Canine Spontaneous Head and Neck Squamous Cell Carcinomas Represent Their Human Counterparts at the Molecular Level

English version České info

Head and neck squamous cell carcinoma (HNSCC) represents the sixth leading cancer by incidence in humans; thus, developing effective therapeutic interventions is important. Although great advance has been made in our understanding of the biology of HNSCC over the past several decades, translating the research findings into clinical success has been frustratingly slow, and anticancer drug development remains a lengthy and expensive process. A significant challenge is that drug effects in current preclinical cancer models often do not predict clinical results, and there lacks translational models that can bridge the gap between preclinical research and human clinical trials. Here we report a pilot study that represents the first genome-wide characterization of spontaneously occurring HNSCCs in pet dogs. The study reveals a strong dog-human molecular homology at various levels, indicating the likelihood that spontaneous canine HNSCC molecularly represents its human counterpart. If conclusions of this pilot study are validated with a large sample size and more efforts are put into building better resource and infrastructure for canine cancer research, spontaneous canine HNSCCs could effectively serve as a much-needed translational model that bridges the gap between preclinical research and human trials.

Vyšlo v časopise: Canine Spontaneous Head and Neck Squamous Cell Carcinomas Represent Their Human Counterparts at the Molecular Level. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005277
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005277

Souhrn

Zdroje

1. Cancer Genome Atlas N (2015) Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 517 : 576–582. doi: 10.1038/nature14129 25631445

2. Pickering CR, Zhang J, Yoo SY, Bengtsson L, Moorthy S, et al. (2013) Integrative genomic characterization of oral squamous cell carcinoma identifies frequent somatic drivers. Cancer discovery 3 : 770–781. doi: 10.1158/2159-8290.CD-12-0537 23619168

3. Stransky N, Egloff AM, Tward AD, Kostic AD, Cibulskis K, et al. (2011) The Mutational Landscape of Head and Neck Squamous Cell Carcinoma. Science 333 : 1157–1160. doi: 10.1126/science.1208130 21798893

4. Agrawal N, Frederick MJ, Pickering CR, Bettegowda C, Chang K, et al. (2011) Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 333 : 1154–1157. doi: 10.1126/science.1206923 21798897

5. Hammerman PS, Hayes DN, Grandis JR (2015) Therapeutic Insights from Genomic Studies of Head and Neck Squamous Cell Carcinomas. Cancer discovery doi: 10.1158/2159-8290.CD-14-1205

6. Leemans CR, Braakhuis BJ, Brakenhoff RH (2011) The molecular biology of head and neck cancer. Nature reviews Cancer 11 : 9–22. doi: 10.1038/nrc2982 21160525

7. Bose P, Brockton NT, Dort JC (2013) Head and neck cancer: from anatomy to biology. International journal of cancer Journal international du cancer 133 : 2013–2023. doi: 10.1002/ijc.28112 23417723

8. Cantley LC, Baselga J (2011) The Era of Cancer Discovery. Cancer discovery 1 : 1–U15. doi: 10.1158/2159-8274.CD-11-0049 22586302

9. Hait WN (2010) Anticancer drug development: the grand challenges. Nature reviews Drug discovery 9 : 253–254. doi: 10.1038/nrd3144 20369394

10. Kim S (2009) Animal models of cancer in the head and neck region. Clinical and experimental otorhinolaryngology 2 : 55–60. doi: 10.3342/ceo.2009.2.2.55 19565028

11. Richmond A, Su Y (2008) Mouse xenograft models vs GEM models for human cancer therapeutics. Disease models & mechanisms 1 : 78–82.

12. Lu SL, Herrington H, Wang XJ (2006) Mouse models for human head and neck squamous cell carcinomas. Head & neck 28 : 945–954.

13. Simon C, Nemechek AJ, Boyd D, O'Malley BW Jr., Goepfert H, et al. (1998) An orthotopic floor-of-mouth cancer model allows quantification of tumor invasion. The Laryngoscope 108 : 1686–1691. 9818827

14. Visvader JE (2011) Cells of origin in cancer. Nature 469 : 314–322. doi: 10.1038/nature09781 21248838

15. Meuten DJ (2002) Tumors in domestic animals. Ames, Iowa: Iowa State University Press. xii, 788 p. p.

16. Paoloni M, Khanna C (2008) Translation of new cancer treatments from pet dogs to humans. Nature reviews Cancer 8 : 147–156. doi: 10.1038/nrc2273 18202698

17. Rowell JL, McCarthy DO, Alvarez CE (2011) Dog models of naturally occurring cancer. Trends in molecular medicine 17 : 380–388. doi: 10.1016/j.molmed.2011.02.004 21439907

18. Gordon I, Paoloni M, Mazcko C, Khanna C (2009) The Comparative Oncology Trials Consortium: using spontaneously occurring cancers in dogs to inform the cancer drug development pathway. PLoS medicine 6: e1000161. doi: 10.1371/journal.pmed.1000161 19823573

