Use of pharmacogenetics for predicting cancer prognosis and treatment exposure, response and toxicity

Journal of Human Genetics

Volumn 58, Issue 6, 2013, Pages 346-352

  Hertz, Daniel L ^a,b   McLeod, Howard L ^a  

^a UNC Hamner Institute for Drug Safety Sciences   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

cancer; efficacy; personalized medicine; pharmacogenetics; prediction; prognosis; toxicity

Indexed keywords

BETA TUBULIN; DOXIFLURIDINE; EVEROLIMUS; FIRTECAN; FLUOROURACIL; FOLINIC ACID; GLUCURONOSYLTRANSFERASE 1A1; IRINOTECAN; OXALIPLATIN; PACLITAXEL; VEMURAFENIB;

ANOREXIA; ASTHENIA; BLADDER TUMOR; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER HORMONE THERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SURGERY; CANCER THERAPY; CELL DIVISION; COLORECTAL CANCER; CONSTIPATION; DIARRHEA; DNA DAMAGE; DNA REPLICATION; DNA SEQUENCE; DRUG ABSORPTION; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG EXCRETION; DRUG EXPOSURE; DRUG METABOLISM; DRUG TARGETING; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; GENOME; GLUCURONIDATION; HAPLOTYPE; HUMAN; INFECTION; KIDNEY CANCER; LEUKOPENIA; MELANOMA; NAUSEA; NEUTROPENIA; PANCREAS CANCER; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PHARMACOGENETICS; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; STIMULUS RESPONSE; TOXICITY; TREATMENT DURATION; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR VOLUME; VOMITING;

BIOLOGICAL MARKERS; DNA, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VARIATION; GENOME, HUMAN; GENOTYPE; GERM-LINE MUTATION; HUMANS; NEOPLASMS; PHARMACOGENETICS; PROGNOSIS; TREATMENT OUTCOME;

EID: 84880896589     PISSN: 14345161     EISSN: 1435232X     Source Type: Journal    
DOI: 10.1038/jhg.2013.42     Document Type: Review

References (81)

