Oligonucleotide modulation of multidrug resistance

European Journal of Cancer

Volumn 32, Issue 6, 1996, Pages 1010-1018

  Bouffard, D Y ^a   Ohkawa, T ^a   Kijima, H ^a,d   Irie, A ^a   Suzuki, T ^a   Curcio, L D ^b   Holm, P S ^a   Sassani, A ^a   Scanlon, K J ^a,c  

^a Section of Biochemical Pharmacology   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^c BAYER AG   (Germany)

^d TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ANTISENSE OLIGONUCLEOTIDE; CARRIER PROTEIN; CYCLOSPORIN A; DIFLOXACIN; GENE PRODUCT; GLYCOPROTEIN P; OLIGONUCLEOTIDE; RIBOZYME; VERAPAMIL;

CANCER CELL DESTRUCTION; CHROMOSOME 16; DRUG ACCUMULATION; DRUG TRANSPORT; HUMAN; HUMAN CELL; LEUKEMIA CELL; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MULTIDRUG RESISTANCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ISOLATION; REVIEW;

DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; OLIGONUCLEOTIDES, ANTISENSE; P-GLYCOPROTEIN; PHENOTYPE; RNA, CATALYTIC; SIGNAL TRANSDUCTION;

EID: 0029999403     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/0959-8049(96)00065-2     Document Type: Article

References (111)

1. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976, 455, 152-162.
2. Kartner N, Riordan JR, Ling V. Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 1983, 221, 1285-1288.
3. Kartner N, Evernden-Porelle D, Bradley G, Ling V. Detection of P-glycoprotein in multidrug-resistant cell lines by monoclonal antibodies. Nature 1985, 316, 820-823.
4. Gros P, Croop J, Roninson I, Varshavsky A, Housman DE. Isolation and characterization of DNA sequences amplified in multidrug resistant hamster cells. Proc Natl Acad Sci USA 1986, 83, 337-341.
5. Roninson IB, Chin JE, Choi K, et al. Isolation of human mdr DNA sequences amplified in multidrug-resistant KB carcinoma cells. Proc Natl Acad Sci USA 1986, 83, 4538-4542.
6. Fojo AT, Ueda K, Slamon DJ, Poplack DG, Gottesman MM, Pastan I. Expression of a multidrug-resistance gene in human tumors and tissues. Proc Natl Acad Sci USA 1987, 84, 265-269.
7. Gottesman MM, Hrycyna CA, Schoenlein PV, Germann UA, Pastan I. Genetic analysis of the multidrug transporter. Ann Rev Genet 1995, 29, 607-649.
8. Chen C-j, Chin JE, 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.
9. Higgins CF, Hiles ID, Salmond GPC, et al. A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature 1986, 323, 448-450.
10. Cornwell MM, Tsuruo T, Gottesman MM, Pastan I. ATP-binding properties of P-glycoprotein from multidrug-resistant KB cells. FASEB J 1987, 1, 51-54.
11. Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Ann Rev Biochem 1993, 62, 385-427.
12. Mirski SEL, Gerlach JH, Cole SPC. Multidrug resistance in a human small cell lung cancer cell line selected in adriamycin. Cancer Res 1987, 47, 2594-2598.
13. Marsh W, Sicheri D, Center MS. Isolation and characterization of adriamycin-resistant HL-60 cells which are not defective in the initial intracellular accumulation of drug. Cancer Res 1986, 46, 4053-4057.
14. McGrath T, Center MS. Adriamycin resistance in HL-60 cells in the absence of detectable P-glycoprotein. Biochem Biophys Res Commun 1987, 145, 1171-1176.
15. Cole SPC, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258, 1650-1654.
16. Krishnamachary N, Center MS. The MRP gene associated with a non-P-glycoprotein multidrug resistance encodes a 190-kDa membrane bound glycoprotein. Cancer Res 1993, 53, 3658-3661.
17. Zaman GJR, Flens MJ, van Leusden MR, et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci USA 1994, 91, 8822-8826.
18. Scheper RJ, Broxterman HJ, Scheffer GL, et al. Overexpression of a Mr 110,000 vesicular protein in non-P-glycoprotein-mediated multidrug resistance. Cancer Res 1993, 53, 1475-1479.
19. Scheffer GL, Wijngaard PLJ, Flens MJ, et al. The drug resistance-related protein LRP is the human major vault protein. Nature Med 1995, 1, 578-582.
20. Slovak ML, Ho JP, Cole SPC, et al. The LRP gene encoding a major vault protein associated with drug resistance maps proximal to MRP on chromosome 16: evidence that chromosome breakage plays a key role in MRP or LRP gene amplification. Cancer Res 1995, 55, 4214-4219.
21. Tritton TR, Hickman JA. How to kill cancer cells: membranes and cell signaling as targets in cancer chemotherapy. Cancer Cells 1990, 2, 95-105.
22. Brunton VG, Workman P. Cell-signaling targets for antitumour drug development. Cancer Chemother Pharmacol 1993, 32, 1-19.
23. Aftab DT, Yang JM, Hait WN. Functional role of phosphorylation of the multidrug transporter (P-glycoprotein) by protein kinase C in multidrug-resistant MCF-7 cells. Oncol Res 1994, 6, 59-70.
24. Chambers TC, Pohl J, Raynor RL, Kuo JF. Identification of specific sites in human P-1 glycoprotein phosphorylated by protein kinase-C. J Biol Chem 1993, 268, 4592-4595.
25. Boguski MS, McCormick F. Proteins regulating Ras and its relatives. Nature 1993, 366, 643-654.
26. Ishida H, Kijima H, Ohta Y, Kashani-Sabet M, Scanlon KJ. Mechanisms of cisplatin resistance and reversal in human tumors. In Kellen JA, ed. Alternative Mechanisms of Multidrug Resistance in Cancer. Boston, Birkhäuser, 1995, 225-264.
27. Ueeda K, Clark DP, Chen C-j, Roninson IB, Gottesman MM, Pastan I. The human multidrug resistance (mdr1) gene: cDNA cloning and transcription initiation. J Biol Chem 1987, 262, 505-508.
28. Madden MJ, Morrow CS, Nakagawa M, Goldsmith ME, Fairchild CR, Cowan KH. Identification of 5′ and 3′ sequences involved in the regulation of transcription of the human mdr1 gene in vivo. J Biol Chem 1993, 268, 8290-8297.
