Basic mechanisms of therapeutic resistance to radiation and chemotherapy in lung cancer

Cancer Journal (United States)

Volumn 19, Issue 3, 2013, Pages 200-207

  Willers, Henning ^a   Azzoli, Christopher G ^a   Santivasi, Wil L ^b   Xia, Fen ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Cytotoxic therapies; DNA repair pathways; Lung cancer

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; ANTIMETABOLITE; CISPLATIN; DNA TOPOISOMERASE INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; MULTIDRUG RESISTANCE PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; PHOSPHATIDYLINOSITOL 3 KINASE; PLATINUM DERIVATIVE; PROTEIN TYROSINE KINASE INHIBITOR; VINCA ALKALOID;

CANCER PROGNOSIS; CANCER SIZE; CANCER STEM CELL; CELL CYCLE ARREST; CELL DEATH; CELL GROWTH; CELL HYPOXIA; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHEMORADIOTHERAPY; CYTOPENIA; CYTOTOXICITY; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; FATIGUE; GENE MUTATION; GENOMIC INSTABILITY; GLUTATHIONE METABOLISM; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; KIDNEY INJURY; LUNG CANCER; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; NAUSEA; NERVE INJURY; OVERALL SURVIVAL; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RADIATION DOSE; RADIATION INJURY; RADIOSENSITIVITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; STEREOTACTIC BODY RADIATION THERAPY; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

ANIMALS; CELL HYPOXIA; CELL PROLIFERATION; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; RADIATION TOLERANCE; TUMOR BURDEN; TUMOR MARKERS, BIOLOGICAL;

EID: 84880109173     PISSN: 15289117     EISSN: 1540336X     Source Type: Journal    
DOI: 10.1097/PPO.0b013e318292e4e3     Document Type: Review

References (101)

