The mechanism of chemoresistance against tyrosine kinase inhibitors in malignant glioma

Brain Tumor Pathology

Volumn 31, Issue 3, 2014, Pages 198-207

  Nakada, Mitsutoshi ^a   Kita, Daisuke ^a   Watanabe, Takuya ^a   Hayashi, Yutaka ^a   Hamada, Jun Ichiro ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

Chemoresistance; Glioma; Tyrosine kinase inhibitor

Indexed keywords

AFATINIB; BEVACIZUMAB; CABOZANTINIB; CEDIRANIB; CETUXIMAB; DACOMITINIB; DASATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; HYDROXYUREA; IMATINIB; LAPATINIB; NIMOTUZUMAB; ONARTUZUMAB; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN TYROSINE KINASE INHIBITOR; RAPAMYCIN; RILOTUMUMAB; SCATTER FACTOR RECEPTOR; SORAFENIB; SU 10944; SUNITINIB; TANDUTINIB; TEMOZOLOMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANDETANIB; VASCULOTROPIN INHIBITOR; ENZYME INHIBITOR; PROTEIN TYROSINE KINASE;

ABDOMINAL PAIN; ALKALINE PHOSPHATASE BLOOD LEVEL; AMYLASE BLOOD LEVEL; ANEMIA; ANOREXIA; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; BLOOD BRAIN BARRIER; BLOOD TOXICITY; BRAIN EDEMA; BRAIN HEMORRHAGE; CANCER INHIBITION; CARDIOVASCULAR DISEASE; CENTRAL NERVOUS SYSTEM DISEASE; CONFUSION; CONJUNCTIVITIS; CONSTIPATION; DEEP VEIN THROMBOSIS; DEHYDRATION; DIARRHEA; DRUG BINDING SITE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG EXCRETION; DRUG FATALITY; DRUG METABOLISM; DRUG PENETRATION; DRUG TARGETING; DRUG TOLERABILITY; DRUG TRANSPORT; DRY SKIN; DYSPNEA; EDEMA; ELECTROLYTE BLOOD LEVEL; FATIGUE; FEBRILE NEUTROPENIA; FEVER; GASTROINTESTINAL TOXICITY; GLIOBLASTOMA; GLIOMA; HAND FOOT SYNDROME; HEADACHE; HUMAN; HYPERTENSION; HYPOALBUMINEMIA; HYPOKALEMIA; HYPOMAGNESEMIA; HYPOPHOSPHATEMIA; HYPOTENSION; INFECTION; LEUKOPENIA; LUNG EDEMA; LUNG TOXICITY; LYMPHOCYTOPENIA; MOLECULARLY TARGETED THERAPY; MUCOSA INFLAMMATION; MUSCLE DISEASE; MUSCLE WEAKNESS; NAUSEA; NEPHROTOXICITY; NEUTROPENIA; PHASE 2 CLINICAL TRIAL (TOPIC); PNEUMOCYSTIS PNEUMONIA; PROTEINURIA; RASH; REVIEW; SEIZURE; SEPSIS; SIGNAL TRANSDUCTION; SKIN TOXICITY; STOMATITIS; THROMBOCYTOPENIA; TREATMENT RESPONSE; TRIACYLGLYCEROL LIPASE BLOOD LEVEL; TUMOR RESISTANCE; UNSPECIFIED SIDE EFFECT; URINARY TRACT DISEASE; URINE INCONTINENCE; VOMITING; ANTAGONISTS AND INHIBITORS; DRUG RESISTANCE; GENETICS; PATHOLOGY; PHYSIOLOGY;

DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; GLIOBLASTOMA; HUMANS; MOLECULAR TARGETED THERAPY; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 84905120812     PISSN: 14337398     EISSN: 1861387X     Source Type: Journal    
DOI: 10.1007/s10014-013-0174-9     Document Type: Review

References (50)