19. Tang J, Le S, Sun L, Yan X, Zhang M, et al. (2010) Copy number abnormalities in sporadic canine colorectal cancers. Genome research 20 : 341–350. doi: 10.1101/gr.092726.109 20086242

20. Youmans L, Taylor C, Shin E, Harrell A, Ellis AE, et al. (2012) Frequent alteration of the tumor suppressor gene APC in sporadic canine colorectal tumors. PloS one 7: e50813. doi: 10.1371/journal.pone.0050813 23251390

21. Liu D, Xiong H, Ellis AE, Northrup NC, Rodriguez CO, Jr., et al. (2014) Molecular homology and difference between spontaneous canine mammary cancer and human breast cancer. Cancer research doi: 10.1158/0008-5472.CAN-14-0392

22. Fenger JM, London CA, Kisseberth WC (2014) Canine osteosarcoma: a naturally occurring disease to inform pediatric oncology. ILAR journal / National Research Council, Institute of Laboratory Animal Resources 55 : 69–85. doi: 10.1093/ilar/ilu009 24936031

23. Gorden BH, Kim JH, Sarver AL, Frantz AM, Breen M, et al. (2014) Identification of Three Molecular and Functional Subtypes in Canine Hemangiosarcoma through Gene Expression Profiling and Progenitor Cell Characterization. American Journal of Pathology 184 : 985–995. doi: 10.1016/j.ajpath.2013.12.025 24525151

24. Boyko AR (2011) The domestic dog: man's best friend in the genomic era. Genome biology 12 : 216. doi: 10.1186/gb-2011-12-2-216 21338479

25. Rotroff DM, Thomas R, Breen M, Motsinger-Reif AA (2013) Naturally occuring canine cancers: powerful models for stimulating pharmacogenomic advancement in human medicine. Pharmacogenomics 14 : 1929–1931. doi: 10.2217/pgs.13.178 24279843

26. Angstadt AY, Thayanithy V, Subramanian S, Modiano JF, Breen M (2012) A genome-wide approach to comparative oncology: high-resolution oligonucleotide aCGH of canine and human osteosarcoma pinpoints shared microaberrations. Cancer genetics 205 : 572–587. doi: 10.1016/j.cancergen.2012.09.005 23137772

27. Candille SI, Kaelin CB, Cattanach BM, Yu B, Thompson DA, et al. (2007) A-defensin mutation causes black coat color in domestic dogs. Science 318 : 1418–1423. 17947548

28. Davis BW, Ostrander EA (2014) Domestic dogs and cancer research: a breed-based genomics approach. ILAR journal / National Research Council, Institute of Laboratory Animal Resources 55 : 59–68. doi: 10.1093/ilar/ilu017 24936030

29. Karyadi DM, Karlins E, Decker B, vonHoldt BM, Carpintero-Ramirez G, et al. (2013) A copy number variant at the KITLG locus likely confers risk for canine squamous cell carcinoma of the digit. PLoS genetics 9: e1003409. doi: 10.1371/journal.pgen.1003409 23555311

30. Tang J, Li Y, Lyon K, Camps J, Dalton S, et al. (2014) Cancer driver-passenger distinction via sporadic human and dog cancer comparison: a proof-of-principle study with colorectal cancer. Oncogene 33 : 814–822. doi: 10.1038/onc.2013.17 23416983

31. Nasir L, Devlin P, McKevitt T, Rutteman G, Argyle DJ (2001) Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia 3 : 351–359. 11571635

32. Rangarajan A, Weinberg RA (2003) Opinion: Comparative biology of mouse versus human cells: modelling human cancer in mice. Nature reviews Cancer 3 : 952–959. 14737125

33. 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. 16341006

34. Ji X, Zhao S (2008) DA and Xiao-two giant and composite LTR-retrotransposon-like elements identified in the human genome. Genomics 91 : 249–258. 18083327

35. Gardner DG (1996) Spontaneous squamous cell carcinomas of the oral region in domestic animals: a review and consideration of their relevance to human research. Oral diseases 2 : 148–154. 8957928

36. Strafuss AC, Cook JE, Smith JE (1976) Squamous cell carcinoma in dogs. Journal of the American Veterinary Medical Association 168 : 425–427. 1254515

37. Hoyt RF, Withrow SJ (1984) Oral Malignancy in the Dog. J Am Anim Hosp Assoc 20 : 83–92.

38. Ragin CCR, Modugno F, Gollin SM (2007) The epidemiology and risk factors of head and neck cancer: a focus on human papillomavirus. J Dent Res 86 : 104–114. 17251508

39. Teifke JP, Lohr CV, Shirasawa H (1998) Detection of canine oral papillomavirus-DNA in canine oral squamous cell carcinomas and p53 overexpressing skin papillomas of the dog using the polymerase chain reaction and non-radioactive in situ hybridization. Vet Microbiol 60 : 119–130. 9646444

40. de Vos JP, Burm AG, Focker AP, Boschloo H, Karsijns M, et al. (2005) Piroxicam and carboplatin as a combination treatment of canine oral non-tonsillar squamous cell carcinoma: a pilot study and a literature review of a canine model of human head and neck squamous cell carcinoma. Veterinary and comparative oncology 3 : 16–24. doi: 10.1111/j.1476-5810.2005.00065.x 19379210

41. LaDueMiller T, Price GS, Page RL, Thrall DE (1996) Radiotherapy of canine non-tonsillar squamous cell carcinoma. Vet Radiol Ultrasoun 37 : 74–77.