1. Willers H, Pfäffle HN, Zou L. Targeting homologous recombination repair in cancer. In: Kelley MR, ed. DNA Repair in Cancer Therapy: Molecular Targets and Clinical Applications. London: Academic Press, Elsevier; 2012:119-160.
2. Birkelbach M, Ferraiolo N, Gheorghiu L, et al. Detection of impaired homologous recombination repair in NSCLC cells and tissues. J Thorac Oncol. 2013;8:279-286.
3. Helleday T, Petermann E, Lundin C, et al. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer. 2008;8:193-204.
4. Willers H, Held KD. Introduction to clinical radiation biology. Hematol Oncol Clin North Am. 2006;20:1-24.
5. Baumann M, Krause M, Dikomey E, et al. EGFR-targeted anti-cancer drugs in radiotherapy: preclinical evaluation of mechanisms. Radiother Oncol. 2007;83:238-248.
6. Krause M, Yaromina A, Eicheler W, et al. Cancer stem cells: targets and potential biomarkers for radiotherapy. Clin Cancer Res. 2011;17: 7224-7229.
7. O'Flaherty JD, Barr M, Fennell D, et al. The cancer stem-cell hypothesis: its emerging role in lung cancer biology and its relevance for future therapy. J Thorac Oncol. 2012;7:1880-1890.
8. Dubben HH, Thames HD, Beck-Bornholdt HP. Tumor volume: a basic and specific response predictor in radiotherapy. Radiother Oncol. 1998;47:167-174.
9. Yaromina A, Krause M, Thames H, et al. Pre-treatment number of clonogenic cells and their radiosensitivity are major determinants of local tumour control after fractionated irradiation. Radiother Oncol. 2007;83:304-310.
10. Alexander BM, Othus M, Caglar HB, et al. Tumor volume is a prognostic factor in non-small-cell lung cancer treated with chemoradiotherapy. Int J Radiat Oncol Biol Phys. 2011;79:1381-1387.
11. Soliman M, Yaromina A, Appold S, et al. GTV differentially impacts locoregional control of non-small cell lung cancer (NSCLC) after different fractionation schedules: subgroup analysis of the prospective randomized CHARTWEL trial. Radiother Oncol. 2013 Jan 16 [Epub ahead of print].
12. Werner-Wasik M, Swann RS, Bradley J, et al. Increasing tumor volume is predictive of poor overall and progression-free survival: secondary analysis of the Radiation Therapy Oncology Group 93-11 phase I-II radiation dose-escalation study in patients with inoperable non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 2008;70:385-390.
13. Zhao L, West BT, Hayman JA, et al. High radiation dose may reduce the negative effect of large gross tumor volume in patients with medically inoperable early-stage non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 2007;68:103-110.
14. Le Chevalier T, Arriagada R, Quoix E, et al. Radiotherapy alone versus combined chemotherapy and radiotherapy in nonresectable non-small-cell lung cancer: first analysis of a randomized trial in 353 patients. J Natl Cancer Inst. 1991;83:417-423.
15. Curran WJ Jr, Paulus R, Langer CJ, et al. Sequential vs. concurrent chemoradiation for stage III non-small cell lung cancer: randomized phase III trial RTOG 9410. J Natl Cancer Inst. 2011;103:1452-1460.
16. Cox JD. Are the results of RTOG 0617 mysterious? Int J Radiat Oncol Biol Phys. 2012;82:1042-1044.
17. Ausborn NL, Le QT, Bradley JD, et al. Molecular profiling to optimize treatment in non-small cell lung cancer: a review of potential molecular targets for radiation therapy by the translational research program of the radiation therapy oncology group. Int J Radiat Oncol Biol Phys. 2012;83:e453-e464.
18. Provencio M, Sanchez A, Garrido P, et al. New molecular targeted therapies integrated with radiation therapy in lung cancer. Clin Lung Cancer. 2010;11:91-97.
19. Neal JW, Sequist LV. First-line use of EGFR tyrosine kinase inhibitors in patients with NSCLC containing EGFR mutations. Clin Adv Hematol Oncol. 2010;8:119-126.
20. Sharma SV, Lee DY, Li B, et al. A chromatin-mediated reversible drugtolerant state in cancer cell subpopulations. Cell. 2010;141:69-80.
21. Kim JJ, Tannock IF. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer. 2005;5:516-525.
22. Krause M, Zips D, Thames HD, et al. Preclinical evaluation of molecular-targeted anticancer agents for radiotherapy. Radiother Oncol. 2006;80:112-122.
