Polygenic inheritance of paclitaxel-induced sensory peripheral neuropathy driven by axon outgrowth gene sets in CALGB 40101 (Alliance)

Pharmacogenomics Journal

Volumn 14, Issue 4, 2014, Pages 336-342

  Chhibber, A ^a,b   Mefford, J ^a,b   Stahl, E A ^c,d,m   Pendergrass, S A ^e   Baldwin, R M ^a,b   Owzar, K ^f   Li, M ^a,b   Winer, E P ^g   Hudis, C A ^h   Zembutsu, H ⁱ   Kubo, M ^j   Nakamura, Y ^i,j,k   McLeod, H L ^l   Ratain, M J ^k   Shulman, L N ^g   Ritchie, M D ^e   Plenge, R M ^c,d   Witte, J S ^a,b   Kroetz, D L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

^h MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

ⁱ UNIVERSITY OF TOKYO   (Japan)

^j RIKEN Center for Integrative Medical Sciences   (Japan)

^k UNIVERSITY OF CHICAGO   (United States)

^l UNIVERSITY OF NORTH CAROLINA   (United States)

^m MOUNT SINAI SCHOOL OF MEDICINE   (United States)

more..

Author keywords

heritability; neuropathy; paclitaxel; pathway; polygenic

Indexed keywords

PACLITAXEL; ANTINEOPLASTIC AGENT;

ARTICLE; BREAST CANCER; CANCER ADJUVANT THERAPY; COHORT ANALYSIS; DISEASE SEVERITY; FEMALE; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC VARIABILITY; GENOTYPE; HUMAN; INHERITANCE; MAJOR CLINICAL STUDY; MULTIPLE CYCLE TREATMENT; NERVE FIBER GROWTH; PATHOGENESIS; PATIENT INFORMATION; PERIPHERAL NEUROPATHY; PHASE 3 CLINICAL TRIAL (TOPIC); PHENOTYPE; PRIORITY JOURNAL; SENSORY NEUROPATHY; SINGLE NUCLEOTIDE POLYMORPHISM; AXON; BREAST NEOPLASMS; CHEMICALLY INDUCED; CLINICAL TRIAL; DRUG EFFECTS; GENETICS; MULTIFACTORIAL INHERITANCE; PHASE 3 CLINICAL TRIAL; PHYSIOLOGY; SENSORY NERVE CELL;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; AXONS; BREAST NEOPLASMS; FEMALE; HUMANS; MULTIFACTORIAL INHERITANCE; PACLITAXEL; PERIPHERAL NERVOUS SYSTEM DISEASES; POLYMORPHISM, SINGLE NUCLEOTIDE; SENSORY RECEPTOR CELLS;

EID: 84904987626     PISSN: 1470269X     EISSN: 14731150     Source Type: Journal    
DOI: 10.1038/tpj.2014.2     Document Type: Article

References (65)

