Targeting MDR1-P-glycoprotein (MDR1-Pgp) in immunochemotherapy of acute myeloid leukemia (AML)

Annali dell'Istituto Superiore di Sanita

Volumn 49, Issue 2, 2013, Pages 190-208

  Cianfriglia, Maurizio ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Acute myeloid leukemia (AML); Gemtuzumab ozogamicin (GO); Immunoconiugate; MDR reversing agents; MDR1 P glycoprotein; Multidrug resistance (MDR)

Indexed keywords

AMINOGLYCOSIDE; ANTINEOPLASTIC AGENT; GEMTUZUMAB; IMMUNOTOXIN; MONOCLONAL ANTIBODY; MULTIDRUG RESISTANCE PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; ANIMAL; ARTICLE; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; HUMAN; IMMUNOCHEMISTRY; IMMUNOLOGY; MALE; MIDDLE AGED; PHENOTYPE; TUMOR CELL LINE; YOUNG ADULT;

ADULT; AGED; AMINOGLYCOSIDES; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNOCHEMISTRY; IMMUNOTOXINS; LEUKEMIA, MYELOID, ACUTE; MALE; MIDDLE AGED; P-GLYCOPROTEIN; PHENOTYPE; YOUNG ADULT;

EID: 84881336359     PISSN: 00212571     EISSN: None     Source Type: Journal    
DOI: 10.4415/ANN-13-02-11     Document Type: Article

References (113)

1. Carter PJ, Senter PD. Antibody-drug-conjugates for cancer therapy. Cancer J 2008;14:154-69. DOI: 10.1097/PPO.0b013e318172d704
2. Wu AM, Senter PD. Arming antibodies: prospects and challenges for immune-conjugates. Nat Biotechnol 2005;23:1137-46. DOI: 10.1038/nbt1141
3. Nicolaou KC, Dai WM, Tsay SC, Estevez VA, Wrasidlo W. Designed enediynes: a new class of DNA-cleaving molecules with potent and selective anticancer activity. Science 1992;256:1172-8. DOI: 10.1126/science.256.5060.1172
4. Hollander I, Kunz A, Hamann P. Selection of reaction additives used in the preparation of monomeric antibody calicheamicin conjugates. Bioconjugate Chem 2008;19:358-61. DOI: 10.1021/bc700321z
5. Bross PF, Beitz J, Chen G, Chen XH, Duffy E, Kieffer L, Roy S, Sridhara R, Rahman A, Williams G, Pazdur R. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clinical Cancer Research 2001;7:1490-6.
6. Petersdorf S, Kopecky K, Stuart RK, Richard A, Larson RA, Nevill TJ, Stenke L, Slovak ML, Tallman MS, Willman CL, Erba H, Appelbaum FR. Preliminary results of Southwest Oncology Group Study S0106: An international intergroup phase 3 randomized trial comparing the addition of gemtuzumab ozogamicin to standard induction therapy versus standard induction therapy followed by a second randomization to post-consolidation gemtuzumab ozogamicin versus no additional therapy for previously untreated acute myeloid leukemia. Blood 2009;114:(abstract 790).
7. Scott AM, Wolchok JD, Old LJ. Antibody therapy of cancer. Nat Rev Cancer 2012;12:278-87. DOI: 10.1038/nrc3236
8. Senter PD. Potent antibody drug conjugates for cancer therapy. Curr Opin Chem Biol 2009;13:235-44. DOI: 10.1016/j.cbpa.2009.03.023
9. Kovtun YV, Goldmacher VS. Cell killing by antibody- drug conjugates. Cancer Lett 2007;255:232-40. DOI: 10.1016/j.canlet.2007.04.010
10. Younes A, Bartlett NL, Leonard JP, Kennedy DA, Pharm D, Lynch C, Sievers EL, Forero-Torres A. Brentuximab Vedotin (SGN-35) for relapsed CD30-positive lymphomas. N Engl J Med 2010;363:1812-21. DOI: 10.1056/NEJMoa1002965
11. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh DY, Diéras V, Guardino E, Fang L, Lu MW, Olsen S, Blackwell K, EMILIA Study Group. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012;367:1783-91. DOI: 10.1056/NEJMoa1209124
12. Krop IE, LoRusso P, Miller KD, Modi S, Yardley D, Rodriguez G, Guardino E, Lu M, Zheng M, Girish S, Amler L, Winer EP, Rugo HS. A phase II study of trastuzumab emtansine in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer who were previously treated with trastuzumab, lapatinib, an anthracycline, a taxane, and capecitabine. J Clin Oncol 2012;30:3234-41.
13. Dowell JA, Korth-Bradley J, Liu H, King SP, Berger MS. Pharmacokinetics of gemtuzumab ozogamicin, an antibody-targeted chemotherapy agent for the treatment of patients with acute myeloid leukemia in first relapse. J Clin Pharmacol 2001;41:1206-14. DOI: 10.1177/00912700122012751
14. Peiper SC, Ashmun RA, Look AT. Molecular cloning, expression, and chromosomal localization of a human gene encoding the CD33 myeloid differentiation antigen. Blood 1988;72:314-21.
