Radiogenomics: The search for genetic predictors of radiotherapy response

Future Oncology

Volumn 10, Issue 15, 2014, Pages 2391-2406

  Kerns, Sarah L ^a,b   West, Catharine M L ^c   Andreassen, C Nicolaj ^d   Barnett, Gillian C ^e,f   Bentzen, Søren M ^g,h   Burnet, Neil G ^f   Dekker, Andre ⁱ   De Ruysscher, Dirk ^j   Dunning, Alison ^e   Parliament, Matthew ^k   Talbot, Chris ^l   Vega, Ana ^m   Rosenstein, Barry S ^a,n  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d AARHUS UNIVERSITY HOSPITAL   (Denmark)

^e CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^h UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

ⁱ MAASTRICHT UNIVERSITY   (Netherlands)

^j UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^k UNIVERSITY OF ALBERTA   (Canada)

^l UNIVERSITY OF LEICESTER   (United Kingdom)

^m UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

ⁿ NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

genome wide association study; normal tissue toxicity; radiogenomics; radiotherapy; single nucleotide polymorphisms

Indexed keywords

CANCER RADIOTHERAPY; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOMICS; HUMAN; PATIENT IDENTIFICATION; PERSONALIZED MEDICINE; PREDICTION; RADIATION INJURY; RADIOGENOMICS; RADIOSENSITIVITY; REVIEW; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT PLANNING; TREATMENT RESPONSE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; NEOPLASMS; RADIATION INJURIES; RISK;

GENOME-WIDE ASSOCIATION STUDY; GENOMICS; HUMANS; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; RADIATION INJURIES; RISK;

EID: 84920023936     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.14.173     Document Type: Review

References (96)