29. Scanlon KJ, Ishida H, Kashani-Sabet M. Ribozyme-mediated reversal of the multidrug-resistant phenotype. Proc Natl Acad Sci USA 1994, 91, 11123-11127.
30. Hollander MC, Fornace AJ Jr. Induction of fos RNA by DNA-damaging agents. Cancer Res 1989, 49, 1687-1692.
31. Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res 1981, 41, 1967-1972.
32. Dalton WS, Grogan TM, Meltzer PS, et al. Drug-resistance in multiple myeloma and non-Hodgkin's lymphoma: detection of P-glycoprotein and potential circumvention by addition of verapamil to chemotherapy. J Clin Oncol 1989, 7, 415-424.
33. Salmon SE, Dalton WS, Grogan TM, et al. Multidrug-resistant myeloma: laboratory and clinical effects of verapamil as a chemosensitizer. Blood 1991, 78, 44-50.
34. Futscher BW, Campbell K, Dalton WS. Collateral sensitivity to nitrosoureas in multidrug-resistant cells selected with verapamil. Cancer Res 1992, 52, 5013-5017.
35. Slater LM, Sweet P, Stupecky M, Gupta S. Cyclosporin A reverses vincristine and daunorubicin resistance in acute lymphatic leukemia in vitro. J Clin Invest 1986, 77, 1405-1408.
36. Sonneveld P, Durie BGM, Lokhorst HM, et al. Modulation of multidrug-resistant multiple myeloma by cyclosporin. Lancet 1992, 340, 255-259.
37. Sato W, Fukazawa N, Suzuki T, Yusa K, Tsuruo T. Circumvention of multidrug resistance by a newly synthesised quinoline derivative, MS-073. Cancer Res 1991, 51, 2420-2424.
38. Sato W, Fukazawa N, Nakanishi O, et al. Reversal of multidrug resistance by a novel quinoline derivative, MS-209. Cancer Chemother Pharmacol 1995, 35, 271-277.
39. Gollapudi S, Thadepalli F, Kim CH, Gupta S. Difloxacin reverses multidrug resistance in HL-60/AR cells that overexpress the multidrug resistance-related protein (mrp) gene. Oncol Res 1995, 7, 213-225.
40. Tong AW, Lee J, Wang R-M, et al. Elimination of chemoresistant multiple myeloma clonogenic colony-forming cell by combined treatment with a plasma cell-reactive monoclonal antibody and a P-glycoprotein-reactive monoclonal antibody. Cancer Res 1989, 49, 4829-4834.
41. Inouye M. Antisense RNA: its functions and applications in gene regulation - a review. Gene 1988, 72, 25-34.
42. Zamecnik PC, Stephenson ML. Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide. Proc Natl Acad Sci USA 1978, 75, 280-284.
43. Wagner RW. The state of the art in antisense research. Nature Med 1995, 13, 1116-1118.
44. Leonetti JP, Degols G, Clarenc JP, Mechti N, Lebleu B. Cell delivery and mechanism of action of antisense oligonucleotides. Prog Nucleic Acid Res Mol Biol 1993, 44, 143-166.
45. Neckers L, Whitesell L, Rosolen A, Geselowitz DA. Antisense inhibition of oncogene expression. Crit Rev Oncol 1992, 3, 175-231.
46. Crooke ST. Progress toward oligonucleotide therapeutics: pharmacodynamic properties. FASED J 1993, 7, 533-539.
47. Tidd DM. Synthetic oligonucleotides as therapeutic agents. Br J Cancer 1991, 63, 6-8.
48. Carter G, Lemoine NR. Antisense technology for cancer therapy: does it make sense? Br J Cancer 1993, 67, 869-876.
49. Walder RY, Walder JA. Role of RNase H in hybrid-arrested translation by antisense oligonucleotides. Proc Natl Acad Sci USA 1988, 85, 5011-5015.
50. Tseng BY, Brown KD. Antisense oligonucleotides technology in the development of cancer therapeutics. Cancer Gene Ther 1994, 1, 65-71.
51. Mercola D, Cohen JS. Antisense approaches to cancer gene therapy. Cancer Gene Ther 1995, 2, 47-59.
52. Stein CA, Cheng Y-c. Antisense oligonucleotides as therapeutic agents - is the bullet really magical? Science 1993, 261, 1004-1012.
53. Gao W-y, Han F-s, Storm C, Egan W, Cheng Y-c. Phosphorothioate oligonucleotides are inhibitors of human DNA polymerases and RNase H: implication for antisense technology. Mol Pharmacol 1992, 41, 223-229.
54. Wickstrom E, Bacon TA, Wickstrom EL. Down-regulation of c-MYC antigen expression in lymphocytes of Eu-c-myc transgenic mice treated with anti-c-myc DNA methylphosphonates. Cancer Res 1992, 52, 6741-6745.
55. Hélène C, Toulmé J-J. Specific regulation of gene expression by antisense, sense and antigene nucleic acids. Biochim Biophys Acta 1990, 1049, 99-125.
56. Chang EH, Miller PS, Cushman C, et al. Antisense inhibition of ras p21 expression that is sensitive to a point mutation. Biochemistry 1991, 30, 8283-8286.
57. Vasanthakumar G, Ahmed NK. Modulation of drug resistance in a daunorubicin resistant subline with oligonucleoside methylphosphonates. Cancer Commun 1989, 1, 225-232.