15. Burnett AK, Hills RK, Milligan D, Kjeldsen L, Kell J, Russell NH, Yin JA, Hunter A, Goldstone AH, Wheatley K. Identification of patients with acute myeloblastic leukemia who benefit from the addition of gemtuzumab ozogamicin: Results of the MRC AML15 trial. J Clin Oncol 2011;29:369-77. DOI: 10.1200/JCO.2010.31.4310
16. Castaigne S, Pautas C, Terré C, Raffoux E, Bordessoule D, Bastie JN, Legrand O, Thomas X, Turlure P, Reman O, de Revel T, Gastaud L, de Gunzburg N, Contentin N, Henry E, Marolleau JP, Aljijakli A, Rousselot P, Fenaux P, Preudhomme C, Chevret S, Dombret H, Acute Leukemia French Association. Effect of gemtuzumab ozogamicin onsurvival of adult patients with de-novo acute myeloid leukaemia (ALFA-0701): a randomised, open-label, phase 3 study. Lancet 2012;379:1508-16. DOI: 10.1016/S0140-6736(12)60485-1
17. Delaunay J, Recher C, MD, Pigneux A, Witz F, Vey N,Blanchet O, Lefebvre P, Luquet I, Guillerme I, Volteau E, Gyan F, Lioure B, Jourdan E, Bouscary D, Guieze R, Randriamalala E, Ojeda Uribe ME, Dreyfus F, Lacombe C, Béné MC, Cahn JY, Harousseau JL, Ifrah N. Addition of gemtuzumab ozogamycin to chemotherapy improves event-free survival but not overall survival of AML patients with intermediate cytogenetics not eligible for allogeneic transplantation: Results of the GOELAMS AML 2006 IR study. Blood 2011;118:(abstr 79).
18. Burnett AK, Russell NH, Hills RK, Kell J, Freeman S, Kjeldsen L, Hunter AE, Yin J, Craddock CF, Dufva IH, Wheatley K, Milligan D. Addition of gemtuzumab ozogamicin to induction chemotherapy improves survival in older patients with acute myeloid leukemia. J Clin Oncol 2012;30:3924-31. DOI: 10.1200/JCO.2012.42. 2964
19. Kantarjian H, Thomas D, Jorgensen J, Jabbour E, Kebriaei P, Rytting M, York S, Ravandi F, Kwari M, Faderl S, Rios MB, Cortes J, Fayad L, Tarnai R, Wang SA, Champlin R, Advani A, O'Brien S. Inotuzumab ozogamicin, an anti-CD22-calecheamicin conjugate, for refractory and relapsed acute lymphocytic leukaemia: a phase 2 study. Lancet Oncol 2012;13:403-11. DOI: 10.1016/S1470-2045(11)70386-2
20. Ricart AD. Antibody-drug conjugates of calicheamicin derivative: gemtuzumab ozogamicin and inotuzumab ozogamicin. Clin Cancer Res 2011;17:6417-27. DOI: 10.1158/1078-0432.CCR-11-0486
21. Takeshita A, Shinjo K, Yamakage N, Ono T, Hirano I, Matsui H, Shigeno K, Nakamura S, Tobita T, Maekawa M, Ohnishi K, Sugimoto Y, Kiyoi H, Naoe T, Ohno R. CMC-544 (inotuzumab ozogamicin) shows less effect on multidrug resistant cells: analyses in cell lines and cells from patients with B-cell chronic lymphocytic leukaemia and lymphoma. Br J Haematol 2009;146:34-43. DOI: 10.1111/j.1365-2141. 2009.07701.x
22. Advani A, Coiffier B, Czuczman MS, Dreyling M, Foran J, Gine E, Gisselbrecht C, Ketterer N, Nasta S, Rohatiner A, Schmidt-Wolf IG, Schuler M, Sierra J, Smith MR, Verhoef G, Winter JN, Boni J, Vandendries E, Shapiro M, Fayad L. Safety, pharmacokinetics, and preliminary clinical activity of inotuzumab ozogamicin, a novel immunoconjugate for the treatment of B-cell non-Hodgkin's lymphoma: results of a phase I study. J Clin Oncol 2010;28:2085-93. DOI: 10.1200/JCO.2009.25.1900
23. Sammet B, Steinkühler C, Sewald N. Antibody-drug conjugates in tumor therapy. Pharm Pat Analyst 2012;1:65-73. DOI: 10.4155/ppa.12.4
24. Sievers EL, Senter PD. Antibody-drug conjugates in cancer therapy. Annu Rev Med 2013 (in press). DOI: 10.1146/annurev-med-050311-201823
25. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2:248-58. DOI: 10.1038/nrc706
26. Deeley RG, Cole SP. Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett 2006;580:1103-11. DOI: 10.1016/j.febslet.2005.12.036
27. Robey RW, Polgar O, Deeken J, To KW, Bates SE. ABCG2: determining its relevance in clinical drug resistance. Cancer Metastasis Rev 2007;26:39-57. DOI: 10.1007/s10555-007-9042-6
28. Cianfriglia M, Mallano A, Ascione A, Dupuis ML. Multidrug transporter proteins and cellular factors involved in free and mAb linked calicheamicin-gamma1 (gentuzumab ozogamicin, resistance and in the selection of GO resistant variants of the HL60AML cell line. Int J Oncol 2010;36:1513-20.