23. Saunders M, Dische S, Barrett A, et al. Continuous hyperfractionated accelerated radiotherapy (CHART) versus conventional radiotherapy in non-small-cell lung cancer: a randomised multicentre trial. CHART Steering Committee. Lancet. 1997;350:161-165.
24. TurrisiAT 3rd, KimK, BlumR, et al. Twice-daily comparedwith once-daily thoracic radiotherapy in limited small-cell lung cancer treated concurrently with cisplatin and etoposide. N Engl J Med. 1999;340:265-271.
25. Baumann M, Herrmann T, Koch R, et al. Final results of the randomized phase III CHARTWEL-trial (ARO 97-1) comparing hyperfractionatedaccelerated versus conventionally fractionated radiotherapy in non-small cell lung cancer (NSCLC). Radiother Oncol. 2011;100:76-85.
26. Machtay M, Hsu C, Komaki R, et al. Effect of overall treatment time on outcomes after concurrent chemoradiation for locally advanced non-small-cell lung carcinoma: analysis of the Radiation Therapy Oncology Group (RTOG) experience. Int J Radiat Oncol Biol Phys. 2005;63:667-671.
27. Milas L, Nakayama T, Hunter N, et al. Dynamics of tumor cell clonogen repopulation in a murine sarcoma treated with cyclophosphamide. Radiother Oncol. 1994;30:247-253.
28. Chen CP, Weinberg VK, Jahan TM, et al. Implications of delayed initiation of radiotherapy: accelerated repopulation after induction chemotherapy for stage III non-small cell lung cancer. J Thorac Oncol. 2011;6:1857-1864.
29. El Sharouni SY, Kal HB, Battermann JJ. Accelerated regrowth of non-small-cell lung tumours after induction chemotherapy. Br J Cancer. 2003;89:2184-2189.
30. Huang Q, Li F, Liu X, et al. Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med. 2011;17:860-866.
31. Bentzen SM, Atasoy BM, Daley FM, et al. Epidermal growth factor receptor expression in pretreatment biopsies from head and neck squamous cell carcinoma as a predictive factor for a benefit from accelerated radiation therapy in a randomized controlled trial. J Clin Oncol. 2005;23:5560-5567.
32. Krause M, Ostermann G, Petersen C, et al. Decreased repopulation as well as increased reoxygenation contribute to the improvement in local control after targeting of the EGFR by C225 during fractionated irradiation. Radiother Oncol. 2005;76:162-167.
33. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62.
34. Nieder C, Bremnes RM. Effects of smoking cessation on hypoxia and its potential impact on radiation treatment effects in lung cancer patients. Strahlenther Onkol. 2008;184:605-609.
35. Hoff CM, Grau C, Overgaard J. Effect of smoking on oxygen delivery and outcome in patients treated with radiotherapy for head and neck squamous cell carcinoma - a prospective study. Radiother Oncol. 2012;103:38-44.
36. Langendijk H, de Jong J, Wanders R, et al. The importance of pretreatment haemoglobin level in inoperable non-small cell lung carcinoma treated with radical radiotherapy. Radiother Oncol. 2003;67:321-325.
37. Horsman MR, Mortensen LS, Petersen JB, et al. Imaging hypoxia to improve radiotherapy outcome. Nat Rev Clin Oncol. 2012;9:674-687.
38. Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapynaive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol. 2008;26:3543-3551.
39. Socinski MA, Smit EF, Lorigan P, et al. Phase III study of pemetrexed plus carboplatin compared with etoposide plus carboplatin in chemotherapy-naive patients with extensive-stage small-cell lung cancer. J Clin Oncol. 2009;27:4787-4792.
40. Spiro SG, Rudd RM, Souhami RL, et al. Chemotherapy versus supportive care in advanced non-small cell lung cancer: improved survival without detriment to quality of life. Thorax. 2004;59:828-836.
41. Azzoli CG, Baker S Jr, Temin S, et al. American Society of Clinical Oncology Clinical Practice Guideline update on chemotherapy for stage IV non-small-cell lung cancer. J Clin Oncol. 2009;27:6251-6266.
42. NCCN Guidelines: Non-Small Cell Lung Cancer. 2013.
43. Fukuoka M, Wu YL, Thongprasert S, et al. Biomarker analyses and final overall survival results from a phase III, randomized, open-label, first-line study of gefitinib versus carboplatin/paclitaxel in clinically selected patients with advanced non-small-cell lung cancer in Asia (IPASS). J Clin Oncol. 2011;29:2866-2874.