1. Bentzen SM, Constine LS, Deasy JO et al. Quantitative Analyses of Normal Tissue Effects in the Clinic (QUANTEC): an introduction to the scientific issues. Int. J. Radiat. Oncol. Biol. Phys. 76(3 Suppl.), S3-S9 (2010).
2. Siegel R, Desantis C, Virgo K et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J. Clin. 62(4), 220-241 (2012).
3. Vale C, Nightingale A, Spera N, Whelan A, Hanley B, Tierney JF. Late complications from chemoradiotherapy for cervical cancer: reflections from cervical cancer survivors 10 years after the national cancer institute alert. Clin. Oncol. (R. Coll. Radiol.) 22(7), 588-589 (2010).
4. Resnick MJ, Koyama T, Fan KH et al. Long-term functional outcomes after treatment for localized prostate cancer. N. Engl. J. Med. 368(5), 436-445 (2013).
5. Hopwood P, Haviland JS, Sumo G et al. Comparison of patient-reported breast, arm, and shoulder symptoms and body image after radiotherapy for early breast cancer: 5-year follow-up in the randomised Standardisation of Breast Radiotherapy (START) trials. Lancet Oncol. 11(3), 231-240 (2010).
6. Barnett GC, West CM, Dunning AM et al. Normal tissue reactions to radiotherapy: towards tailoring treatment dose by genotype. Nat. Rev. Cancer 9(2), 134-142 (2009).
7. Schoenfeld JD, Margalit DN, Kasperzyk JL et al. A single nucleotide polymorphism in inflammatory gene RNASEL predicts outcome after radiation therapy for localized prostate cancer. Clin. Cancer Res. 19(6), 1612-1619 (2013).
8. Xie X, Jin H, Hu J. et al. Association between single nucleotide polymorphisms in the p53 pathway and response to radiotherapy in patients with nasopharyngeal carcinoma. Oncol. Rep. 31(1), 223-231 (2014).
9. Kim JC, Ha YJ, Roh SA et al. Novel single-nucleotide polymorphism markers predictive of pathologic response to preoperative chemoradiation therapy in rectal cancer patients. Int. J. Radiat. Oncol. Biol. Phys. 86(2), 350-357 (2013).
10. Yin M, Liao Z, Huang YJ. et al. Polymorphisms of homologous recombination genes and clinical outcomes of non-small cell lung cancer patients treated with definitive radiotherapy. PLoS ONE 6(5), e20055 (2011).
11. Terrazzino S, Agostini M, Pucciarelli S et al. A haplotype of the methylenetetrahydrofolate reductase gene predicts poor tumor response in rectal cancer patients receiving preoperative chemoradiation. Pharmacogenet. Genomics 16(11), 817-824 (2006).
12. Meredith WJ, Massey JB. Fundamental Physics of Radiology(3rd Edition). J. Wright, Bristol, UK (1977).
13. Holthusen H. Erfahrungen über die Verträglichkeitsgrenze für Röntgenstrahlen and deren Nutzanwendung zur Verhütung von Schäden. Strahlentherapie 57, 254-269 (1936).
14. Burnet NG, Johansen J, Turesson I, Nyman J, Peacock JH. Describing patients' normal tissue reactions: concerning the possibility of individualising radiotherapy dose prescriptions based on potential predictive assays of normal tissue radiosensitivity. Steering Committee of the BioMed2 European Union Concerted Action Programme on the Development of Predictive Tests of Normal Tissue Response to Radiation Therapy. Int. J. Cancer 79(6), 606-613 (1998).
15. Norman A, Kagan AR, Chan SL. The importance of genetics for the optimization of radiation therapy. A hypothesis. Am. J. Clin. Oncol. 11(1), 84-88 (1988).
16. West CM, Hendry JH. Intrinsic radiosensitivity as a predictor of patient response to radiotherapy. Br. J. Radiol. 24(Suppl.), 146-152 (1992).
17. Burnet NG, Wurm R, Peacock JH. Low dose-rate fibroblast radiosensitivity and the prediction of patient response to radiotherapy. Int. J. Radiat. Biol. 70(3), 289-300 (1996).
18. Tucker SL, Geara FB, Peters LJ, Brock WA. How much could the radiotherapy dose be altered for individual patients based on a predictive assay of normal-tissue radiosensitivity? Radiother. Oncol. 38(2), 103-113 (1996).
19. Bentzen SM. Potential clinical impact of normal-tissue intrinsic radiosensitivity testing. Radiother. Oncol. 43(2), 121-131 (1997).
20. Mackay RI, Niemierko A, Goitein M, Hendry JH. Potential clinical impact of normal-tissue intrinsic radiosensitivity testing. Radiother. Oncol. 46(2), 215-216 (1998).
21. Burnet NG, Nyman J, Turesson I, Wurm R, Yarnold JR, Peacock JH. Prediction of normal-tissue tolerance to radiotherapy from in-vitro cellular radiation sensitivity. Lancet 339(8809), 1570-1571 (1992).
22. Burnet NG, Nyman J, Turesson I, Wurm R, Yarnold JR, Peacock JH. The relationship between cellular radiation sensitivity and tissue response may provide the basis for individualising radiotherapy schedules. Radiother. Oncol. 33(3), 228-238 (1994).