29. Walter RB, Raden BW, Thompson J, Flowers DA, Kiem HP, Bernstein ID, Linenberger ML. Breast cancer resistance protein (BCRP/ABCG2) does not confer resistance to gemtuzumab ozogamicin and calicheamicin-gamma1 in acute myeloid leukemia cells. Leukemia 2004;18:1914-7. DOI: 10.1038/sj.leu.2403461
30. Szakàcs G, Peterson JK, Ludwig JA, Booth-Genthe C, and Gottesman MM. Targetting multidrug resistance in cancer. Nat Rev Drug Discovery 2006;5:219-34. DOI: 10.1038/nrd1984
31. Shaffer BC, Gillet JP, Patel C, Baer MR, Bates SE, Gottesman MM. Drug resistance: still a daunt ing challenge to the successful treatment of AML. Drug Resist Updat 2012;15:62-9. DOI: 10.1016/j.drup.2012.02.001
32. Walter RB, Gooley TA, van der Velden VH, Loken MR, van Dongen JJ, Flowers DA, Bernstein ID, Appelbaum FR.CD33 expression and P-glycoprotein-mediated drug efflux inversely correlate and predict clinical outcome in patients with acute myeloid leukemia treated with gemtuzumab ozogamicin monotherapy. Blood 2007;109:4168-70. DOI: 10.1182/blood-2006-09-047399
33. Stone RM, Moser B, Sanford B, Schulman P, Kolitz JE, Allen S, Stock W, Galinsky I, Vij R, Marcucci G, Hurd D, Larson RA. Cancer and Leukemia Group B. High dose cytarabine plus gemtuzumab ozogamicin for patients with relapsed or refractory acute myeloid leukemia: Cancer and Leukemia Group B study 19902. Leuk Res 2011;35:329-33. DOI: 10.1016/j.leukres.2010.07.017
34. Goldstone AH, Burnett AK, Wheatley K, Smith AG, Hutchinson RM, Clark RE. Attempts to improve treatment outcomes in acute myeloid leukemia (AML) in older patients: the results of the United Kingdom Medical Research Council AML11 trial. Blood 2001;98:1302-11. DOI: 10.1182/blood.V98.5.1302
35. Shipley JL, Butera JN. Acute myelogenous leukemia. Exp Hematol 2009;37:649-58. DOI: 10.1016/j.exphem.2009.04.002
36. Hauswirth AW, Florian S, Printz D, Sotlar K, Krauth MT, Fritsch G, Schernthaner GH, Wacheck V, Selzer E, Sperr WR, Valent P. Expression of the target receptor CD33 in CD34+/CD38-/CD123+ AML stem cells. Eur J Clin Invest 2007;37:73-82. DOI: 10.1111/j.1365-2362.2007.01746.x
37. Naito K, Takeshita A, Shigeno K, Nakamura S, Fujisawa S, Shinjo K, Yoshida H, Ohnishi K, Mori M, Terakawa S, Ohno R. Calicheamicin-conjugated humanized anti-CD33 monoclonal antibody (gemtuzumab zogamicin, CMA-676) shows cytocidal effect on CD33-positive leukemia cell lines, but is inactive on P-glycoprotein-expressing sublines. Leukemia 2000;14:1436-44. DOI: 10.1038/sj.leu.2401851
38. Jager E, van der Velden VHJ, te Marvelde JG, Roland B, Walter RB, Agur Z, Vainstein V. Targeted drug delivery by gemtuzumab ozogamicin: Mechanism- based mathematical model for treatment strategy improvement and therapy individualization. PLoS ONE 2011;6:1-10. DOI: 10.1371/journal. pone.0024265
39. Dowell JA, Korth-Bradley J, Liu H, King SP, Berger MS. Pharmacokinetics of gemtuzumab ozogamicin, an antibody-targeted chemotherapy agentfor the treatment of patients with acute myeloid leukemia in first relapse. J Clin Pharmacol 2001;41:1206-14.