58. Jaroszweski JW, Kaplan O, Syi J-L, Sehested M, Faustino PJ, Cohen JS. Concerning antisense inhibition of the multiple drug resistance gene. Cancer Commun 1990, 2, 287-294.
59. Efferth T, Volm M. Modulation of P-glycoprotein-mediated multidrug resistance by monoclonal antibodies, immunotoxins or antisense oligodeoxynucleotides in kidney carcinoma and normal kidney cells. Oncology 1993, 50, 303-308.
60. Corrias MV, Tonini GP. An oligomer complementary to the 5′ end region of mdr1 gene decreases resistance to doxorubicin of human adenocarcinoma-resistant cells. Anticancer Res 1992, 12, 1431-1438.
61. Bertram J, Palfner K, Killian M, et al. Reversal of multidrug resistance in vitro by phosphorothioate oligonucleotides and ribozymes. Anticancer Drugs 1995, 6, 123-134.
62. Thierry AR, Rahman A, Dritschilo A. Overcoming multidrug resistance in human tumor cells using free and liposomally encapsulated antisense oligodeoxynucleotides. Biochem Biophys Res Commun 1993, 190, 952-960.
63. Quattrone A, Papucci L, Morganti M, et al. Inhibition of MDR1 gene expression by antimessenger oligonucleotides lowers multiple drug resistance. Oncol Res 1994, 6, 311-320.
64. Rivoltini L, Colombo MP, Supino R, Ballinari D, Tsuruo T, Parmiani G. Modulation of multidrug resistance by verapamil or mdr1 anti-sense oligodeoxynucleotide does not change the high susceptibility to lymphokine-activated killers in mdr-resistant human carcinoma (LoVo) line. Int J Cancer 1990, 46, 727-732.
65. Hanchett LA, Baker RM, Dolnick BJ. Subclonal heterogeneity of the multidrug resistance phenotype in a cell line expressing antisense MDR1 RNA. Somat Cell Mol Genet 1994, 20, 463-480.
66. Cech TR, Zaug AJ, Grabowski PJ. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell 1981, 27, 487-496.
67. Altman S. Ribonuclease P: An enzyme with a catalytic RNA subunit. Adv Enzymol 1987, 62, 1-36.
68. Symons RH. Small catalytic RNAs. Ann Rev Biochem 1992, 61, 641-671.
69. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 1982, 31, 147-157.
70. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 1983, 35, 849-857.
71. Uhlenbeck OC. A small catalytic oligoribonucleotide. Nature 1987, 328, 596-600.
72. Buzayan JM, Gerlach WL, Bruening G. Non-enzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA. Nature 1986, 323, 349-353.
73. Perrotta AT, Been MD. Cleavage of oligoribonucleotides by a ribozyme derived from the hepatitis δ virus RNA sequence. Biochemistry 1992, 31, 16-21.
74. Symons RH. Ribozymes. Curr Opin Struct Biol 1994, 4, 322-330.
75. Christoffersen RE, Marr JJ. Ribozymes as human therapeutic agents. J Med Chem 1995, 38, 2023-2037.
76. Kashani-Sabet M, Scanlon KJ. Application of ribozymes to cancer gene therapy. Cancer Gene Ther 1995, 2, 213-223.
77. Kiehntopf M, Esquivel EL, Brach MA, Herrmann F. Ribozymes: biology, biochemistry, and implications for clinical medicine. J Mol Med 1995, 73, 65-71.
78. Homann M, Tzortzakaki S, Rittner K, Sczakiel G, Tabler M. Incorporation of the catalytic domain of a hammerhead ribozyme into antisense RNA enhances its inhibitory effect on the replication of human immunodeficiency virus type 1. Nucleic Acids Res 1993, 21, 2809-2814.
79. Kiehntopf M, Brach MA, Licht T, et al. Ribozyme-mediated cleavage of the MDR-1 transcript restores chemosensitivity in previously resistant cancer cells. EMBO J 1994, 13, 4645-4652.
80. Taylor NR, Kaplan BE, Swiderski P, Li H, Rossi JJ. Chimeric DNA-RNA hammerhead ribozymes have enhanced in vitro catalytic efficiency and increased stability in vivo. Nucleic Acids Res 1992, 20, 4559-4565.
81. Kobayashi H, Dorai T, Holland JF, Ohnuma T. Cleavage of human MDR1 mRNA by a hammerhead ribozyme. FEBS Lett 1993, 319, 71-74.
82. Kobayashi H, Dorai T, Holland JF, Ohnuma T. Reversal of drug sensitivity in multidrug-resistant tumor cells by a MDR1 (PGY1) ribozyme. Cancer Res 1994, 54, 1271-1275.
83. Gunning P, Leavitt J, Muscat G, Ng S-y, Kedes L. A human β-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci USA 1987, 84, 4831-4835.
84. Scanlon KJ, Jiao L, Funato T, et al. Ribozyme-mediated cleavage of c-fos mRNA reduces gene expression of DNA synthesis enzymes and metallothionein. Proc Natl Acad Sci USA 1991, 88, 10591-10595.
85. Scanlon KJ, Ishida H, Kashani-Sabet M. Ribozyme-mediated reversal of the multidrug-resistant phenotype. Proc Natl Acad Sci USA 1994, 91, 11123-11127.
