Genome-wide Association Study Identifies Shared Risk Loci Common to Two Malignancies in Golden Retrievers

PLoS Genetics

Volumn 11, Issue 2, 2015, Pages 1-24

  Tonomura, Noriko ^a,b   Elvers, Ingegerd ^a,c   Thomas, Rachael ^d   Megquier, Kate ^a,c   Turner Maier, Jason ^a   Howald, Cedric ^a   Sarver, Aaron L ^e   Swofford, Ross ^a   Frantz, Aric M ^e,f   Ito, Daisuke ^e,f   Mauceli, Evan ^a,g   Arendt, Maja ^c   Noh, Hyun Ji ^a   Koltookian, Michele ^a   Biagi, Tara ^a   Fryc, Sarah ^a   Williams, Christina ^d   Avery, Anne C ^h   Kim, Jong Hyuk ^e,f   Barber, Lisa ^b   Burgess, Kristine ^b   Lander, Eric S ^a   Karlsson, Elinor K ^a,i   Azuma, Chieko ^b   Modiano, Jaime F ^e,f   Breen, Matthew ^d   Lindblad Toh, Kerstin ^a,c   more..

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

^b TUFTS UNIVERSITY   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

^g BOSTON CHILDREN S HOSPITAL   (United States)

^h Department of Environmental and Radiological Health Sciences   (United States)

ⁱ HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL 6;

ANGIOSARCOMA; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B CELL LYMPHOMA; CANCER RISK; CARCINOGENESIS; CELL ACTIVATION; CHILD; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC RISK; GENOTYPE; GERMLINE MUTATION; GOLDEN RETRIEVER; HAPLOTYPE; HUMAN; IMMUNOCOMPETENT CELL; NONHUMAN; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL SIGNIFICANCE; STX8 GENE; TRPC6 GENE; ANIMAL; B LYMPHOCYTE; BREEDING; DOG; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; PATHOLOGY; RISK FACTOR; VETERINARY;

CANIS FAMILIARIS;

ANIMALS; B-LYMPHOCYTES; BREEDING; CARCINOGENESIS; DOGS; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; GERM-LINE MUTATION; HAPLOTYPES; HEMANGIOSARCOMA; HUMANS; LYMPHOMA, B-CELL; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK FACTORS;

EID: 84924422639     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004922     Document Type: Article

References (72)