40. Linenberger ML, Hong T, Flowers D, Sievers EL, Gooley TA, Bennett JM, Berger MS, Leopold LH, Appelbaum FR, Bernstein ID. Multidrug-resistance phenotype and clinical response to gemtuzumab ozogamicin. Blood 2001;98:988-94. DOI: 10.1182/blood.V98.4.988
41. Walter RB, Raden BW, Hong TC, Flowers DA, Bernstein ID, Linenberger ML. Multidrug resistance protein attenuates gemtuzumab ozogamicin-induced cytotoxicity in acute myeloid leukemia cells. Blood 2003;102:1466-73. DOI: 10.1182/blood-2003-02-0396
42. Walter RB, Raden BW, Cronk MR, Bernstein ID, Appelbaum FR, Banker DE. The peripheral benzodiazepine receptor ligand PK11195 overcomes different resistance mechanisms to sensitize AML cells to gemtuzumab ozogamicin. Blood 2004;103:4276-84. DOI: 10.1182/blood-2003-11-3825
43. Goemans BF, Zwaan CM, Vijverberg SJ, Loonen AH, Creutzig U, Hählen K, Reinhardt D, Gibson BE, Cloos J, Kaspers GI. Large interindividual differences in cellular sensitivity to calicheamicin may influence gemtuzumab ozogamicin response in acute myeloid leukemia. Leukemia 2008;22:2284-5. DOI: 10.1038/leu.2008.147
44. Tavor S, Rahamim E, Sarid N, Rozovski U, Gibstein L, Aviv F, Kirsner I, Naparstek E. High response rate for treatment with gemtuzumab ozogamicin and cytarabine in elderly patients with acute myeloid leukemia and favorable and intermediate-I cytogenetic risk. Clin Lymphoma Myeloma Leuk 2012;12:438-43. DOI: 10.1016/j.clml.2012.05.007
45. Taksin AL, Legrand O, Raffoux E, de Revel T, Thomas X, Contentin N, Bouabdallah R, Pautas C, Turlure P, Reman O, Gardin C, Varet B, de Botton S, Pousset F, Farhat H, Chevret S, Dombret H, Castaigne S. High efficacy and safety profile of fractionated doses of Mylotarg as induction therapy in patients with relapsed acute myeloblastic leukemia: a prospective study of the alpha group. Leukemia 2007;21:66-71. DOI: 10.1038/sj.leu.2404434
46. Fianchi L, Pagano L, Leoni F, Storti S, Voso MT, Valentini CG, Rutella S, Scardocci A, Caira M, Gianfaldoni G, Leone G. Gemtuzumab, cytosine arabinoside, G-CSF combination (G-AraMy) in the treatment of elderly patients with poor-prognosis acute myeloid leukemia. Ann Oncol 2008;19:128-34. DOI: 10.1093/annonc/mdm451
47. Zhang Y, Liu J, Wang Y, Xian Q, Shao L, Yang Z, Wang X. Immunotherapy using IL-2 and GM-CSF is a potential treatment for multidrug-resistant Mycobacterium tuberculosis. Sci China Life Sci 2012;55:800-6. DOI: 10.1007/s11427-012-4368-x
48. Malagola M, Damiani D, Martinelli G, Michelutti A, Cesana B, Vivo AD, et al. Case-control study of multidrug resistance phenotype and response to induction treatment including or not fludarabine in newly diagnosed acute myeloid leukaemia patients. Br J Haematol 2007;136:87-95. DOI: 10.1111/j.1365-2141.2006.06390.x
49. Pallis M, Hills R, White P, Grundy M, Russell N, Burnett A. Analysis of the interaction of induction regimens with p-glycoprotein expression in patients with acute myeloid leukaemia: results from the MRC AML15 trial. Blood Cancer J 2011;1:2011-23. DOI: 10.1038/bcj.2011.23
50. Higashi Y, Turzanski J, Pallis M, Russell NH. Contrasting in vitro effects for the combination of fludarabine, cytosine arabinoside (Ara-C) and granulocyte colony-stimulating factor (FLAG) compared with daunorubicin and Ara-C in P-glycoprotein-positive and P-glycoprotein-negative acute myeloblastic leukaemia. Br J Haematol 2000;111:565-9.
51. Jabbour E, Garcia-Manero G, Cortes J, Ravandi F, Plunkett W, Gandhi V, Faderl S, O'Brien S, Borthakur G, Kadia T, Burger J, Konopleva M, Brandt M, Huang X, Kantarjian H. Twice-daily fludarabine and cytarabine combination with or without gentuzumab ozogamicin is effective in patients with relapsed/refractory acute myeloid Leukemia, high-risk myelodysplastic syndrome, and blast- phase chronic myeloid Leukemia. Clin Lymphoma Myeloma Leuk 2012;12:244-51. DOI: 10.1016/j.clml.2012.03.003
52. Tsimberidou A, Estey E, Cortes J, Thomas D, Faderl S, Verstovsek S, Garcia-Manero G, Keating M, Albitar M, O'Brien S, Kantarjian H, Giles F. Gemtuzumab, fludarabine,cytarabine, and cyclosporine in patients with newly diagnosed acutemyelogenous leukemia or high-risk myelodysplastic syndromes. Cancer 2003;97:1481-7.
53. Tsimberidou A, Cortes J, Thomas D, Garcia-Manero G, Verstovsek S, Faderl S, Albitar M, Kantarjian H, Estey E, Giles FJ. Gemtuzumab ozogamicin, fludarabine, cytarabine and cyclosporine combination regimen in patients with CD33+ primary resistant or relapsed acute myeloid leukemia. Leukemia Research 2003;27:893-7. DOI: 10.1016/S0145-2126(03)00022-5
54. List AF, Kopecky KJ, Willman CL, Head DR, Persons DL, Slovak ML, Dorr R, Karanes C, Hynes HE, Doroshow JH, Shurafa M, Appelbaum FR. Benefit of cyclosporine modulation of drug resistance in patients with poor-risk acute myeloid leukemia: a Southwest Oncology Group study. Blood 2001;98:3212-20. DOI: 10.1182/blood.V98.12.3212
55. Tamai I, Safa AR.Competitive interaction of cyclosporins with the Vinca alkaloid-binding site of P-glycoprotein in multidrug-resistant cells. J Biol Chem 1990;265:16509-13.