1. McLeod, H. L. Cancer pharmacogenomics: early promise, but concerted effort needed. Science 339, 1563-1566 (2013).
2. Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E. et al. Intratumor Heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892 (2013).
3. Ganem, N. J. & Pellman, D. Linking abnormal mitosis to the acquisition of DNA damage. J. Cell Biol. 199, 871-881 (2012).
4. Greene, F. L. & Sobin, L. H. The staging of cancer: a retrospective and prospective appraisal. CA Cancer J. Clin. 58, 180-190 (2008). (Pubitemid 351830301)
5. Sørlie, T., Perou, C. M., Tibshirani, R., Aas, T., Geisler, S., Johnsen, H. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869-10874 (2001). (Pubitemid 32878711)
6. Nielsen, T. O., Parker, J. S., Leung, S., Voduc, D., Ebbert, M., Vickery, T. et al. A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer. Clin. Cancer Res. 16, 5222-5232 (2010).
7. Goldhirsch, A., Ingle, J. N., Gelber, R. D., Coates, A. S., Thü rlimann, B., Senn, H. et al. Thresholds for therapies: highlights of the St Gallen International Expert Consensus on the primary therapy of early breast cancer 2009. Ann. Oncol. 20, 1319-1329 (2009).
8. Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817-2826 (2004). (Pubitemid 40051905)
9. Albain, K. S., Barlow, W. E., Shak, S., Hortobagyi, G. N., Livingston, R. B., Yeh, I. T. et al. Prognostic and predictive value of the 21-gene recurrence score assay in postmenopausal women with node-positive, oestrogen-receptor- positive breast cancer on chemotherapy: a retrospective analysis of a randomised trial. Lancet Oncol. 11, 55-65 (2010).
10. Sparano, J. A. The TAILORx trial: individualized options for treatment. Comm. Oncol. 83, 494-496 (2006). (Pubitemid 44476516)
11. van't Veer, L. J., Dai, H., van de Vijver, M. J., He, Y. D., Hart, A. A., Mao, M. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536 (2002). (Pubitemid 34130608)
12. van de Vijver, M. J., He, Y. D., van't Veer, L. J., Dai, H., Hart, A. A., Voskuil, D. W. et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (2002). (Pubitemid 35461656)
13. Wittner, B. S., Sgroi, D. C., Ryan, P. D., Bruinsma, T. J., Glas, A. M., Male, A. et al. Analysis of the MammaPrint breast cancer assay in a predominantly postmenopausal cohort. Clin. Cancer Res. 14, 2988-2993 (2008).
14. Rutgers, E., Piccart-Gebhart, M. J., Bogaerts, J., Delaloge, S., Veer, L. V., Rubio, I. T. et al. The EORTC 10041/BIG 03-04 MINDACT trial is feasible: results of the pilot phase. Eur. J. Cancer 47, 2742-2749 (2011).
15. Fan, C., Oh, D. S., Wessels, L., Weigelt, B., Nuyten, D. S., Nobel, A. B. et al. Concordance among gene-expression-based predictors for breast cancer. N. Engl. J. Med. 355, 560-569 (2006). (Pubitemid 44200649)
16. Tsimberidou, A. M., Iskander, N. G., Hong, D. S., Wheler, J. J., Falchook, G. S., Fu, S. et al. Personalized medicine in a phase I clinical trials program: the MD Anderson Cancer Center initiative. Clin. Cancer Res. 18, 6373-6383 (2012).
17. Roychowdhury, S., Iyer, M. K., Robinson, D. R., Lonigro, R. J., Wu, Y. M., Cao, X. et al. Personalized oncology through integrative high-throughput sequencing: a pilot study. Sci. Transl. Med. 3, 111ra121 (2011).
18. Mandrekar, S. J. & Sargent, D. J. Clinical trial designs for predictive biomarker validation: theoretical considerations and practical challenges. J. Clin. Oncol. 27, 4027-4034 (2009).
19. Inoki, K., Corradetti, M. N. & Guan, K. L. Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 37, 19-24 (2005). (Pubitemid 40070934)
20. Meikle, L., Pollizzi, K., Egnor, A., Kramvis, I., Lane, H., Sahin, M. et al. Response of a neuronal model of tuberous sclerosis to mammalian target of rapamycin (mTOR) inhibitors: effects on mTORC1 and Akt signaling lead to improved survival and function. J. Neurosci. 28, 5422-5432 (2008).
21. Franz, D. N. Everolimus: an mTOR inhibitor for the treatment of tuberous sclerosis. Expert Rev. Anticancer Ther. 11, 1181-1192 (2011).
22. Iyer, G., Hanrahan, A. J., Milowsky, M. I., Al-Ahmadie, H., Scott, S. N., Janakiraman, M. et al. Genome sequencing identifies a basis for everolimus sensitivity. Science 338, 221 (2012).