42. Richards KL, Motsinger-Reif AA, Chen HW, Fedoriw Y, Fan C, et al. (2013) Gene profiling of canine B-cell lymphoma reveals germinal center and postgerminal center subtypes with different survival times, modeling human DLBCL. Cancer research 73 : 5029–5039. doi: 10.1158/0008-5472.CAN-12-3546 23783577

43. Thomas R, Seiser EL, Motsinger-Reif A, Borst L, Valli VE, et al. (2011) Refining tumor-associated aneuploidy through 'genomic recoding' of recurrent DNA copy number aberrations in 150 canine non-Hodgkin lymphomas. Leukemia Lymphoma 52 : 1321–1335. doi: 10.3109/10428194.2011.559802 21375435

44. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, et al. (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer discovery 2 : 401–404. doi: 10.1158/2159-8290.CD-12-0095 22588877

45. Cancer Genome Atlas N (2012) Comprehensive molecular portraits of human breast tumours. Nature 490 : 61–70. doi: 10.1038/nature11412 23000897

46. Cancer Genome Atlas N (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487 : 330–337. doi: 10.1038/nature11252 22810696

47. Freier K, Knoepfle K, Flechtenmacher C, Pungs S, Devens F, et al. (2010) Recurrent copy number gain of transcription factor SOX2 and corresponding high protein expression in oral squamous cell carcinoma. Genes, chromosomes & cancer 49 : 9–16.

48. Chen Y, Chen C (2008) DNA copy number variation and loss of heterozygosity in relation to recurrence of and survival from head and neck squamous cell carcinoma: a review. Head & neck 30 : 1361–1383.

49. Wei W, Bracher-Manecke JC, Zhao X, Davies NH, Zhou L, et al. (2013) Oncogenic but non-essential role of N-myc downstream regulated gene 1 in the progression of esophageal squamous cell carcinoma. Cancer biology & therapy 14 : 164–174.

50. Melotte V, Qu XH, Ongenaert M, van Criekinge W, de Bruine AP, et al. (2010) The N-myc downstream regulated gene (NDRG) family: diverse functions, multiple applications. Faseb J 24 : 4153–4166. doi: 10.1096/fj.09-151464 20667976

51. Ortiz B, White JR, Wu WH, Chan TA (2014) Deletion of Ptprd and Cdkn2a cooperate to accelerate tumorigenesis. Oncotarget.

52. Nishikawa Y, Miyazaki T, Nakashiro KI, Yamagata H, Isokane M, et al. (2011) Human FAT1 cadherin controls cell migration and invasion of oral squamous cell carcinoma through the localization of beta-catenin. Oncology reports 26 : 587–592. doi: 10.3892/or.2011.1324 21617878

53. Royer C, Lu X (2011) Epithelial cell polarity: a major gatekeeper against cancer? Cell death and differentiation 18 : 1470–1477. doi: 10.1038/cdd.2011.60 21617693

54. Govindan R, Ding L, Griffith M, Subramanian J, Dees ND, et al. (2012) Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 150 : 1121–1134. doi: 10.1016/j.cell.2012.08.024 22980976

55. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, et al. (2012) The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481 : 157–163. doi: 10.1038/nature10725 22237106

56. Blitzer GC, Smith MA, Harris SL, Kimple RJ (2014) Review of the clinical and biologic aspects of human papillomavirus-positive squamous cell carcinomas of the head and neck. International journal of radiation oncology, biology, physics 88 : 761–770. doi: 10.1016/j.ijrobp.2013.08.029 24606845

57. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, et al. (2013) Signatures of mutational processes in human cancer. Nature 500 : 415–421. doi: 10.1038/nature12477 23945592

58. Salk JJ, Horwitz MS (2010) Passenger mutations as a marker of clonal cell lineages in emerging neoplasia. Semin Cancer Biol 20 : 294–303. doi: 10.1016/j.semcancer.2010.10.008 20951806

59. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate—a Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc B Met 57 : 289–300.

60. Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, et al. (2007) Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proceedings of the National Academy of Sciences of the United States of America 104 : 20007–20012.

61. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome biology 11: R106. doi: 10.1186/gb-2010-11-10-r106 20979621

62. Yaping Li JX, Huan Xiong, Zhongyao Ma, Zhenghe Wang, Kipreos Edward T., Stephen Dalton and Shaying Zhao (2014) Cancer driver candidate genes AVL9, DENND5A and NUPL1 contribute to MDCK cystogenesis. Oncoscience 1 : 854–865. 25621300