56. Tamai I, Safa AR. Azidopine non competitively interacts with vinblastine and cyclosporin A binding to P-glycoprotein in multidrug resistant cells. J Biol Chem 1991;266:16796-800.
57. Goldberg H, Ling V, Wong PY, Skorecki K. Reduced cyclosporin accumulation in multidrug-resistant cells. Biochem Biophys Res Commun 1988;152:552-8. DOI: 10.1016/S0006-291X(88)80073-1
58. Lum BL, Kaubisch S, Yahanda AM, Adler KM, Jew L, Ehsan MN, Brophy NA, Halsey J, Gosland MP, Sikic BI. Alteration of etoposide pharmacokinetics and pharmacodynamics by cyclosporine in a phase I trial to modulate multidrug resistance. J Clin Oncol 1992;10:1635-42.
59. Yahanda AM, Alder KM, Fisher GA, Brophy NA, Halsey J, Hardy RI, Gosland MP, Lum BL, Sikic BI. Phase I trial of etoposide with cyclosporine as a modulator of multidrug resistance. J Clin Oncol 1992;10:1624-34.
60. Pallis M, Russell N. Strategies for overcoming p-glycoprotein-mediated drug resistance in acute myeloblastic leukaemia. Leukemia 2004;18:1927-30. DOI: 10.1038/sj.leu.2403511
61. Turzanski J, Grundy M, Shang S, Russell N, Pallis M. P-glycoprotein is implicated in the inhibition of ceramide-induced apoptosis in TF-1 acute myeloid leukemia cells by modulation of the glucosylceramide synthase pathway. Exp Hematol 2005;33:62-72. DOI: 10.1016/j.exphem.2004.10.005
62. Linenberger ML, Hong T, Flowers D, Sievers EL, Gooley TA, Bennett JM, Berger MS, Leopold LH, Appelbaum FR, Bernstein ID. Multidrug-resistance phenotype and clinical responses to gemtuzumab ozogamicin. Blood 2001;98:988-94. DOI: 10.1182/blood.V98.4.988
63. Wattel E, Solary E, Hecquet B, Caillot D, Ifrah N, Brion A, Mahé B, Milpied N, Janvier M, Guerci A, Rochant H, Cordonnier C, Dreyfus F, Buzyn A, Hoang-Ngoc L, Stoppa AM, Gratecos N, Sadoun A, Stamatoulas A, Tilly H, Brice P, Maloisel F, Lioure B, Desablens B, Fenaux P, et al. Quinine improves the results of intensive chemotherapy in myelodysplastic syndromes expressing P glycoprotein: results of a randomized study. Br J Haematol 1998;102:1015-24. DOI: 10.1046/j.1365-2141.1998.00870.x
64. Jachez B, Cianfriglia M, Loor, F. Modulation of human P-glycoprotein epitope expression by temperature and/or resistance-modulating agents. Anti-Cancer Drugs 1994;5:655-65. DOI: 10.1097/00001813-199412000-00008
65. Matsui H, Takeshita A, Naito K, Shinjo K, Shigeno K, Maekawa M, Yamakawa Y, Tanimoto M, Kobayashi M, Ohnishi K, Ohno R.Reduced effect of gemtuzumab ozogamicin (CMA-676) on P-glycoprotein and/or CD34-positive leukemia cells and its restoration by multidrug resistance modifiers. Leukemia 2002;16:813-9. DOI: 10.1038/sj.leu.2402459
66. Greenberg PL, Lee SJ, Advani R, et al. Mitoxantrone, etoposide, and cytarabine with or without valspodar in patients with relapsed or refractory acute myeloid leukemia and high-risk myelodysplastic syndrome: a phase III trial (E2995). J Clin Oncol 2004;22:1078-86. DOI: 10.1200/JCO.2004.07.048
67. Baer MR, George SL, Dodge RK, et al. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and Leukemia Group B Study 9720. Blood 2002;100:1224-32.
68. Van der Holt B, Lowenberg B, Burnett AK, et al. The value of the MDR1 reversal agent PSC-833 in addition to daunorubicin and cytarabine in the treatment of elderly patients with previously untreated acute myeloid leukemia (AML), in relation to MDR1 status at diagnosis. Blood 2005;106:2646-54. DOI: 10.1182/blood-2005-04-1395
69. Baer MR, Cuviello NW, Shoemaker JS, Barrier Jr.R, Caligiuri, MA, Kolitz,JE, Powell BL, Larson RA, Bloomfield CD. Treatment failure is strongly predicted by P-glycoprotein (Pgp) function but not by multidrug resistance protein (MRP-1), breast cancer resistance protein (BCRP) or lung resistance protein (LRP) in acute myeloid leukemia (AML) patients 60 years and older receiving intensive chemotherapy (CALGB 9720/9760). Blood 2005;106:(abstr 661).