1. Siegel R, Ma J, Zou Z, Jemal A, (2014) Cancer statistics, 2014. CA Cancer J Clin 64: 9–29. doi: 10.3322/caac.21208 24399786
2. Anderson JR, Armitage JO, Weisenburger DD, (1998) Epidemiology of the non-Hodgkin’s lymphomas: distributions of the major subtypes differ by geographic locations. Non-Hodgkin’s Lymphoma Classification Project. Ann Oncol 9: 717–720. doi: 10.1023/A:1008265532487 9739436
3. Penel N, Marreaud S, Robin YM, Hohenberger P, (2011) Angiosarcoma: state of the art and perspectives. Crit Rev Oncol Hematol 80: 257–263. doi: 10.1016/j.critrevonc.2010.10.007 21055965
4. Enzinger FMaW S.W., Soft Tissue Tumors, p 648–77, 3rd Edition.: Mosby, St. Louis, MO, 1995.
5. Glickman LG, N.; Thorpe, R. (2000) The Golden Retriever Club of America National Health Survey 1998–1999. (available at http://wwwgrcaorg/pdf/health/healthsurveypdf).
6. Valli VE, San Myint M, Barthel A, Bienzle D, Caswell J, et al. (2011) Classification of canine malignant lymphomas according to the World Health Organization criteria. Vet Pathol 48: 198–211. doi: 10.1177/0300985810379428 20861499
7. Modiano JF, Breen M, Burnett RC, Parker HG, Inusah S, et al. (2005) Distinct B-cell and T-cell lymphoproliferative disease prevalence among dog breeds indicates heritable risk. Cancer Res 65: 5654–5661. doi: 10.1158/0008-5472.CAN-04-4613 15994938
8. Vail DM, MacEwen EG, (2000) Spontaneously occurring tumors of companion animals as models for human cancer. Cancer Invest 18: 781–792. doi: 10.3109/07357900009012210 11107448
9. Ito D, Frantz AM, Modiano JF, (2014) Canine lymphoma as a comparative model for human non-Hodgkin lymphoma: recent progress and applications. Vet Immunol Immunopathol 159: 192–201. doi: 10.1016/j.vetimm.2014.02.016 24642290
10. Priester WA, (1976) Hepatic angiosarcomas in dogs: an excessive frequency as compared with man. J Natl Cancer Inst 57: 451–454. 1034019
11. Fosmire SP, Dickerson EB, Scott AM, Bianco SR, Pettengill MJ, et al. (2004) Canine malignant hemangiosarcoma as a model of primitive angiogenic endothelium. Lab Invest 84: 562–572. doi: 10.1038/labinvest.3700080 15064773
12. Tan DE, Foo JN, Bei JX, Chang J, Peng R, et al. (2013) Genome-wide association study of B cell non-Hodgkin lymphoma identifies 3q27 as a susceptibility locus in the Chinese population. Nat Genet 45: 804–807. doi: 10.1038/ng.2666 23749188
13. Goldin LR, Bjorkholm M, Kristinsson SY, Turesson I, Landgren O, (2009) Highly increased familial risks for specific lymphoma subtypes. Br J Haematol 146: 91–94. doi: 10.1111/j.1365-2141.2009.07721.x 19438470
14. Smedby KE, Foo JN, Skibola CF, Darabi H, Conde L, et al. (2011) GWAS of follicular lymphoma reveals allelic heterogeneity at 6p21.32 and suggests shared genetic susceptibility with diffuse large B-cell lymphoma. PLoS Genet 7: e1001378. doi: 10.1371/journal.pgen.1001378 21533074
15. Cerhan JR, Berndt SI, Vijai J, Ghesquieres H, McKay J, et al. (2014) Genome-wide association study identifies multiple susceptibility loci for diffuse large B cell lymphoma. Nat Genet. doi: 10.1038/ng.3105 25261932
16. Wilbe M, Jokinen P, Truve K, Seppala EH, Karlsson EK, et al. (2010) Genome-wide association mapping identifies multiple loci for a canine SLE-related disease complex. Nat Genet 42: 250–254. doi: 10.1038/ng.525 20101241
17. Dodman NH, Karlsson EK, Moon-Fanelli A, Galdzicka M, Perloski M, et al. (2010) A canine chromosome 7 locus confers compulsive disorder susceptibility. Mol Psychiatry 15: 8–10. doi: 10.1038/mp.2009.111 20029408
18. Karlsson EK, Sigurdsson S, Ivansson E, Thomas R, Elvers I, et al. (2013) Genome-wide analyses implicate 33 loci in heritable dog osteosarcoma, including regulatory variants near CDKN2A/B. Genome Biol 14: R132. doi: 10.1186/gb-2013-14-12-r132 24330828
19. Tang R, Noh H, Wang D, Sigurdsson S, Swofford R, et al. (2014) Candidate genes and functional noncoding variants identified in a canine model of obsessive-compulsive disorder. Genome Biol 15: R25. doi: 10.1186/gb-2014-15-3-r25 24995881
20. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803–819. doi: 10.1038/nature04338 16341006
21. Sutter NB, Ostrander EA, (2004) Dog star rising: the canine genetic system. Nat Rev Genet 5: 900–910. doi: 10.1038/nrg1492 15573122
22. Paoloni M, Khanna C, (2008) Translation of new cancer treatments from pet dogs to humans. Nat Rev Cancer 8: 147–156. doi: 10.1038/nrc2273 18202698