23. Davies, H., Bignell, G. R., Cox, C., Stephens, P., Edkins, S., Clegg, S. et al. Mutations of the BRAF gene in human cancer. Nature 417, 949-954 (2002). (Pubitemid 34716871)
24. Tsai, J., Lee, J. T., Wang, W., Zhang, J., Cho, H., Mamo, S. et al. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc. Natl Acad. Sci. USA 105, 3041-3046 (2008). (Pubitemid 351723664)
25. Flaherty, K. T., Puzanov, I., Kim, K. B., Ribas, A., McArthur, G. A., Sosman, J. A. et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med. 363, 809-819 (2010).
26. Chapman, P. B., Hauschild, A., Robert, C., Haanen, J. B., Ascierto, P., Larkin, J. et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 364, 2507-2516 (2011).
27. Halait, H., Demartin, K., Shah, S., Soviero, S., Langland, R., Cheng, S. et al. Analytical performance of a real-time PCR-based assay for V600 mutations in the BRAF gene, used as the companion diagnostic test for the novel BRAF inhibitor vemurafenib in metastatic melanoma. Diagn Mol. Pathol. 21, 1-8 (2012).
28. Li, F. P. Translational research on hereditary colon, breast, and ovarian cancers. J. Natl Cancer Inst. Monogr. 17, 1-4 (1995).
29. McLeod, H. L. & Evans, W. E. Pharmacogenomics: unlocking the human genome for better drug therapy. Annu. Rev. Pharmacol. Toxicol. 41, 101-121 (2001). (Pubitemid 32385884)
30. Theodoratou, E., Montazeri, Z., Hawken, S., Allum, G. C., Gong, J., Tait, V. et al. Systematic meta-analyses and field synopsis of genetic association studies in colorectal cancer. J. Natl Cancer Inst. 104, 1433-1457 (2012).
31. Siddiq, A., Couch, F. J., Chen, G. K., Lindstrom, S., Eccles, D., Millikan, R. C. et al. A meta-analysis of genome-wide association studies of breast cancer identifies two novel susceptibility loci at 6q14 and 20q11. Hum. Mol. Genet. 21, 5373-5384 (2012).
32. Collins, F. S. & Barker, A. D. Mapping the cancer genome. Pinpointing the genes involved in cancer will help chart a new course across the complex landscape of human malignancies. Sci. Am. 296, 50-57 (2007).
33. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
34. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615 (2011).
35. Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 489, 519-525 (2012).
36. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70 (2012).
37. Yang, D., Khan, S., Sun, Y., Hess, K., Shmulevich, I., Sood, A. K. et al. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. JAMA 306, 1557-1565 (2011).
38. Bolton, K. L., Chenevix-Trench, G., Goh, C., Sadetzki, S., Ramus, S. J., Karlan, B. Y. et al. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA 307, 382-390 (2012).
39. Park, Y. G., Zhao, X., Lesueur, F., Lowy, D. R., Lancaster, M., Pharoah, P. et al. Sipa1 is a candidate for underlying the metastasis efficiency modifier locus Mtes1. Nat. Genet. 37, 1055-1062 (2005). (Pubitemid 41486657)
40. Crawford, N. P., Ziogas, A., Peel, D. J., Hess, J., Anton-Culver, H. & Hunter, K. W. Germline polymorphisms in SIPA1 are associated with metastasis and other indicators of poor prognosis in breast cancer. Breast Cancer Res. 8, R16 (2006).
41. Pei, R., Xu, Y., Wei, Y., Ouyang, T., Li, J., Wang, T. et al. Association of SIPA1 545 C4T polymorphism with survival in Chinese women with metastatic breast cancer. Front Med. 7, 138-142 (2013).
42. Crawford, N. P., Alsarraj, J., Lukes, L., Walker, R. C., Officewala, J. S., Yang, H. H. et al. Bromodomain 4 activation predicts breast cancer survival. Proc. Natl Acad. Sci. USA 105, 6380-6385 (2008). (Pubitemid 351758354)
43. Crawford, N. P., Qian, X., Ziogas, A., Papageorge, A. G., Boersma, B. J., Walker, R. C. et al. Rrp1b, a new candidate susceptibility gene for breast cancer progression and metastasis. PLoS Genet. 3, e214 (2007).
44. Hsieh, S. M., Look, M. P., Sieuwerts, A. M., Foekens, J. A. & Hunter, K. W. Distinct inherited metastasis susceptibility exists for different breast cancer subtypes: a prognosis study. Breast Cancer Res. 11, R75 (2009).
45. Shimizu, Y., Hamazaki, Y., Hattori, M., Doi, K., Terada, N., Kobayashi, T. et al. SPA-1 controls the invasion and metastasis of human prostate cancer. Cancer Sci. 102, 828-836 (2011).
46. Lin, J. H. Pharmacokinetic and pharmacodynamic variability: a daunting challenge in drug therapy. Curr. Drug Metab. 8, 109-136 (2007). (Pubitemid 46218679)