44. Shaw AT, Yeap BY, Solomon BJ, et al. Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol. 2011; 12:1004-1012.
45. Sequist LV, Waltman BA, Dias-Santagata D, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med. 2011;3:75ra26.
46. Turke AB, Zejnullahu K, Wu YL, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell. 2010;17:77-88.
47. Galluzzi L, Senovilla L, Vitale I, et al. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31:1869-1883.
48. Chen KG, Sikic BI. Molecular pathways: regulation and therapeutic implications of multidrug resistance. Clin Cancer Res. 2012;18:1863-1869.
49. Sau A, Pellizzari Tregno F, Valentino F, et al. Glutathione transferases and development of new principles to overcome drug resistance. Arch Biochem Biophys. 2010;500:116-122.
50. Filipits M, Pirker R, Dunant A, et al. Cell cycle regulators and outcome of adjuvant cisplatin-based chemotherapy in completely resected non-small-cell lung cancer: the International Adjuvant Lung Cancer Trial Biologic Program. J Clin Oncol. 2007;25:2735-2740.
51. Tsao MS, Aviel-Ronen S, Ding K, et al. Prognostic and predictive importance of p53 and RAS for adjuvant chemotherapy in non small-cell lung cancer. J Clin Oncol. 2007;25:5240-5247.
52. Brambilla E, Bourredjem A, Lantuejoul S, et al. Bax expression as a predictive marker of survival benefit in non-small cell lung carcinoma treated by adjuvant cisplatin-based chemotherapy. J Thorac Oncol. 2010;5(12 suppl 7):S503.
53. Olaussen KA, Dunant A, Fouret P, et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med. 2006;355:983-991.
54. Kamal NS, Soria JC, Mendiboure J, et al. MutS homologue 2 and the long-term benefit of adjuvant chemotherapy in lung cancer. Clin Cancer Res. 2010;16:1206-1215.
55. Willers H, Dahm-Daphi J, Powell SN. Repair of radiation damage to DNA. Br J Cancer. 2004;90:1297-1301.
56. Wei Q, Cheng L, Hong WK, et al. Reduced DNA repair capacity in lung cancer patients. Cancer Res. 1996;56:4103-4107.
57. Frosina G. DNA repair and resistance of gliomas to chemotherapy and radiotherapy. Mol Cancer Res. 2009;7:989-999.
58. Hagiwara H, Sunada Y. Mechanism of taxane neurotoxicity. Breast Cancer. 2004;11:82-85.
59. Chattopadhyay S, Moran RG, Goldman ID. Pemetrexed: biochemical and cellular pharmacology, mechanisms, and clinical applications. Mol Cancer Ther. 2007;6:404-417.
60. Pauwels B, Korst AE, Pattyn GG, et al. Cell cycle effect of gemcitabine and its role in the radiosensitizing mechanism in vitro. Int J Radiat Oncol Biol Phys. 2003;57:1075-1083.
61. Lieber MR, Ma Y, Pannicke U, et al. Mechanism and regulation of human non-homologousDNAend-joining.Nat RevMolCell Biol. 2003;4:712-720.
62. Shibata A, Conrad S, Birraux J, et al. Factors determining DNA doublestrand break repair pathway choice in G2 phase.EMBOJ. 2011;30:1079-1092.
63. Weterings E, Chen DJ. The endless tale of non-homologous end-joining. Cell Res. 2008;18:114-124.
64. Spagnolo L, Rivera-CalzadaA, Pearl LH, et al. Three-dimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol Cell. 2006;22:511-519.
65. Moll U, Lau R, Sypes MA, et al. DNA-PK, the DNA-activated protein kinase, is differentially expressed in normal and malignant human tissues. Oncogene. 1999;18:3114-3126.
66. Ma Y, Pannicke U, Schwarz K, et al. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell. 2002; 108:781-794.
67. Suzuki K, Kodama S, Watanabe M. Recruitment of ATM protein to double strand DNA irradiated with ionizing radiation. J Biol Chem. 1999;274:25571- 25575.
68. Yamtich J, Sweasy JB. DNA polymerase family X: function, structure, and cellular roles. Biochim Biophys Acta. 2010;1804:1136-1150.
69. Mao Z, Bozzella M, Seluanov A, et al. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair (Amst). 2008;7:1765-1771.
70. Wilson TE, Grawunder U, Lieber MR. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature. 1997;388:495-498.
71. Alberts B, Johnson A, Lewis J, et al. Molecular Biology of the Cell. 5th ed. Oxford, UK: Garland Science; 2008.
72. Moynahan ME, Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol. 2010;11:196-207.
73. Brenneman MA, Wagener BM, Miller CA, et al. XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol Cell. 2002;10:387-395.