23. Vaysse A, Ratnakumar A, Derrien T, Axelsson E, Rosengren Pielberg G, et al. (2011) Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping. PLoS Genet 7: e1002316. doi: 10.1371/journal.pgen.1002316 22022279
24. Price AL, Zaitlen NA, Reich D, Patterson N, (2010) New approaches to population stratification in genome-wide association studies. Nat Rev Genet 11: 459–463. doi: 10.1038/nrg2813 20548291
25. Yang J, Lee SH, Goddard ME, Visscher PM, (2011) GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88: 76–82. doi: 10.1016/j.ajhg.2010.11.011 21167468
26. Purcell S PLINK: http://pngu.mgh.harvard.edu/purcell/plink/.
27. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559–575. doi: 10.1086/519795 17701901
28. Barrett JC, Fry B, Maller J, Daly MJ, (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263–265. doi: 10.1093/bioinformatics/bth457 15297300
29. Abramowitz J, Birnbaumer L, (2009) Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 23: 297–328. doi: 10.1096/fj.08-119495 18940894
30. Carrillo C, Hichami A, Andreoletti P, Cherkaoui-Malki M, del Mar Cavia M, et al. (2012) Diacylglycerol-containing oleic acid induces increases in [Ca(2+)](i) via TRPC3/6 channels in human T-cells. Biochim Biophys Acta 1821: 618–626. doi: 10.1016/j.bbalip.2012.01.008 22306362
31. Tseng PH, Lin HP, Hu H, Wang C, Zhu MX, et al. (2004) The canonical transient receptor potential 6 channel as a putative phosphatidylinositol 3,4,5-trisphosphate-sensitive calcium entry system. Biochemistry 43: 11701–11708. doi: 10.1021/bi049349f 15362854
32. Ingenuity®Systems http://www.ingenuity.com.
33. Croce M, Orengo AM, Azzarone B, Ferrini S, (2012) Immunotherapeutic applications of IL-15. Immunotherapy 4: 957–969. doi: 10.2217/imt.12.92 23046239
34. Kappes DJ, (2010) Expanding roles for ThPOK in thymic development. Immunol Rev 238: 182–194. doi: 10.1111/j.1600-065X.2010.00958.x 20969593
35. Liao W, Lin JX, Leonard WJ, (2013) Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 38: 13–25. doi: 10.1016/j.immuni.2013.01.004 23352221
36. Bautch VL, (2011) Stem cells and the vasculature. Nat Med 17: 1437–1443. doi: 10.1038/nm.2539 22064433
37. Lamerato-Kozicki AR, Helm KM, Jubala CM, Cutter GC, Modiano JF, (2006) Canine hemangiosarcoma originates from hematopoietic precursors with potential for endothelial differentiation. Exp Hematol 34: 870–878. doi: 10.1016/j.exphem.2006.04.013 16797414
38. Pickrell JK, (2014) Joint analysis of functional genomic data and genome-wide association studies of 18 human traits. Am J Hum Genet 94: 559–573. doi: 10.1016/j.ajhg.2014.03.004 24702953
39. Smolewski P, Robak T, (2011) Inhibitors of apoptosis proteins (IAPs) as potential molecular targets for therapy of hematological malignancies. Curr Mol Med 11: 633–649. doi: 10.2174/156652411797536723 21902653
40. Zeng L, Dai J, Ying K, Zhao E, Jin W, et al. (2003) Identification of a novel human angiopoietin-like gene expressed mainly in heart. J Hum Genet 48: 159–162. doi: 10.1007/s10038-003-0033-3 12624729
41. Chen TC, Lee SA, Hong TM, Shih JY, Lai JM, et al. (2009) From midbody protein-protein interaction network construction to novel regulators in cytokinesis. J Proteome Res 8: 4943–4953. doi: 10.1021/pr900325f 19799413
42. Roedding AS, Li PP, Warsh JJ, (2006) Characterization of the transient receptor potential channels mediating lysophosphatidic acid-stimulated calcium mobilization in B lymphoblasts. Life Sci 80: 89–97. doi: 10.1016/j.lfs.2006.08.021 16979191
43. Damann N, Owsianik G, Li S, Poll C, Nilius B, (2009) The calcium-conducting ion channel transient receptor potential canonical 6 is involved in macrophage inflammatory protein-2-induced migration of mouse neutrophils. Acta Physiol (Oxf) 195: 3–11. doi: 10.1111/j.1748-1716.2008.01918.x
44. http://www.bu.edu/nf-kb/gene-resources/target-genes/ (accessed Oct 22, 2014).
45. Schall TJ, Bacon K, Toy KJ, Goeddel DV, (1990) Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347: 669–671. doi: 10.1038/347669a0 1699135
46. Sanchez-Sanchez N, Riol-Blanco L, Rodriguez-Fernandez JL, (2006) The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J Immunol 176: 5153–5159. doi: 10.4049/jimmunol.176.9.5153 16621978
47. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, et al. (2008) CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 181: 8391–8401. doi: 10.4049/jimmunol.181.12.8391 19050256
48. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, et al. (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403: 503–511. doi: 10.1038/35000501 10676951
49. Frantz AM, Sarver AL, Ito D, Phang TL, Karimpour-Fard A, et al. (2013) Molecular Profiling Reveals Prognostically Significant Subtypes of Canine Lymphoma. Vet Pathol. doi: 10.1177/0300985812465325 23125145
50. Chang KC, Huang GC, Jones D, Lin YH, (2007) Distribution patterns of dendritic cells and T cells in diffuse large B-cell lymphomas correlate with prognoses. Clin Cancer Res 13: 6666–6672. doi: 10.1158/1078-0432.CCR-07-0504 18006767
51. Hasselblom S, Sigurdadottir M, Hansson U, Nilsson-Ehle H, Ridell B, et al. (2007) The number of tumour-infiltrating TIA-1+ cytotoxic T cells but not FOXP3+ regulatory T cells predicts outcome in diffuse large B-cell lymphoma. Br J Haematol 137: 364–373. doi: 10.1111/j.1365-2141.2007.06593.x 17456059
52. Muris JJ, Meijer CJ, Cillessen SA, Vos W, Kummer JA, et al. (2004) Prognostic significance of activated cytotoxic T-lymphocytes in primary nodal diffuse large B-cell lymphomas. Leukemia 18: 589–596. doi: 10.1038/sj.leu.2403240 14712286
53. Riemersma SA, Oudejans JJ, Vonk MJ, Dreef EJ, Prins FA, et al. (2005) High numbers of tumour-infiltrating activated cytotoxic T lymphocytes, and frequent loss of HLA class I and II expression, are features of aggressive B cell lymphomas of the brain and testis. J Pathol 206: 328–336. doi: 10.1002/path.1783 15887291
54. Lippman SM, Spier CM, Miller TP, Slymen DJ, Rybski JA, et al. (1990) Tumor-infiltrating T-lymphocytes in B-cell diffuse large cell lymphoma related to disease course. Mod Pathol 3: 361–367. 2194216
55. Rimsza LM, Roberts RA, Miller TP, Unger JM, LeBlanc M, et al. (2004) Loss of MHC class II gene and protein expression in diffuse large B-cell lymphoma is related to decreased tumor immunosurveillance and poor patient survival regardless of other prognostic factors: a follow-up study from the Leukemia and Lymphoma Molecular Profiling Project. Blood 103: 4251–4258. 14976040
56. Burnett RC, Vernau W, Modiano JF, Olver CS, Moore PF, et al. (2003) Diagnosis of canine lymphoid neoplasia using clonal rearrangements of antigen receptor genes. Vet Pathol 40: 32–41. doi: 10.1354/vp.40-1-32 12627711
57. PLINK http://pngu.mgh.harvard.edu/purcell/plink/.
58. Price A, Patterson N, Plenge R, Weinblatt M, Shadick N, et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature genetics 38: 904–909. doi: 10.1038/ng1847 16862161
59. Consortium TWTCC, (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447: 661–678. doi: 10.1038/nature05911
60. Yang J, Manolio TA, Pasquale LR, Boerwinkle E, Caporaso N, et al. (2011) Genome partitioning of genetic variation for complex traits using common SNPs. Nat Genet 43: 519–525. doi: 10.1038/ng.823 21552263
61. Picard-pipeline http://picard.sourceforge.net.
62. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498. doi: 10.1038/ng.806 21478889
63. SEQscoring http://www.seqscoring.org.
64. Truvé KE O., Norling M, Wilbe M, Mauceli E, Lindblad-Toh K, Bongcam-Rudloff E, . (2011) SEQscoring: a tool to facilitate the interpretation of data generated with next generation sequencing technologies. EMBnet journal 17: 38. doi: 10.14806/ej.17.1.211
65. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, et al. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6: 80–92. doi: 10.4161/fly.19695
66. Thorvaldsdottir H, Robinson JT, Mesirov JP, (2012) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. doi: 10.1093/bib/bbs017 22517427
67. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073–1081. doi: 10.1038/nprot.2009.86 19561590
68. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111. doi: 10.1093/bioinformatics/btp120 19289445
69. HTseq http://www-huber.embl.de/users/anders/HTseq/.
70. Hoeppner MP, Lundquist A, Pirun M, Meadows JR, Zamani N, et al. (2014) An improved canine genome and a comprehensive catalogue of coding genes and non-coding transcripts. PLoS One 9: e91172. doi: 10.1371/journal.pone.0091172 24625832
71. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308
72. Kang H, Sul J, Service S, Zaitlen N, Kong S-Y, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42: 348–354. doi: 10.1038/ng.548 20208533