1. Rowinsky EK, Donehower RC. Paclitaxel (taxol). N Engl J Med 1995; 332: 1004-1014.
2. Lee JJ, Swain SM. Peripheral neuropathy induced by microtubule- stabilizing agents. J Clin Oncol 2006; 24: 1633-1642.
3. Donehower RC, Rowinsky EK, Grochow LB, Longnecker SM, Ettinger DS. Phase I trial of taxol in patients with advanced cancer. Cancer Treat Rep 1987; 71: 1171-1177.
4. Postma TJ, Vermorken JB, Liefting AJ, Pinedo HM, Heimans JJ. Paclitaxel-induced neuropathy. Ann Oncol 1995; 6: 489-494.
5. Rowinsky EK, Chaudhry V, Cornblath DR, Donehower RC. Neurotoxicity of taxol. J Natl Cancer Inst Monogr 1993; 15: 107-115.
6. Rowinsky EK, Eisenhauer EA, Chaudhry V, Arbuck SG, Donehower RC. Clinical toxicities encountered with paclitaxel (Taxol). Semin Oncol 1993; 20: 1-15.
7. Lipton RB, Apfel SC, Dutcher JP, Rosenberg R, Kaplan J, Berger A et al. Taxol produces a predominantly sensory neuropathy. Neurology 1989; 39: 368-373.
8. Flatters SJ, Bennett GJ. Studies of peripheral sensory nerves in paclitaxel-induced painful peripheral neuropathy: evidence for mitochondrial dysfunction. Pain 2006; 122: 245-257.
9. Leandro-Garcia LJ, Leskela S, Jara C, Green H, Avall-Lundqvist E, Wheeler HE et al. Regulatory polymorphisms in b-tubulin IIa are associated with paclitaxel-induced peripheral neuropathy. Clin Cancer Res 2012; 18: 4441-4448.
10. Leskela S, Jara C, Leandro-Garcia LJ, Martinez A, Garcia-Donas J, Hernando S et al. Polymorphisms in cytochromes P450 2C8 and 3A5 are associated with paclitaxel neurotoxicity. Pharmacogenomics J 2011; 11: 121-129.
11. Sissung TM, Mross K, Steinberg SM, Behringer D, Figg WD, Sparreboom A et al. Association of ABCB1 genotypes with paclitaxel-mediated peripheral neuropathy and neutropenia. Eur J Cancer 2006; 42: 2893-2896.
12. Bergmann TK, Green H, Brasch-Andersen C, Mirza MR, Herrstedt J, Holund B et al. Retrospective study of the impact of pharmacogenetic variants on paclitaxel toxicity and survival in patients with ovarian cancer. Eur J Clin Pharmacol 2011; 67: 693-700.
13. Ofverholm A, Einbeigi Z, Manouchehrpour S, Albertsson P, Skrtic S, Enerback C. The ABCB1 3435 T allele does not increase the risk of paclitaxel-induced neuro-toxicity. Oncol Lett 2010; 1: 151-154.
14. Baldwin RM, Owzar K, Zembutsu H, Chhibber A, Kubo M, Jiang C et al. A genome-wide association study identifies novel loci for paclitaxel-induced sensory peripheral neuropathy in CALGB 40101. Clin Cancer Res 2012; 18: 5099-5109.
15. Schneider BP, Li L, Miller K, Flockhart DA, Radovich M, Hancock BA et al. Genetic associations with taxane-induced neuropathy by a genome-wide association study in E5103. J Clin Oncol 2011; 29 Suppl: 1000.
16. Bergmann TK, Vach W, Feddersen S, Eckhoff L, Green H, Herrstedt J et al. GWAS-based association between RWDD3 and TECTA variants and paclitaxel induced neuropathy could not be confirmed in Scandinavian ovarian cancer patients. Acta Oncol 2013; 52: 871-874.
17. Motsinger-Reif AA, Jorgenson E, Relling MV, Kroetz DL, Weinshilboum R, Cox NJ et al. Genome-wide association studies in pharmacogenomics: successes and lessons. Pharmacogenet Genomics 2010; 23: 389-394.
18. Koren G, Cairns J, Chitayat D, Gaedigk A, Leeder SJ. Pharmacogenetics of morphine poisoning in a breastfed neonate of a codeine-prescribed mother. Lancet 2006; 368: 704.
19. Lee SH, Wray NR, Goddard ME, Visscher PM. Estimating missing heritability for disease from genome-wide association studies. Am J Hum Genet 2011; 88: 294-305.
20. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR et al. Common SNPs explain a large proportion of the heritability for human height. Nat Genet 2010; 42: 565-569.
21. Li Y, Willer C, Sanna S, Abecasis G. Genotype imputation. Annu Rev Genomics Hum Genet 2009; 10: 387-406.
22. Li Y, Willer CJ, Ding J, Scheet P, Abecasis GR. MaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes. Genet Epidemiol 2010; 34: 816-834.
23. Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, Gibbs RA et al. A map of human genome variation from population-scale sequencing. Nature 2010; 467: 1061-1073.
24. Shulman LN, Cirrincione CT, Berry DA, Becker HP, Perez EA, O'Regan RO et al. Six cycles of doxorubicin and cyclophosphamide or paclitaxel are not superior to 4 cycles as adjuvant chemotherapy for breast cancer in women with 0-3 positive axillary nodes: CALGB 40101. J Clin Oncol 2012; 30: 4071-4076.
25. Muggia FM, Braly PS, Brady MF, Sutton G, Niemann TH, Lentz SL et al. Phase III randomized study of cisplatin versus paclitaxel versus cisplatin and paclitaxel in patients with suboptimal stage III or IV ovarian cancer: a gynecologic oncology group study. J Clin Oncol 2000; 18: 106-115.
26. Perez EA, Vogel CL, Irwin DH, Kirshner JJ, Patel R. Multicenter phase II trial of weekly paclitaxel in women with metastatic breast cancer. J Clin Oncol 2001; 19: 4216-4223.
27. Bouzigon E, Ulgen A, Dizier MH, Siroux V, Lathrop M, Kauffmann F et al. Evidence for a pleiotropic QTL on chromosome 5q13 influencing both time to asthma onset and asthma score in French EGEA families. Hum Genet 2007; 121: 711-719.
28. Dickson MR, Li J, Wiener HW, Perry RT, Blacker D, Bassett SS et al. A genomic scan for age at onset of Alzheimer's disease in 437 families from the NIMH Genetic Initiative. Am J Med Genet B Neuropsychiatr Genet 2008; 147B: 784-792.
29. Hunt KJ, Lehman DM, Arya R, Fowler S, Leach RJ, Goring HH et al. Genome-wide linkage analyses of type 2 diabetes in Mexican Americans: the San Antonio Family Diabetes/Gallbladder Study. Diabetes 2005; 54: 2655-2662.
30. Therneau TM. A package for survival analysis in S. R package version 2.37-7, 2014, http://CRAN.R-project.org/package=survival.
31. Therneau TM, Grambsch PM. Modeling Survival Data: Extending the Cox Model. Springer-Verlag: New York, NY, USA, 2000.
32. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000; 25: 25-29.
33. Timmerman V. Inherited peripheral neuropathies mutation database 2011. http://www.molgen.ua.ac.be/cmtmutations/Home/Default.cfm.
34. Oshiro C, Marsh S, McLeod H, Carrillo M, Klein T, Altman R. Taxane pathway. Pharmacogenet Genomics 2009; 19: 979-983.
35. Smigielski EM, Sirotkin K, Ward M, Sherry ST. dbSNP: a database of single nucleotide polymorphisms. Nucleic Acids Res 2000; 28: 352-355.
36. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81: 559-575.
37. Pruitt KD, Harrow J, Harte RA, Wallin C, Diekhans M, Maglott DR et al. The consensus coding sequence (CCDS) project: identifying a common protein-coding gene set for the human and mouse genomes. Genome Res 2009; 19: 1316-1323.
38. Bush WS, Dudek SM, Ritchie MD. Biofilter: a knowledge-integration system for the multi-locus analysis of genome-wide association studies. Pac Symp Biocomput 2009; 14: 368-379.
39. Yang J, Lee SH, Goddard ME, Visscher PM. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 2011; 88: 76-82.
40. Yang J, Manolio TA, Pasquale LR, Boerwinkle E, Caporaso N, Cunningham JM et al. Genome partitioning of genetic variation for complex traits using common SNPs. Nat Genet 2011; 43: 519-525.
41. Chaudhry V, Rowinsky EK, Sartorius SE, Donehower RC, Cornblath DR. Peripheral neuropathy from taxol and cisplatin combination chemotherapy: clinical and electrophysiological studies. Ann Neurol 1994; 35: 304-311.
42. Letourneau PC, Ressler AH. Inhibition of neurite initiation and growth by taxol. J Cell Biol 1984; 98: 1355-1362.
43. Melli G, Jack C, Lambrinos GL, Ringkamp M, Hoke A. Erythropoietin protects sensory axons against paclitaxel-induced distal degeneration. Neurobiol Dis 2006; 24: 525-530.
44. Sahenk Z, Barohn R, New P, Mendell JR. Taxol neuropathy. Electrodiagnostic and sural nerve biopsy findings. Arch Neurol 1994; 51: 726-729.
