. Proc Natl Acad Sci (USA) 1989; 86: 5128–5132
   PubMed Web of Science ®Google Scholar
• Yang C. PH, Mellado W., Horwitz S. B. Azidopine labeling of multidrug resistance-associated glycoproteins. Biochem pharmacol 1988; 37: 1417–1421
   PubMed Web of Science ®Google Scholar
• Yoshimura A., Kuwazuru Y., Sumizawa T., et al. Cytoplasmic orientation and two domain structure of the multidrug transporter, P-glycoprotein, demonstrated with sequence-specific antibodies. J Biol Chem 1989; 264: 16282–16291
   PubMed Web of Science ®Google Scholar
• Bruggemann E. P., Germann U. A., Gottesman M. M., et al. Two different regions of phosphoglycoprotein are photoaffbity-labeled by azidopine. J Biol Chem 1989; 264: 15483–15488
   PubMed Web of Science ®Google Scholar
• Choi K., Chen C., Kriegler M., et al. An altered pattern of crossresistance in multidrug-resistant human cells results from spontaneous mutations in the mdr1 (P-glycoprotein) gene. Cell 1988; 53: 519–529
   PubMed Web of Science ®Google Scholar
• West I. C. What determines the substrate specificity of the multidrugresistance pump?. TIBS 1990; 15: 42–46
   PubMed Web of Science ®Google Scholar
• Trumper L. H., Ho A. D., Wulf G., et al. Addition of verapamil to overcome drug resistance in multiple myeloma: Preliminary clinical observations in 10 patients. J Clin Oncol 1989; 7: 1578
   PubMed Web of Science ®Google Scholar
• Slater L. M., Sweet P., Stupecky M., et al. Cyclosporin A reverses vincristine and daunorubicin resistance in acute lymphatic leukemia in vitro. J Clin Invest 1986; 77: 1405–1408
   PubMed Web of Science ®Google Scholar
• Twentyman P. R. Modification of cytotoxic drug resistance by non-immunosuppressive cyclospohs. Br J Cancer 1988; 57: 254–258
   PubMed Web of Science ®Google Scholar
• Foxwell B. MJ, Mackie A., Ling V., et al. Identification of the multidrug resistance related P-glycoprotein as a cyclosporin binding protein. Mol Pharmacol 1989; 36: 543–546
   PubMed Web of Science ®Google Scholar
• Miller L. H., Howard R. J., Carter R., et al. Research toward malaria vaccines. Science 1986; 234: 1349–1356
   PubMed Web of Science ®Google Scholar
• Krogstad D. J., Gluzman I. Y., Kyle D. E., et al. Efflux of chloroquine from Plasmodium falciparum: Mechanism of chloroquine resistance. Science 1987; 238: 1283–1285
   PubMed Web of Science ®Google Scholar
• Foote S. J., Thompson J. K., Cowman A. F., et al. Amplification of the multidrug resistance gene in some chloroquine-resistant isolates of P. falciparum. Cell 1989; 57: 921–930
   PubMed Web of Science ®Google Scholar
• McGrath J. P., Varshavsky A. The yeast STE6 gene encodes a homolog of the mammalian multidrug resistance P-glycoprotein. Nature 1989; 340: 400–404
   PubMed Web of Science ®Google Scholar
• Kuchler K., Steme R. E., Thomer J. Saccharomyces cerevisiae STE6 gene ptuduct: a novel pathway of protein export in eukaryotic cells. EMBO J 1989; 13: 13973–3984
   Google Scholar
• Riordan J. R., Rommens J. M., Kerem B-S, et al. Identification of the cystic fibrosis gene: Cloning and characterization of complementary DNA. Science 1989; 245: 1066–1073
   PubMed Web of Science ®Google Scholar