23. Geara FB, Peters LJ, Ang KK, Wike JL, Brock WA. Prospective comparison of in vitro normal cell radiosensitivity and normal tissue reactions in radiotherapy patients. Int. J. Radiat. Oncol. Biol. Phys. 27(5), 1173-1179 (1993).
24. Johansen J, Bentzen SM, Overgaard J, Overgaard M. Evidence for a positive correlation between in vitro radiosensitivity of normal human skin fibroblasts and the occurrence of subcutaneous fibrosis after radiotherapy. Int. J. Radiat. Biol. 66(4), 407-412 (1994).
25. Johansen J, Bentzen SM, Overgaard J, Overgaard M. Relationship between the in vitro radiosensitivity of skin fibroblasts and the expression of subcutaneous fibrosis, telangiectasia, and skin erythema after radiotherapy. Radiother. Oncol. 40(2), 101-109 (1996).
26. Brock WA, Tucker SL, Geara FB et al. Fibroblast radiosensitivity versus acute and late normal skin responses in patients treated for breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 32(5), 1371-1379 (1995).
27. Ramsay J, Birrell G. Normal tissue radiosensitivity in breast cancer patients. Int. J. Radiat. Oncol. Biol. Phys. 31(2), 339-344 (1995).
28. Peacock J, Ashton A, Bliss J et al. Cellular radiosensitivity and complication risk after curative radiotherapy. Radiother. Oncol. 55(2), 173-178 (2000).
29. Safwat A, Bentzen SM, Turesson I, Hendry JH. Deterministic rather than stochastic factors explain most of the variation in the expression of skin telangiectasia after radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 52(1), 198-204 (2002).
30. Curwen GB, Cadwell KK, Winther JF et al. The heritability of G2 chromosomal radiosensitivity and its association with cancer in Danish cancer survivors and their offspring. Int. J. Radiat. Biol. 86(11), 986-995 (2010).
31. Surowy H, Rinckleb A, Luedeke M et al. Heritability of baseline and induced micronucleus frequencies. Mutagenesis 26(1), 111-117 (2011).
32. Finnon P, Robertson N, Dziwura S et al. Evidence for significant heritability of apoptotic and cell cycle responses to ionising radiation. Hum. Genet. 123(5), 485-493 (2008).
33. Schmitz A, Bayer J, Dechamps N, Goldin L, Thomas G. Heritability of susceptibility to ionizing radiation-induced apoptosis of human lymphocyte subpopulations. Int. J. Radiat. Oncol. Biol. Phys. 68(4), 1169-1177 (2007).
34. Wu X, Spitz MR, Amos CI et al. Mutagen sensitivity has high heritability: evidence from a twin study. Cancer Res. 66(12), 5993-5996 (2006).
35. Curwen GB, Winther JF, Tawn EJ et al. G(2) chromosomal radiosensitivity in Danish survivors of childhood and adolescent cancer and their offspring. Br. J. Cancer 93(9), 1038-1045 (2005).
36. Roberts SA, Spreadborough AR, Bulman B, Barber JB, Evans DG, Scott D. Heritability of cellular radiosensitivity: a marker of low-penetrance predisposition genes in breast cancer? Am. J. Hum. Genet. 65(3), 784-794 (1999).
37. West CM, Barnett GC. Genetics and genomics of radiotherapy toxicity: towards prediction. Genome Med. 3(8), 52 (2011).
38. Rosenstein BS. Identification of SNPs associated with susceptibility for development of adverse reactions to radiotherapy. Pharmacogenomics 12(2), 267-275 (2011).
39. Barnett GC, Coles CE, Elliott RM et al. Independent validation of genes and polymorphisms reported to be associated with radiation toxicity: a prospective analysis study. Lancet Oncol. 13(1), 65-77 (2012).
40. Edvardsen H, Landmark-Hoyvik H, Reinertsen KV et al. SNP in TXNRD2 associated with radiation-induced fibrosis: a study of genetic variation in reactive oxygen species metabolism and signaling. Int. J. Radiat. Oncol. Biol. Phys. 86(4), 791-799 (2013).
41. Pang Q, Wei Q, Xu T et al. Functional promoter variant rs2868371 of HSPB1 is associated with risk of radiation pneumonitis after chemoradiation for non-small cell lung cancer. Int. J. Radiat. Oncol. Biol. Phys. 85(5), 1332-1339 (2013).
42. Lopez Guerra JL, Wei Q, Yuan X et al. Functional promoter rs2868371 variant of HSPB1 associates with radiation-induced esophageal toxicity in patients with non-small-cell lung cancer treated with radio(chemo)therapy. Radiother. Oncol. 101(2), 271-277 (2011).
43. Guerra JL, Gomez D, Wei Q et al. Association between single nucleotide polymorphisms of the transforming growth factor beta1 gene and the risk of severe radiation esophagitis in patients with lung cancer. Radiother. Oncol. 105(3), 299-304 (2012).
44. Zhang L, Yang M, Bi N et al. Association of TGF-beta1 and XPD polymorphisms with severe acute radiation-induced esophageal toxicity in locally advanced lung cancer patients treated with radiotherapy. Radiother. Oncol. 97(1), 19-25 (2010).