74. Zou Y, Liu Y, Wu X, et al. Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J Cell Physiol. 2006;208:267-273.
75. Maloisel L, Fabre F, Gangloff S. DNA polymerase delta is preferentially recruited during homologous recombination to promote hetero-duplex DNA extension. Mol Cell Biol. 2008;28:1373-1382.
76. Goetz JD, Motycka TA, Han M, et al. Reduced repair of DNA doublestrand breaks by homologous recombination in a DNA ligase I-deficient human cell line. DNA Repair (Amst). 2005;4:649-654.
77. Al-Minawi AZ, Lee YF, Hakansson D, et al. The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross-links. Nucleic Acids Res. 2009;37:6400-6413.
78. McHugh PJ, Spanswick VJ, Hartley JA. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol. 2001;2:483-490.
79. Li L, Wang H, Yang ES, et al. Erlotinib attenuates homologous recombinational repair of chromosomal breaks in human breast cancer cells. Cancer Res. 2008;68:9141-9146.
80. Chinnaiyan P, Huang S, Vallabhaneni G, et al. Mechanisms of enhanced radiation response following epidermal growth factor receptor signaling inhibition by erlotinib (Tarceva). Cancer Res. 2005;65:3328-3335.
81. Jacquemont C, Simon JA, D'Andrea AD, et al. Non-specific chemical inhibition of the Fanconi anemia pathway sensitizes cancer cells to cisplatin. Mol Cancer. 2012;11:26.
82. Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. Bioessays. 2004;26:882-893.
83. Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434:913-917.
84. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434:917-921.
85. Turner NC, Lord CJ, Iorns E, et al. A synthetic lethal siRNA screen identifying genes mediating sensitivity to a PARP inhibitor. EMBO J. 2008;27:1368-1377.
86. Fong PC, Boss DS, Yap TA, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med. 2009;361:123-134.
87. Underhill C, Toulmonde M, Bonnefoi H. A review of PARP inhibitors: from bench to bedside. Ann Oncol. 2011;22:268-279.
88. Johnson N, Li YC, Walton ZE, et al. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat Med. 2010;17:875-882.
89. Marsit CJ, Liu M, Nelson HH, et al. Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene. 2004;23:1000-1004.
90. Rosell R, Skrzypski M, Jassem E, et al. BRCA1: a novel prognostic factor in resected non-small-cell lung cancer. PLoS One. 2007;2:e1129.
91. Engelman JA, Zejnullahu K, Mitsudomi T, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007;316:1039-1043.
92. Plo I, Laulier C, Gauthier L, et al. AKT1 inhibits homologous recombination by inducing cytoplasmic retention of BRCA1 and RAD51. Cancer Res. 2008;68:9404-9412.
93. McEllin B, Camacho CV, Mukherjee B, et al. PTEN loss compromises homologous recombination repair in astrocytes: implications for glioblastoma therapy with temozolomide or poly(ADP-ribose) polymerase inhibitors. Cancer Res. 2010;70:5457-5464.
94. Bindra RS, Schaffer PJ, Meng A, et al. Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol. 2004;24:8504-8518.
95. Chan N, Koritzinsky M, Zhao H, et al. Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res. 2008;68:605-614.
96. Graeser M, McCarthy A, Lord CJ, et al. A marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancer. Clin Cancer Res. 2010;16:6159-6168.
97. Willers H, Taghian AG, Luo C-M, et al. Utility of DNA repair protein foci for the detection of putative BRCA1-pathway defects in breast cancer biopsies. Mol Cancer Res. 2009;7:1304-1309.
98. Das AK, Sato M, Story MD, et al. Non-small-cell lung cancers with kinase domain mutations in the epidermal growth factor receptor are sensitive to ionizing radiation. Cancer Res. 2006;66:9601-9608.
99. Mak RH, Doran E, Muzikansky A, et al. KRAS mutation is associated with decreased overall survival after thoracic radiation therapy in patients with locally advanced non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 2010;78(3 suppl 1):abstract #76.
100. Bernhard EJ, Stanbridge EJ, Gupta S, et al. Direct evidence for the contribution of activated N-ras and K-ras oncogenes to increased intrinsic radiation resistance in human tumor cell lines. Cancer Res. 2000;60:6597-6600.
101. Riballo E, Kuhne M, Rief N, et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell. 2004;16:715-724.