70. Kolitz JE, George SL, Marcucci G, Vij R, Powell BL, Allen SL, DeAngelo DJ, Shea TC, Stock W, Baer MR, Hars V, Maharry K, Hoke E, Vardiman JW, Bloomfield CD, Larson RA, Cancer and Leukemia Group B. P-glycoprotein inhibition using valspodar (PSC-833) does not improve outcomes for patients younger than age 60 years with newly diagnosed acute myeloid leukemia: Cancer and Leukemia Group B study 19808. Blood 2010;116:1413-21. DOI: 10.1182/blood-2009-07-229492
71. Morjani H, Madoulet C. Immunosuppressors as multidrug resistance reversal agents. Methods Mol Biol 2010;596:433-46. DOI: 10.1007/978-1-60761-416-6-19
72. Falasca M, Linton KJ .Investigational ABC transporter inhibitors. Expert Opin Investig Drugs 2012;21:657-66. DOI: 10.1517/13543784.2012.679339 DOI: 10.1182/blood-2010-04-277269
73. Cripe LD, Uno H, Paietta EM, Litzow MR, Ketterling RP, Bennett JM, Rowe JM, Lazarus HM, Luger S, Tallman MS. Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: a randomized, placebo-controlled trial of the Eastern Cooperative Oncology Group 3999. Blood 2010;116:4077-85.
74. Plasschaert SL, de Bont ES, Boezen M, et al. Expression of multidrug resistance-associated proteins predicts prognosis in childhood and adult acute lymphoblastic leukemia. Clin Cancer Res 2005;11:8661-8. DOI: 10.1158/1078-0432.CCR-05-1096
75. Gillet JP, Varma S, Gottesman MM. The clinical relevance of cancer cell lines. J Natl Cancer Inst 2013 (in press). DOI: 10.1093/jnci/djt007
76. Jiang K, He B, Lai L, Chen Q, Liu Y, Guo Q, Wang Q. Cyclosporine A inhibits breast cancer cell growth by downregulating the expression of pyruvate kinase subtype M2. Int J Mol Med 2012;30:302-8. DOI: 10.3892/ijmm.2012.989
77. De Souza PS, da Cunha Vasconcelos F, Silva LF, Maia RC. Cyclosporine A enables vincristine-induced apoptosis during reversal of multidrug resistance phenotype in chronic myeloid leukemia cells. Tumour Biol 2012;33:943-56. DOI: 10.1007/s13277-012-0323-5
78. Hernández GL, Volpert OV, Iñiguez MA, Lorenzo E, Martínez-Martínez S, Grau R, Fresno M, Redondo JM. Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J Exp Med 2001;193:607-20. DOI: 10.1084/jem.193.5.607
79. Matsouka P, Pagoni M, Zikos P, Giannakoulas N, Apostolidis I Asprogeraka T, et al. Addition of cyclosporin-A to chemotherapy in secondary (post-MDS) AML in the elderly. A multicenter randomized trial of the Leukemia Working Group of the Hellenic society of hematology. Ann Hematol 2006;85:250-6. DOI: 10.1007/s00277-005-0066-0
80. Liu Yin JA, Wheatley K, Rees JK, Burnett AK. Comparison of 'sequential' versus 'standard' chemotherapy as re-induction treatment, with or without cyclosporine, in refractory/relapsed acute myeloid leukaemia (AML): results of the UK Medical Research Council AML-R trial. Br J Haematol 2001;113:713-26. DOI: 10.1046/j.1365-2141.2001.02785.x
81. Pluchino KM, Hall MD, Goldsborough AS, Callaghan R, Gottesman MM. Collateral sensitivity as a strategy against cancer multidrug resistance. Drug Resist Updat 2012;15:98-105. DOI: 10.1016/j.drup.2012.03.002
82. Goldsborough AS, Handley MD, Dulcey AE, Pluchino KM, Kannan P, Brimacombe KR, Hall MD, Griffiths G, Gottesman MM. Collateral sensitivity of multidrug-resistant cells to the orphan drug tiopronin. J Med Chem 2011;54:4987-97. DOI: 10.1021/jm2001663
83. Dönmez Y, Akhmetova L, Ýthorneri ÖD, Kars MD, Gündüz U.Effect of MDR modulators verapamil and promethazine on gene expression levels of MDR1 and MRP1 in doxorubicin-resistant MCF-7 cells. Cancer Chemother Pharmacol 2011;67:823-8.