47. Felici, A., Verweij, J. & Sparreboom, A. Dosing strategies for anticancer drugs: the good, the bad and body-surface area. Eur. J. Cancer 38, 1677-1684 (2002).
48. McLeay, S. C., Morrish, G. A., Kirkpatrick, C. M. & Green, B. The relationship between drug clearance and body size: systematic review and meta-analysis of the literature published from 2000 to 2007. Clin. Pharmacokinet. 51, 319-330 (2012).
49. Krens, S. D., McLeod, H. L. & Hertz, D. L. Pharmacogenetics, enzyme probes and therapeutic drug monitoring as potential tools for individualizing taxane therapy. Pharmacogenomics 14, 555-574 (2013).
50. Begg, E. J., Helsby, N. A. & Jensen, B. P. Pharmacogenetics of drug-metabolizing enzymes: the prodrug hypothesis. Pharmacogenomics 13, 83-89 (2012).
51. Iyer, L., Hall, D., Das, S., Mortell, M. A., Ramirez, J., Kim, S. et al. Phenotype-genotype correlation of in vitro SN-38 (active metabolite of irinotecan) and bilirubin glucuronidation in human liver tissue with UGT1A1 promoter polymorphism. Clin. Pharmacol. Ther. 65, 576-582 (1999). (Pubitemid 29237332)
52. Ando, Y., Saka, H., Asai, G., Sugiura, S., Shimokata, K. & Kamataki, T. UGT1A1 genotypes and glucuronidation of SN-38, the active metabolite of irinotecan. Ann. Oncol. 9, 845-847 (1998). (Pubitemid 28440442)
53. Paoluzzi, L., Singh, A. S., Price, D. K., Danesi, R., Mathijssen, R. H., Verweij, J. et al. Influence of genetic variants in UGT1A1 and UGT1A9 on the in vivo glucuronidation of SN-38. J. Clin. Pharmacol. 44, 854-860 (2004). (Pubitemid 38971566)
54. Stewart, C. F., Panetta, J. C., O'Shaughnessy, M. A., Throm, S. L., Fraga, C. H., Owens, T. et al. UGT1A1 promoter genotype correlates with SN-38 pharmacokinetics, but not severe toxicity in patients receiving low-dose irinotecan. J. Clin. Oncol. 25, 2594-2600 (2007). (Pubitemid 47041233)
55. Toffoli, G., Cecchin, E., Corona, G., Russo, A., Buonadonna, A., D'Andrea, M. et al. The role of UGT1A128 polymorphism in the pharmacodynamics and pharmacokinetics of irinotecan in patients with metastatic colorectal cancer. J. Clin. Oncol. 24, 3061-3068 (2006). (Pubitemid 46638941)
56. Saito, Y., Sai, K., Maekawa, K., Kaniwa, N., Shirao, K., Hamaguchi, T. et al. Close association of UGT1A9 IVS1\+399C4T with UGT1A128, 6, or60 haplotype and its apparent influence on 7-ethyl-10-hydroxycamptothecin (SN-38) glucuronidation in Japanese. Drug Metab. Dispos. 37, 272-276 (2009).
57. Minami, H., Sai, K., Saeki, M., Saito, Y., Ozawa, S., Suzuki, K. et al. Irinotecan pharmacokinetics/pharmacodynamics and UGT1A genetic polymorphisms in Japanese: roles of UGT1A16 and28. Pharmacogenet. Genomics 17, 497-504 (2007). (Pubitemid 46905216)
58. Yamamoto, N., Takahashi, T., Kunikane, H., Masuda, N., Eguchi, K., Shibuya, M. et al. Phase I/II pharmacokinetic and pharmacogenomic study of UGT1A1 polymorphism in elderly patients with advanced non-small cell lung cancer treated with irinotecan. Clin. Pharmacol. Ther. 85, 149-154 (2009).
59. Sai, K., Saeki, M., Saito, Y., Ozawa, S., Katori, N., Jinno, H. et al. UGT1A1 haplotypes associated with reduced glucuronidation and increased serum bilirubin in irinotecanadministered Japanese patients with cancer. Clin. Pharmacol. Ther. 75, 501-515 (2004). (Pubitemid 38746601)
60. Ramchandani, R. P., Wang, Y., Booth, B. P., Ibrahim, A., Johnson, J. R., Rahman, A. et al. The role of SN-38 exposure, UGT1A128 polymorphism, and baseline bilirubin level in predicting severe irinotecan toxicity. J. Clin. Pharmacol. 47, 78-86 (2007). (Pubitemid 44974001)
61. Evaluation of Genomic Applications in Practice and Prevention (EGAPP) Working Group. Recommendations from the EGAPP Working Group: can UGT1A1 genotyping reduce morbidity and mortality in patients with metastatic colorectal cancer treated with irinotecan? Genet. Med. 11, 15-20 (2009).
62. Di Paolo, A., Bocci, G., Polillo, M., Del Re, M., Di Desidero, T., Lastella, M. et al. Pharmacokinetic and pharmacogenetic predictive markers of irinotecan activity and toxicity. Curr. Drug Metab. 12, 932-943 (2011).
63. Hazama, S., Nagashima, A., Kondo, H., Yoshida, S., Shimizu, R., Araki, A. et al. Phase I study of irinotecan and doxifluridine for metastatic colorectal cancer focusing on the UGT1A128 polymorphism. Cancer Sci. 101, 722-727 (2010).