86. Teeter LD, Eckersberg T, Tsai Y, Kuo MT. Analysis of the Chinese hamster P-glycoprotein/multidrug resistance gene pgp1 reveals that the AP-1 site is essential for full promoter activity. Cell Growth Differ 1991, 2, 429-437.
87. Holm PS, Scanlon KJ, Dietel M. Reversion of multidrug resistance in the P-glycoprotein-positive human pancreatic cell line (EPP85-181RDB) by introduction of a hammerhead ribozyme. Br J Cancer 1994, 70, 239-243.
88. Palfner K, Kneba M, Hiddemann W, Bertram J. Improvement of hammerhead ribozymes cleaving mdr-1 mRNA. Biol Chem Hoppe Seyler 1995, 376, 289-295.
89. Nakashima E, Matsushita R, Negishi H, et al. Reversal of drug sensitivity in MDR subline of P388 leukemia by gene-targeted antisense oligonucleotide. J Pharm Sci 1995, 84, 1205-1209.
90. Rossi JJ. Controlled, targeted, intracellular expression of ribozymes: progress and problems. Trends Biotechnol 1995, 13, 301-306.
91. Sullenger BA, Cech TR. Tethering ribozymes to a retroviral packaging signal for destruction of viral RNA. Science 1993, 262, 1566-1569.
92. Hodgson CP. The vector void in gene therapy. Biotechnology 1995, 13, 222-225.
93. Ledley FD. Nonviral gene therapy: the promise of genes as pharmaceutical products. Hum Gene Ther 1995, 6, 1129-1144.
94. Yang N-S, Burkholder J, Roberts B, Martinell B, McCabe D. In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment. Proc Natl Acad Sci USA 1991, 88, 2726-2730.
95. Ascadi G, Jiao S, Jani A, et al. Direct gene transfer and expression into heart in vivo. New Biol 1991, 3, 71-81.
96. Ascadi G, Dickson G, Love DR, et al. Human dystrophin expression in mdx mice after intracellular injection of DNA constructs. Nature 1991, 352, 815-818.
97. Wolff JA, Budker V. Cationic lipid-mediated gene transfer. In Sobol RE, Scanlon KH, eds. The Internet Book of Gene Therapy: Cancer Therapeutics. Stamford, CT, Appleton & Lange, 1995, 65-73.
98. Wagner E, Zenke M, Cotten M, Beug H, Birnstiel ML. Transferrin-polycation conjugates as carriers for DNA uptake into cells. Proc Natl Acad Sci USA 1990, 87, 3410-3414.
99. Zenke M, Steinlein P, Wagner E, Cotten M, Beug H, Birnstiel ML. Receptor-mediated endocytosis of transferrin-polycation conjugates: an efficient way to introduce DNA into hematopo-ietic cells. Proc Natl Acad Sci USA 1990, 87, 3655-3659.
100. Harris CE, Agarwal S, Hu P, Wagner E, Curiel DT. Receptor-mediated gene transfer to airway epithelial cells in primary culture. Am J Respir Cell Mol Biol 1993, 9, 441-447.
101. Curiel DT, Agarwal S, Wagner E, Cotten M. Adenovirus enhancement of transferrin-polylysine-mediated gene delivery. Proc Natl Acad Sci USA 1991, 88, 8850-8854.
102. Cotten M, Wagner E, Zatloukal K, Phillips S, Curiel DT, Birnstiel ML. High-efficiency receptor-mediated delivery of small and large 48 kilobase gene constructs using the endosome-disruption activity of defective or chemically inactivated adenovirus particles. Proc Natl Acad Sci USA 1992, 89, 6094-6098.
103. Curiel DT, Agarwal S, Romer MU, et al. Gene transfer to respirator epithelial cells via the receptor-mediated endocytosis pathway. Am J Respir Cell Mol Biol 1992, 6, 247-252.
104. Curiel DT, Wagner E, Cotten M, et al. High-efficiency gene transfer mediated by adenovirus coupled to DNA-polylysine complexes. Hum Gene Ther 1992, 3, 147-154.
105. Cristiano RJ, Smith LC, Woo SL. Hepatic gene therapy: adenovirus enhancement of receptor-mediated gene delivery and expression in primary hepatocytes. Proc Natl Acad Sci USA 1993, 90, 2122-2126.
106. Wu GY, Zhan P, Sze LL, Rosenberg AR, Wu CH. Incorporation of adenovirus into a ligand-based DNA carrier system results in retention of original receptor specificity and enhances targeted gene expression. J Biol Chem 1994, 269, 11542-11546.
107. Wagner E, Plank C, Zatloukal K, Cotten M, Birnstiel ML. Influenza virus hemagglutinin HA-2N-terminal fusogenic peptides augment gene transfer by transferrin-polylysine-DNA complexes: toward a synthetic virus-like gene-transfer vehicle. Proc Natl Acad Sci USA 1992, 89, 7934-7938.
108. Vile RG, Russell SJ. Retrovirus as vectors. Br Med Bull 1995, 51, 12-30.
109. Flotte TR, Carter BJ. Adeno-associated virus vectors for gene therapy. Gene Ther 1995, 2, 357-362.
110. Efstathiou S, Minson AC. Herpes virus-based vectors. Br Med Bull 1995, 51, 45-55.
111. Weitzman MD, Wilson JM, Eck SL. Adenovirus vectors in cancer gene therapy. In Sobol RE, Scanlon KJ, eds. The Internet Book of Gene Therapy: Cancer Therapeutics. Stamford, CT, Appleton & Lange, 1995, 17-25.