84. Bergman AM, Pinedo HM, Talianidis I, Veerman G, Loves WJ, van der Wilt CL, Peters GJ. Increased sensitivity to gemcitabine of P-glycoprotein and multidrug resistance-associated protein-overexpressing human cancer cell lines. Br J Cancer 2003;88:1963-70. DOI: 10.1007/s00280-010-1385-y
85. Advani AS, Shadman M, Ali-Osman F, Barker A, Rybicki L, Kalaycio M, Sekeres MA, de Castro CM, Diehl LF, Moore JO, Beaven A, Copelan E, Sobecks R, Talea P, Rizzieri DA. A Phase II trial of gemcitabine and mitoxantrone for patients with acute myeloid leukemia in first relapse. Clin Lymphoma Myeloma Leuk 2010;10:473-6. DOI: 10.1038/sj.bjc.6601011
86. Perl AE, Kasner MT, Shank D, Luger SM, Carroll M. Single-cell pharmacodynamic monitoring of S6 ribosomal protein phosphorylation in AML blasts during a clinical trial combining the mTOR inhibitor sirolimus and intensive chemotherapy. Clin Cancer Res 2012;18:1716-25. DOI: 10.3816/CLML.2010.n.082
87. Chiarini F, Lonetti A, Teti G, Orsini E, Bressanin D, Cappellini A, Ricci F, Tazzari PL, Ognibene A, Falconi M, Pagliaro P, Iacobucci I, Martinelli G, Amadori S, McCubrey JA, Martelli AM. A combination of temsirolimus, an allosteric mTOR inhibitor, with clofarabine as a new therapeutic option for patients with acute myeloid leukemia. Oncotarget 2013; (in press). DOI: 10.1158/1078-0432.CCR-11-2346
88. Medeiros BC, Landau HJ, Morrow M, Lockerbie RO, Pitts T, Eckhardt SG. The farnesyl transferase inhibitor, tipifarnib, is a potent inhibitor of the MDR1 gene product MDR1-Pgp and demonstrates significant cytotoxic synergism against human leukemia cell lines. Leukemia 2007;21:739-46.
89. Karp JE, Vener TI, Raponi M, Ritchie EK, Smith BD, Gore SD, Morris LE, Feldman EJ, Greer JM, Malek S, Carraway HE, Ironside V, Galkin S, Levis MJ, McDevitt MA, Roboz GR, Gocke CD, Derecho C, Palma J, Wang Y, Kaufmann SH, Wright JJ, Garret-Mayer E. Multi-institutional phase 2 clinical and pharmacogenomic trial of tipifarnib plus etoposide for elderly adults with newly diagnosed acute myelogenous leukemia. Blood 2012;119:55-63.
90. Jawad M, Yu N, Seedhouse C, Tandon K, Russell NH, Pallis M. Targeting of CD34+CD38- cells using Gemtuzumab ozogamicin (Mylotarg) in combination with tipifarnib (Zarnestra) in Acute Myeloid Leukaemia. BMC Cancer 2012;12:431-45. DOI: 10.1182/blood-2011-08-370825
91. Rosen DB, Harrington KH, Cordeiro JA, Leung LY, Putta S, Lacayo N, Laszlo GS, Gudgeon CJ, Hogge DE, Hawtin RE, Cesano A, Walter RB. AKT signaling as a novel factor associated with in vitro resistance of human AML to gemtuzumab ozogamicin. PLoS One 2013;8:1-10. DOI: 10.1186/1471-2407-12-431
92. Kovtun YV, Audette CA, Mayo MF, Jones GE, Doherty H, Maloney EK, Erickson HK, Sun X, Wilhelm S, Ab O, Lai KC, Widdison WC, Kellogg B, Johnson H, Pinkas J, Lutz RJ, Singh R, Goldmacher VS, Chari RV. Antibody-maytansinoid conjugates designed to bypass multidrug resistance. Cancer Res 2010;70:2528-37. DOI: 10.1371/journal.pone.0053518
93. Cianfriglia M, Cenciarelli C, Barca S, Tombesi M, Flego M, Dupuis ML. Monoclonal antibodies as a tool for structure-function studies of the MDR1-P-glycoprotein. Curr Protein Pept Sci 2002;3:513-30. DOI: 10.1158/0008-5472.CAN-09-3546
94. Cenciarelli C, Currier SJ, Willingham MC, Thiebaut F, Germann UA, Rutherford AV, Gottesman MM, Barca S, Tombesi M, Morrone S, Santoni A, Mariani M, Ramoni C, Dupuis ML, Cianfriglia M. Characterization by somatic cell genetics of a monoclonal antibody to the MDR1 gene product (P-glycoprotein): determination of P-glycoprotein expression in multi-drug-resistant KB and CEM cell variants. Int J Cancer 1991;49:394-407. DOI: 10.2174/1389203023380477
95. Mechetner EB, Roninson IB. Efficient inhibition of Pglycoprotein-mediated multidrug resistance with a monoclonal antibody. Proc Natl Acad Sci USA 1992;89:5824-8.
96. Ghetie MA, Ghetie V, Vitetta ES. Anti-CD19 antibodies inhibit the function of the P-gp pump in multidrug-resistant B lymphoma cells. Clin Cancer Res 1999;5:3920-7.
97. Ghetie MA, Marches R, Kufert S, Vitetta ES. An anti-CD19 antibody inhibits the interaction between P-lycoprotein (P-gp) and CD19, causes P-gp to translocate out of lipid rafts, and chemosensitizes a multidrug-resistant (MDR) lymphoma cell line. Blood 2004;104:178-83.