1. Dumur CI, Idowu MO, Powers CN (2013) Targeting tyrosine kinases in cancer: the converging roles of cytopathology and molecular pathology in the era of genomic medicine. Cancer Cytopathol 121:61-71
2. Nakada M, Kita D, Watanabe T, Hayashi Y, Teng L, Pyko IV, Hamada J (2011) Aberrant signaling pathways in glioma. Cancers 3:3242-3278
3. Hegi ME, Rajakannu P, Weller M (2012) Epidermal growth factor receptor: a re-emerging target in glioblastoma. Curr Opin Neurol 25:774-779
4. Tanaka S, Louis DN, Curry WT, Batchelor TT, Dietrich J (2013) Diagnostic and therapeutic avenues for glioblastoma: no longer a dead end? Nat Rev Clin Oncol 10:14-26
5. Chi AS, Batchelor TT, Kwak EL, Clark JW, Wang DL, Wilner KD, Louis DN, Iafrate AJ (2012) Rapid radiographic and clinical improvement after treatment of a MET-amplified recurrent glioblastoma with a mesenchymal-epithelial transition inhibitor. J Clin Oncol 30:e30-e33
6. Prados MD, Chang SM, Butowski N, DeBoer R, Parvataneni R, Carliner H, Kabuubi P, Ayers-Ringler J, Rabbitt J, Page M, Fedoroff A, Sneed PK, Berger MS, McDermott MW, Parsa AT, Vandenberg S, James CD, Lamborn KR, Stokoe D, Haas-Kogan DA (2009) Phase II study of erlotinib plus temozolomide during and after radiation therapy in patients with newly diagnosed glioblastoma multiforme or gliosarcoma. J Clin Oncol 27:579-584
7. Raizer JJ, Abrey LE, Lassman AB, Chang SM, Lamborn KR, Kuhn JG, Yung WK, Gilbert MR, Aldape KA, Wen PY, Fine HA, Mehta M, Deangelis LM, Lieberman F, Cloughesy TF, Robins HI, Dancey J, Prados MD (2010) A phase II trial of erlotinib in patients with recurrent malignant gliomas and nonprogressive glioblastoma multiforme postradiation therapy. Neuro Oncol 12:95-103
8. Peereboom DM, Shepard DR, Ahluwalia MS, Brewer CJ, Agarwal N, Stevens GH, Suh JH, Toms SA, Vogelbaum MA, Weil RJ, Elson P, Barnett GH (2010) Phase II trial of erlotinib with temozolomide and radiation in patients with newly diagnosed glioblastoma multiforme. J Neurooncol 98:93-99
9. Mukasa A, Wykosky J, Ligon KL, Chin L, Cavenee WK, Furnari F (2010) Mutant EGFR is required for maintenance of glioma growth in vivo, and its ablation leads to escape from receptor dependence. Proc Natl Acad Sci USA 107:2616-2621
10. Weller M, Stupp R, Hegi M, Wick W (2012) Individualized targeted therapy for glioblastoma: fact or fiction? Cancer J 18:40-44
11. Szerlip NJ, Pedraza A, Chakravarty D, Azim M, McGuire J, Fang Y, Ozawa T, Holland EC, Huse JT, Jhanwar S, Leversha MA, Mikkelsen T, Brennan CW (2012) Intratumoral heterogeneity of receptor tyrosine kinases EGFR and PDGFRA amplification in glioblastoma defines subpopulations with distinct growth factor response. Proc Natl Acad Sci USA 109:3041-3046
12. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R, Stegh AH, Bradner JE, Ligon KL, Brennan C, Chin L, DePinho RA (2007) Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318:287-290 (Pubitemid 47574858)
13. Network CGAR (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061-1068
14. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807-1812
15. Rich JN, Rasheed BK, Yan H (2004) EGFR mutations and sensitivity to gefitinib. N Engl J Med 351:1260-1261
16. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, Lu KV, Yoshimoto K, Huang JH, Chute DJ, Riggs BL, Horvath S, Liau LM, Cavenee WK, Rao PN, Beroukhim R, Peck TC, Lee JC, Sellers WR, Stokoe D, Prados M, Cloughesy TF, Sawyers CL, Mischel PS (2005) Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353:2012-2024 (Pubitemid 41609094)
17. De Witt Hamer PC (2010) Small molecule kinase inhibitors in glioblastoma: a systematic review of clinical studies. Neuro Oncol 12:304-316