64. Satoh, T., Ura, T., Yamada, Y., Yamazaki, K., Tsujinaka, T., Munakata, M. et al. Genotype-directed, dose-finding study of irinotecan in cancer patients with UGT1A128 and/or UGT1A16 polymorphisms. Cancer Sci. 102, 1868-1873 (2011).
65. Sunakawa, Y., Fujita, K., Ichikawa, W., Ishida, H., Yamashita, K., Araki, K. et al. A phase I study of infusional 5-fluorouracil, leucovorin, oxaliplatin and irinotecan in Japanese patients with advanced colorectal cancer who harbor UGT1A11/1, 1/6 or1/28. Oncology 82, 242-248 (2012).
66. Okuyama, Y., Hazama, S., Nozawa, H., Kobayashi, M., Takahashi, K., Fujikawa, K. et al. Prospective phase II study of FOLFIRI for mCRC in Japan, including the analysis of UGT1A1 28/6 polymorphisms. Jpn. J. Clin. Oncol. 41, 477-482 (2011).
67. Marcuello, E., Paez, D., Pare, L., Salazar, J., Sebio, A., del Rio, E. et al. A genotypedirected phase I-IV dose-finding study of irinotecan in combination with fluorouracil/leucovorin as first-line treatment in advanced colorectal cancer. Br. J. Cancer 105, 53-57 (2011).
68. Toffoli, G., Cecchin, E., Gasparini, G., D'Andrea, M., Azzarello, G., Basso, U. et al. Genotype-driven phase I study of irinotecan administered in combination with fluorouracil/leucovorin in patients with metastatic colorectal cancer. J. Clin. Oncol. 28, 866-871 (2010).
69. Freyer, G., Duret, A., Milano, G., Chatelut, E., Rebischung, C., Delord, J. P. et al. Pharmacogenetic tailoring of irinotecan-based first-line chemotherapy in metastatic colorectal cancer: results of a pilot study. Anticancer Res. 31, 359-366 (2011).
70. de Jong, F. A., Mathijssen, R. H., Xie, R., Verweij, J. & Sparreboom, A. Flat-fixed dosing of irinotecan: influence on pharmacokinetic and pharmacodynamic variability. Clin. Cancer Res. 10 (Part 1), 4068-4071 (2004). (Pubitemid 38812483)
71. Mathijssen, R. H., Marsh, S., Karlsson, M. O., Xie, R., Baker, S. D., Verweij, J. et al. Irinotecan pathway genotype analysis to predict pharmacokinetics. Clin. Cancer Res. 9, 3246-3253 (2003). (Pubitemid 37086673)
72. Innocenti, F., Kroetz, D. L., Schuetz, E., Dolan, M. E., Ramirez, J., Relling, M. et al. Comprehensive pharmacogenetic analysis of irinotecan neutropenia and pharmacokinetics. J. Clin. Oncol. 27, 2604-2614 (2009).
73. Sai, K., Saito, Y., Tatewaki, N., Hosokawa, M., Kaniwa, N., Nishimaki-Mogami, T. et al. Association of carboxylesterase 1 A genotypes with irinotecan pharmacokinetics in Japanese cancer patients. Br. J. Clin. Pharmacol. 70, 222-233 (2010).
74. Sai, K., Saito, Y., Fukushima-Uesaka, H., Kurose, K., Kaniwa, N., Kamatani, N. et al. Impact of CYP3A4 haplotypes on irinotecan pharmacokinetics in Japanese cancer patients. Cancer Chemother. Pharmacol. 62, 529-537 (2008).
75. Lee, J. J. & Swain, S. M. Peripheral neuropathy Induced by microtubule-stabilizing agents. J. Clin. Oncol. 24, 1633-1642 (2006). (Pubitemid 46638788)
76. Wilson, L. & Jordan, M. A. Microtubule dynamics: taking aim at a moving target. Chem. Biol. 2, 569-573 (1995).
77. Bamburg, J. R., Bray, D. & Chapman, K. Assembly of microtubules at the tip of growing axons. Nature 321, 788-790 (1986). (Pubitemid 16077908)
78. Berrieman, H. K., Lind, M. J. & Cawkwell, L. Do b-tubulin mutations have a role in resistance to chemotherapy? Lancet Oncol. 5, 158-164 (2004). (Pubitemid 38262847)
79. Leandro-Garcia, L. J., Leskela, S., Jara Sanchez, C., Green, H., Avall Lundqvist, E., Wheeler, H. E. et al. Regulatory polymorphisms in beta-tubulin IIa are associated with paclitaxel-induced peripheral neuropathy. Clin. Cancer Res. 18, 4441-4448 (2012).
80. Sucheston, L., Zhao, H., Yao, S., Zirpoli, G., Liu, S., Barlow, W. et al. Genetic predictors of taxane-induced neurotoxicity in a SWOG phase III intergroup adjuvant breast cancer treatment trial (S0221). Breast Cancer Res. Treat. 130, 993-1002 (2011).
81. Delague, V., Jacquier, A., Hamadouche, T., Poitelon, Y., Baudot, C., Boccaccio, I. et al. Mutations in FGD4 encoding the Rho GDP/GTP exchange factor FRABIN cause autosomal recessive Charcot-Marie-Tooth type 4H. Am. J. Hum. Genet. 81, 1-16 (2007). (Pubitemid 47001152)