45. Barnett GC, Elliott RM, Alsner J. et al. Individual patient data meta-analysis shows no association between the SNP rs1800469 in TGFB and late radiotherapy toxicity. Radiother. Oncol. 105(3), 289-295 (2012).
46. Talbot CJ, Tanteles GA, Barnett GC et al. A replicated association between polymorphisms near TNFalpha and risk for adverse reactions to radiotherapy. Br. J. Cancer 107(4), 748-753 (2012).
47. Kerns SL, Stock RG, Stone NN et al. Genome-wide association study identifies a region on chromosome 11q14.3 associated with late rectal bleeding following radiation therapy for prostate cancer. Radiother. Oncol. 107(3), 372-376 (2013).
48. Fachal L, Gómez-Caamaño A, Barnett G.C et al. A three stage genome wide association study reveals susceptibility for late radiotherapy toxicity at the 2q24.1 (TANC1) locus. Nat. Genet. (2014) (In Press).
49. Nardelli B, Zaritskaya L, Semenuk M et al. Regulatory effect of IFN-kappa, a novel type I IFN, on cytokine production by cells of the innate immune system. J. Immunol. 169(9), 4822-4830 (2002).
50. Sachidanandam R, Weissman D, Schmidt SC et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409(6822), 928-933 (2001).
51. Huang Q, Whitington T, Gao P et al. A prostate cancer susceptibility allele at 6q22 increases RFX6 expression by modulating HOXB13 chromatin binding. Nat. Genet. 46(2), 126-135 (2014).
52. Easton DF, Pooley KA, Dunning AM et al. Genome-wide association study identifies novel breast cancer susceptibility loci. Nature 447(7148), 1087-1093 (2007).
53. Long J, Cai Q, Sung H et al. Genome-wide association study in east Asians identifies novel susceptibility loci for breast cancer. PLoS Genet. 8(2), e1002532 (2012).
54. Encode Project Consortium. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306(5696), 636-640 (2004).
55. Encode Project Consortium, Bernstein BE, Birney E et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489(7414), 57-74 (2012).
56. 1000 Genomes Project Consortium, Abecasis GR, Auton A et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491(7422), 56-65 (2012).
57. Andreassen CN, Barnett GC, Langendijk JA et al. Conducting radiogenomic research-do not forget careful consideration of the clinical data. Radiother. Oncol. 105(3), 337-340 (2012).
58. West C, Rosenstein BS. Establishment of a radiogenomics consortium. Radiother. Oncol. 94(1), 117-118 (2010).
59. West C, Rosenstein BS, Alsner J. et al. Establishment of a Radiogenomics Consortium. Int. J. Radiat. Oncol. Biol. Phys. 76(5), 1295-1296 (2010).
60. EGRP-Supported Epidemiology Consortia. http://epi.grants.cancer.gov
61. Kerns SL, Ostrer H, Stock R et al. Genome-wide association study to identify single nucleotide polymorphisms (SNPs) associated with the development of erectile dysfunction in African-American men after radiotherapy for prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 78(5), 1292-1300 (2010).
62. Simoni M, Weinbauer GF, Gromoll J, Nieschlag E. Role of FSH in male gonadal function. Ann. Endocrinol. (Paris) 60(2), 102-106 (1999).
63. Themmen APN, Huhtaniemi IT. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr. Rev. 21(5), 551-583 (2000).
64. Kerns SL, Stone NN, Stock RG, Rath L, Ostrer H, Rosenstein BS. A two-stage genome-wide association study to identify single nucleotide polymorphisms associated with development of urinary symptoms following radiotherapy for prostate cancer. J. Urol. 190(1), 102-108 (2013).
65. Kerns SL, Stock R, Stone N et al. A 2-stage genome-wide association study to identify single nucleotide polymorphisms associated with development of erectile dysfunction following radiation therapy for prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 85(1), e21-e28 (2013).
66. Heublein S, Kazi S, Ogmundsdottir MH et al. Proton-assisted amino-acid transporters are conserved regulators of proliferation and amino-acid-dependent mTORC1 activation. Oncogene 29(28), 4068-4079 (2010).
67. Pillai SM, Meredith D. SLC36A4 (hPAT4) is a high affinity amino acid transporter when expressed in Xenopus laevis oocytes. J. Biol. Chem. 286(4), 2455-2460 (2011).
68. 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. 83(4), e453-e464 (2012).
69. Schiewer MJ, Den R, Hoang DT et al. mTOR is a selective effector of the radiation therapy response in androgen receptor-positive prostate cancer. Endocr. Relat. Cancer 19(1), 1-12 (2012).
70. Barnett GC, Thompson D, Fachal L et al. A genome wide association study (GWAS) providing evidence of an association between common genetic variants and late radiotherapy toxicity. Radiother. Oncol. 111(2), 178-185 (2014).