18. Snuderl M, Fazlollahi L, Le LP, Nitta M, Zhelyazkova BH, Davidson CJ, Akhavanfard S, Cahill DP, Aldape KD, Betensky RA, Louis DN, Iafrate AJ (2011) Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 20:810-817
19. Little SE, Popov S, Jury A, Bax DA, Doey L, Al-Sarraj S, Jurgensmeier JM, Jones C (2012) Receptor tyrosine kinase genes amplified in glioblastoma exhibit a mutual exclusivity in variable proportions reflective of individual tumor heterogeneity. Cancer Res 72:1614-1620
20. Reardon DA, Desjardins A, Vredenburgh JJ, Gururangan S, Friedman AH, Herndon JE 2nd, Marcello J, Norfleet JA, McLendon RE, Sampson JH, Friedman HS (2010) Phase 2 trial of erlotinib plus sirolimus in adults with recurrent glioblastoma. J Neurooncol 96:219-230
21. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-760 (Pubitemid 44949604)
22. Huang Z, Cheng L, Guryanova OA, Wu Q, Bao S (2010) Cancer stem cells in glioblastoma-molecular signaling and therapeutic targeting. Protein Cell 1:638-655
23. Ozvegy-Laczka C, Cserepes J, Elkind NB, Sarkadi B (2005) Tyrosine kinase inhibitor resistance in cancer: role of ABC multidrug transporters. Drug Resist Update 8:15-26 (Pubitemid 40797953)
24. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG (2005) Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2? and ABCG2- cancer cells are similarly tumorigenic. Cancer Res 65:6207-6219 (Pubitemid 40994406)
25. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW, Holland EC (2009) PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4:226-235
26. Ozvegy-Laczka C, Hegedus T, Varady G, Ujhelly O, Schuetz JD, Varadi A, Keri G, Orfi L, Nemet K, Sarkadi B (2004) Highaffinity interaction of tyrosine kinase inhibitors with the ABCG2 multidrug transporter. Mol Pharmacol 65:1485-1495 (Pubitemid 38668306)
27. Yanase K, Tsukahara S, Asada S, Ishikawa E, Imai Y, Sugimoto Y (2004) Gefitinib reverses breast cancer resistance proteinmediated drug resistance. Mol Cancer Ther 3:1119-1125 (Pubitemid 39295009)
28. Wang XK, Fu LW (2010) Interaction of tyrosine kinase inhibitors with the MDR-related ABC transporter proteins. Curr Drug Metab 11:618-628
29. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME (2007) Molecular targets of glioma invasion. Cell Mol Life Sci 64:458-478
30. Nakada M, Kita D, Teng L, Pyko IV, Watanabe T, Hayashi Y, Hamada J (2013) Receptor tyrosine kinases: principles and functions in glioma invasion. Adv Exp Med Biol 986:143-170
31. Hatzikirou H, Basanta D, Simon M, Schaller K, Deutsch A (2012) 'Go or grow': the key to the emergence of invasion in tumour progression? Math Med Biol 29:49-65
32. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, Thorsen F, Taxt T, Bartos M, Jirik R, Miletic H, Wang J, Stieber D, Stuhr L, Moen I, Rygh CB, Bjerkvig R, Niclou SP (2011) Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci USA 108:3749-3754
33. Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I, Garren N, Mackey M, Butman JA, Camphausen K, Park J, Albert PS, Fine HA (2009) Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 27:740-745
34. Friedman HS, Prados MD, Wen PY, Mikkelsen T, Schiff D, Abrey LE, Yung WK, Paleologos N, Nicholas MK, Jensen R, Vredenburgh J, Huang J, Zheng M, Cloughesy T (2009) Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 27:4733-4740
35. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, Inoue M, Bergers G, Hanahan D, Casanovas O (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15:220-231
36. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15:232-239
37. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, Kozak KR, Cahill DP, Chen PJ, Zhu M, Ancukiewicz M, Mrugala MM, Plotkin S, Drappatz J, Louis DN, Ivy P, Scadden DT, Benner T, Loeffler JS, Wen PY, Jain RK (2007) AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11:83-95 (Pubitemid 46075199)
38. Vivanco I, Robins HI, Rohle D, Campos C, Grommes C, Nghiemphu PL, Kubek S, Oldrini B, Chheda MG, Yannuzzi N, Tao H, Zhu S, Iwanami A, Kuga D, Dang J, Pedraza A, Brennan CW, Heguy A, Liau LM, Lieberman F, Yung WK, Gilbert MR, Reardon DA, Drappatz J, Wen PY, Lamborn KR, Chang SM, Prados MD, Fine HA, Horvath S, Wu N, Lassman AB, DeAngelis LM, Yong WH, Kuhn JG, Mischel PS, Mehta MP, Cloughesy TF, Mellinghoff IK (2012) Differential sensitivity of glioma- versus lung cancer-specific EGFR mutations to EGFR kinase inhibitors. Cancer Discov 2:458-471
39. Schwechheimer K, Huang S, Cavenee WK (1995) EGFR gene amplification-rearrangement in human glioblastomas. Int J Cancer 62:145-148
40. Leis JF, Stepan DE, Curtin PT, Ford JM, Peng B, Schubach S, Druker BJ, Maziarz RT (2004) Central nervous system failure in patients with chronic myelogenous leukemia lymphoid blast crisis and Philadelphia chromosome positive acute lymphoblastic leukemia treated with imatinib (STI-571). Leuk Lymphoma 45:695-698 (Pubitemid 38256028)
41. Glavinas H, Krajcsi P, Cserepes J, Sarkadi B (2004) The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 1:27-42
42. Dai H, Marbach P, Lemaire M, Hayes M, Elmquist WF (2003) Distribution of STI-571 to the brain is limited by P-glycoproteinmediated efflux. J Pharmacol Exp Ther 304:1085-1092 (Pubitemid 36254421)
43. Burger H, van Tol H, Boersma AW, Brok M, Wiemer EA, Stoter G, Nooter K (2004) Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump. Blood 104:2940-2942 (Pubitemid 39434984)
44. Polli JW, Olson KL, Chism JP, John-Williams LS, Yeager RL, Woodard SM, Otto V, Castellino S, Demby VE (2009) An unexpected synergist role of P-glycoprotein and breast cancer resistance protein on the central nervous system penetration of the tyrosine kinase inhibitor lapatinib (N-{3-chloro-4-[(3-fluorobenzyl) oxy]phenyl}-6-[5-({[2-(methylsulfonyl) ethyl]amino}methyl)-2-furyl]-4-quinazolinamine; GW572016). Drug Metab Dispos 37:439-442
45. Agarwal S, Manchanda P, Vogelbaum MA, Ohlfest JR, Elmquist WF (2013) Function of the blood-brain barrier and restriction of drug delivery to invasive glioma cells: findings in an orthotopic rat xenograft model of glioma. Drug Metab Dispos 41:33-39
46. Kodaira H, Kusuhara H, Ushiki J, Fuse E, Sugiyama Y (2010) Kinetic analysis of the cooperation of P-glycoprotein (P-gp/ Abcb1) and breast cancer resistance protein (Bcrp/Abcg2) in limiting the brain and testis penetration of erlotinib, flavopiridol, and mitoxantrone. J Pharmacol Exp Ther 333:788-796
47. Elmeliegy MA, Carcaboso AM, Tagen M, Bai F, Stewart CF (2011) Role of ATP-binding cassette and solute carrier transporters in erlotinib CNS penetration and intracellular accumulation. Clin Cancer Res 17:89-99
48. Tang SC, Lankheet NA, Poller B, Wagenaar E, Beijnen JH, Schinkel AH (2012) P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) restrict brain accumulation of the active sunitinib metabolite N-desethyl sunitinib. J Pharmacol Exp Ther 341:164-173
49. van Erp NP, Gelderblom H, Guchelaar HJ (2009) Clinical pharmacokinetics of tyrosine kinase inhibitors. Cancer Treat Rev 35:692-706
50. Del Vecchio CA, Li G, Wong AJ (2012) Targeting EGF receptor variant III: tumor-specific peptide vaccination for malignant gliomas. Expert Rev Vaccines 11:133-144