98. Tarasova NI, Seth R, Tarasov SG, Kosakowska-Cholody T, Hrycyna CA, Gottesman MM, Michejda CJ. Transmembrane inhibitors of P-glycoprotein, an ABC transporter. J Med Chem 2005;48:3768-75.
99. Pawlak-Roblin C, Tosi PF, Perrin L, Devy J, Venteo L, Albert P, Nicolau C, Madoulet C. Inhibition of multidrug resistance by immunisation with synthetic P-glycoprotein-derived peptides. Eur J Cancer 2004;40(4):606-13. DOI: 10.1021/jm049065t
100. Lin TL, Levy MY. Acute myeloid leukemia: focus on novel therapeutic strategies. Clin Med Insights Oncol 2012;6:205-17. DOI: 10.1016/j.ejca.2003.11. 019
101. Roboz GJ. Current treatment of acute myeloid leukemia. Curr Opin Oncol 2012;24:711-9. DOI: 10.4137/CMO.S7244
102. Burnett AK, Hills RK, Milligan D, Kjeldsen L, Kell J, Russell NH, Yin JA, Hunter A, Goldstone AH, Wheatley K. Identification of patients with acute myeloblastic leukemia who benefit from the addition of gemtuzumab ozogamicin: results of the MRC AML15 trial. J Clin Oncol 2011;29:369-77. DOI: 10.1097/CCO.0b013e328358f62d
103. Ravandi F, Estey EH, Appelbaum FR, Lo-Coco F, Schiffer CA, Larson RA, Burnett AK, Kantarjian HM. Gemtuzumab ozogamicin: time to resurrect? J Clin Oncol 2012;30:3921-3. DOI: 10.1200/JCO.2010.31.4310
104. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, McMichael JF, Wallis JW, Lu C, Shen D, Harris CC, Dooling DJ, Fulton RS, Fulton LL, Chen K, Schmidt H, Kalicki-Veizer J, Magrini VJ, Cook L, McGrath SD, Vickery TL, Wendl MC, Heath S, Watson MA, Link DC, Tomasson MH, Shannon WD, Payton JE, Kulkarni S, Westervelt P, Walter MJ, Graubert TA, Mardis ER, Wilson RK, DiPersio JF. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012;481:506-10. DOI: 10.1200/JCO.2012.43.0132
105. Mortland L, Alonzo TA, Walter RB, Gerbing RB, Mitra AK, Pollard JA, Loken MR, Hirsch B, Raimondi S, Franklin J, Pounds S, Cao X, Rubnitz JE, Ribeiro RC, Gamis A, Meshinchi S, Lamba JK. Clinical Significance of CD33 Nonsynonymous Single-Nucleotide Polymorphisms in Pediatric Patients with Acute Myeloid Leukemia Treated with Gemtuzumab-Ozogamicin-Containing Chemotherapy. Clin Cancer Res 2013;19:1620-7. DOI: 10.1038/nature10738
106. Boghaert ER, et al. Tumoricidal effect of calicheamicin immuno-conjugates using a passive targeting strategy. Int J Oncol 2006;28:675-84. DOI: 10.1158/1078-0432.CCR-12-3115
107. Jedema I, Barge RM, van der Velden VH, Nijmeijer BA, van Dongen JJ, Willemze R, Falkenburg JH. Internalization and cell cycle-dependent killing of leukemic cells by Gemtuzumab Ozogamicin: rationale for efficacy in CD33-negative malignancies with endocytic capacity. Leukemia 2004;18:316-25. DOI: 10.1038/sj.leu.2403205
108. Mahadevan D, List AF. Targeting the multidrug resistance- 1 transporter in AML: molecular regulation and therapeutic strategies. Blood 2004;104:1940-51. DOI: 10.1182/blood-2003-07-2490
109. Govindan SV, Goldenberg DM. Designing immunoconjugates for cancer therapy. Expert Opin Biol Ther 2012;12:873-90. DOI: 10.1517/14712598.2012.685153
110. Kim KM, McDonagh CF, Westendorf L, Brown LL, Sussman D, Feist T, Lyon R, Alley SC, Okeley NM, Zhang X, Thompson MC, Stone I, Gerber HP, Carter PJ. Anti-CD30 diabody-drug conjugates with potent antitumor activity. Mol Cancer Ther 2008;7:2486-97. DOI: 10.1158/1535-7163.MCT-08-0388
111. Holliger P, Prospero T, Winter G. "Diabodies": small bivalent and bispecific antibody fragments. Proc Natl Aca Sci USA 1993;90:6444-8. DOI: 10.1073/pnas.90.14.6444
112. Li E, Pedraza A, Bestagno M, Mancardi S, Sanchez R, Burrone O. Mammalian cell expression of dimeric small immune proteins (SIP). Protein Eng 1997;10:731-6. DOI: 10.1093/protein/10.6.731
113. Beck A. Biosimilar, biobetter and next generation therapeutic antibodies. MAbs 2011;3:107-10. DOI: 10.4161/mabs.3.2.14785