71. Alsbeih GA, Al-Harbi NM, El-Sebaie MM, Al-Rajhi NM, Al-Hadyan KS, Abu-Amero KK. Involvement of mitochondrial DNA sequence variations and respiratory activity in late complications following radiotherapy. Clin. Cancer Res. 15(23), 7352-7360 (2009).
72. Fachal L, Mosquera-Miguel A, Gomez-Caamano A et al. Evaluating the role of mitochondrial DNA variation to the genetic predisposition to radiation-induced toxicity. Radiother. Oncol. 111(2), 199-205 (2014).
73. Mcclellan J, King MC. Genetic heterogeneity in human disease. Cell 141(2), 210-217 (2010).
74. Hindorff LA, MacArthur J, Morales J. et al. A catalog of published genome-wide association studies. www.genome.gov/gwastudies
75. Eeles RA, Olama AA, Benlloch S et al. Identification of 23 new prostate cancer susceptibility loci using the iCOGS custom genotyping array. Nat. Genet. 45(4), 385-391, e381-e382 (2013).
76. Goh CL, Schumacher FR, Easton D et al. Genetic variants associated with predisposition to prostate cancer and potential clinical implications. J. Intern. Med. 271(4), 353-365 (2012).
77. Akamatsu S, Takata R, Haiman CA et al. Common variants at 11q12, 10q26 and 3p11.2 are associated with prostate cancer susceptibility in Japanese. Nat. Genet. 44(4), 426-429, S421 (2012).
78. Gudmundsson J, Sulem P, Gudbjartsson DF et al. Genome-wide association and replication studies identify four variants associated with prostate cancer susceptibility. Nat. Genet. 41(10), 1122-1126 (2009).
79. Xu J, Mo Z, Ye D et al. Genome-wide association study in Chinese men identifies two new prostate cancer risk loci at 9q31.2 and 19q13.4. Nat. Genet. 44(11), 1231-1235 (2012).
80. Amin Al Olama A, Kote-Jarai Z, Schumacher FR et al. A meta-analysis of genome-wide association studies to identify prostate cancer susceptibility loci associated with aggressive and non-aggressive disease. Hum. Mol. Genet. 22(2), 408-415 (2013).
81. Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB. Rare variants create synthetic genome-wide associations. PLoS Biol. 8(1), e1000294 (2010).
82. Orozco G, Barrett JC, Zeggini E. Synthetic associations in the context of genome-wide association scan signals. Hum. Mol. Genet. 19(R2), R137-R144 (2010).
83. Edwards SL, Beesley J, French JD, Dunning AM. Beyond GWASs: illuminating the dark road from association to function. Am. J. Hum. Genet. 93(5), 779-797 (2013).
84. French JD, Ghoussaini M, Edwards SL et al. Functional variants at the 11q13 risk locus for breast cancer regulate cyclin D1 expression through long-range enhancers. Am. J. Hum. Genet. 92(4), 489-503 (2013).
85. Best T, Li D, Skol AD et al. Variants at 6q21 implicate PRDM1 in the etiology of therapy-induced second malignancies after Hodgkin's lymphoma. Nat. Med. 17(8), 941-943 (2011).
86. Tang H, Jin X, Li Y et al. A large-scale screen for coding variants predisposing to psoriasis. Nat. Genet. 46(1), 45-50 (2014).
87. Garcia-Closas M, Chanock S. Genetic susceptibility loci for breast cancer by estrogen receptor status. Clin. Cancer Res. 14(24), 8000-8009 (2008).
88. Wheeler HE, Maitland ML, Dolan ME, Cox NJ, Ratain MJ. Cancer pharmacogenomics: strategies and challenges. Nat. Rev. Genet. 14(1), 23-34 (2013).
89. Kerns SL, De Ruysscher D, Andreassen CN et al. STROGAR-STrengthening the Reporting Of Genetic Association studies in Radiogenomics. Radiother. Oncol. 110(1), 182-188 (2014).
90. Lambin P, Van Stiphout RG, Starmans MH et al. Predicting outcomes in radiation oncology-multifactorial decision support systems. Nat. Rev. Clin. Oncol. 10(1), 27-40 (2013).
91. Barnett GC, West CM, Coles CE et al. Standardized Total Average Toxicity score: a scale-and grade-independent measure of late radiotherapy toxicity to facilitate pooling of data from different studies. Int. J. Radiat. Oncol. Biol. Phys. 82(3), 1065-1074 (2012).
92. Pollard JM, Gatti RA. Clinical radiation sensitivity with DNA repair disorders: an overview. Int. J. Radiat. Oncol. Biol. Phys. 74(5), 1323-1331 (2009).
93. Bentzen SM, Overgaard M. Relationship between early and late normal-tissue injury after postmastectomy radiotherapy. Radiother. Oncol. 20(3), 159-165 (1991).
94. Bentzen SM, Overgaard M, Overgaard J. Clinical correlations between late normal tissue endpoints after radiotherapy: implications for predictive assays of radiosensitivity. Eur. J. Cancer 29A(10), 1373-1376 (1993).
95. OncoArray Consortium launches genotyping effort. Cancer Discovery. http://cancerdiscovery.aacrjournals.org
96. Zeliadt SB, Ramsey SD, Penson DF et al. Why do men choose one treatment over another?: a review of patient decision making for localized prostate cancer. Cancer 106(9), 1865-1874 (2006).