45. Roytta M, Raine CS. Taxol-induced neuropathy: chronic effects of local injection. J Neurocytol 1986; 15: 483-496.
46. Allen E, Ding J, Wang W, Pramanik S, Chou J, Yau V et al. Gigaxonin-controlled degradation of MAP1B light chain is critical to neuronal survival. Nature 2005; 438: 224-228.
47. Einarsdottir E, Carlsson A, Minde J, Toolanen G, Svensson O, Solders G et al. A mutation in the nerve growth factor beta gene (NGFB) causes loss of pain perception. Hum Mol Genet 2004; 13: 799-805.
48. Becker E, Richardson DR. Frataxin: its role in iron metabolism and the patho-genesis of Friedreich's ataxia. Int J Biochem Cell Biol 2001; 33: 1-10.
49. Bedlack RS, Edelman D, Gibbs 3rd JW, Kelling D, Strittmatter W, Saunders AM et al. APOE genotype is a risk factor for neuropathy severity in diabetic patients. Neurology 2003; 60: 1022-1024.
50. Corder EH, Robertson K, Lannfelt L, Bogdanovic N, Eggertsen G, Wilkins J et al. HIV-infected subjects with the E4 allele for APOE have excess dementia and peripheral neuropathy. Nat Med 1998; 4: 1182-1184.
51. Pande M, Hur J, Hong Y, Backus C, Hayes JM, Oh SS et al. Transcriptional profiling of diabetic neuropathy in the BKS db/db mouse: a model of type 2 diabetes. Diabetes 2011; 60: 1981-1989.
52. Zurowski D, Nowak L, Machowska A, Wordliczek J, Thor PJ. Exogenous melatonin abolishes mechanical allodynia but not thermal hyperalgesia in neuropathic pain. The role of the opioid system and benzodiazepine-gabaergic mechanism. J Physiol Pharmacol 2012; 63: 641-647.
53. Hori K, Ozaki N, Suzuki S, Sugiura Y. Upregulations of P2X(3) and ASIC3 involve in hyperalgesia induced by cisplatin administration in rats. Pain 2010; 149: 393-405.
54. Padi SS, Shi XQ, Zhao YQ, Ruff MR, Baichoo N, Pert CB et al. Attenuation of rodent neuropathic pain by an orally active peptide, RAP-103, which potently blocks CCR2-and CCR5-mediated monocyte chemotaxis and inflammation. Pain 2012; 153: 95-106.
55. Benamar K, Geller EB, Adler MW. First in vivo evidence for a functional interaction between chemokine and cannabinoid systems in the brain. J Pharmacol Exp Ther 2008; 325: 641-645.
56. Li X, Li YH, Yu S, Liu Y. Upregulation of Ryk expression in rat dorsal root ganglia after peripheral nerve injury. Brain Res Bull 2008; 77: 178-184.
57. Yi XN, Zheng LF, Zhang JW, Zhang LZ, Xu YZ, Luo G et al. Dynamic changes in Robo2 and Slit1 expression in adult rat dorsal root ganglion and sciatic nerve after peripheral and central axonal injury. Neurosci Res 2006; 56: 314-321.
58. Gao WQ, Dybdal N, Shinsky N, Murnane A, Schmelzer C, Siegel M et al. Neuro-trophin-3 reverses experimental cisplatin-induced peripheral sensory neuropathy. Ann Neurol 1995; 38: 30-37.
59. Apfel SC, Lipton RB, Arezzo JC, Kessler JA. Nerve growth factor prevents toxic neuropathy in mice. Ann Neurol 1991; 29: 87-90.
60. Peterson ER, Crain SM. Nerve growth factor attenuates neurotoxic effects of taxol on spinal cord-ganglion explants from fetal mice. Science 1982; 217: 377-379.
61. Wilson BD, Ii M, Park KW, Suli A, Sorensen LK, Larrieu-Lahargue F et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006; 313: 640-644.
62. Toth C, Shim SY, Wang J, Jiang Y, Neumayer G, Belzil C et al. Ndel1 promotes axon regeneration via intermediate filaments. PLoS One 2008; 3: e2014.
63. Hur J, Sullivan KA, Pande M, Hong Y, Sima AA, Jagadish HV et al. The identification of gene expression profiles associated with progression of human diabetic neuropathy. Brain 2011; 134: 3222-3235.
64. Lindquist KJ, Jorgenson E, Hoffmann TJ, Witte JS. The impact of improved microarray coverage and larger sample sizes on future genome-wide association studies. Genet Epidemiol 2013; 37: 383-392.
65. Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R et al. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 2004; 32: D258-D261.