Cross-species models of human melanoma

Journal of Pathology

Volumn 238, Issue 2, 2016, Pages 152-165

  Van Der Weyden, Louise ^a   Patton, E Elizabeth ^b   Wood, Geoffrey A ^c   Foote, Alastair K ^d   Brenn, Thomas ^e   Arends, Mark J ^f   Adams, David J ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF GUELPH   (Canada)

^d Rossdales Equine Hospital and Diagnositc Centre   (United Kingdom)

^e WESTERN GENERAL HOSPITAL   (United Kingdom)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cross species analysis; Genome analysis; Melanoma

Indexed keywords

B RAF KINASE; BAP1 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; NRAS PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN P16; PROTEIN P53; STEM CELL FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL MODEL; CLINICAL FEATURE; CROSS BREEDING; DISEASE COURSE; DOG BREED; EQUIDAE; GENETIC ANALYSIS; GENETIC ENGINEERING; GENETIC HETEROGENEITY; GENETIC PREDISPOSITION; GENOMICS; HUMAN; INCIDENCE; MELANOCYTE; MELANOMA; MELANOMA CELL LINE; MURINE; NEXT GENERATION SEQUENCING; NONHUMAN; PATHOLOGICAL ANATOMY; PRIORITY JOURNAL; REVIEW; SOMATIC MUTATION; TRANSPLANTATION; TUMOR XENOGRAFT; ZEBRA FISH; ANIMAL; CANCER TRANSPLANTATION; DISEASE MODEL; DOG; GENETICS; GENOME; HORSE; MOUSE; MUTATION; SKIN NEOPLASMS; TRANSGENIC MOUSE; TUMOR CELL LINE; UVEAL NEOPLASMS; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOGS; GENETIC PREDISPOSITION TO DISEASE; GENOME; HORSES; HUMANS; MELANOMA; MICE; MICE, TRANSGENIC; MUTATION; NEOPLASM TRANSPLANTATION; SKIN NEOPLASMS; TRANSPLANTATION, HETEROLOGOUS; UVEAL NEOPLASMS; ZEBRAFISH;

EID: 84951317305     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4632     Document Type: Review

References (142)

1. Hill VK, Gartner JJ, Samuels Y, et al., The genetics of melanoma: recent advances. Annu Rev Genomics Hum Genet 2013; 14: 257-279.
2. Law MH, Bishop DT, Lee JE, et al., Genome-wide meta-analysis identifies five new susceptibility loci for cutaneous malignant melanoma. Nature Genet 2015; 47: 987-995.
3. Schiöth HB, Raudsepp T, Ringholm A, et al., Remarkable synteny conservation of melanocortin receptors in chicken, human, and other vertebrates. Genomics 2003; 81: 504-509.
4. Scherer D, Kumar R,. Genetics of pigmentation in skin cancer-a review. Mutat Res 2010; 705: 141-153.
5. Shibahara S., Mutations of the tyrosinase gene in oculocutaneous albinism. Pigment Cell Res 1992; 5: 279-283.
6. Yokoyama S, Woods SL, Boyle GM, et al., A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature 2011; 480: 99-103.
7. Duffy DL, Iles MM, Glass D, et al., IRF4 variants have age-specific effects on nevus count and predispose to melanoma. Am J Hum Genet 2010; 87: 6-16.
8. Kamb A, Shattuck-Eidens D, Eeles R, et al., Analysis of the p16 gene (CDKN2) as a candidate for the chromosome 9p melanoma susceptibility locus. Nature Genet 1994; 8: 23-26.
9. Hussussian CJ, Struewing JP, Goldstein AM, et al., Germline p16 mutations in familial melanoma. Nature Genet 1994; 8: 15-21.
10. INK4 function. Nature Genet 1995; 10: 114-116.
11. Horn S, Figl A, Rachakonda PS, et al., TERT promoter mutations in familial and sporadic melanoma. Science 2013; 339: 959-961.
12. Robles-Espinoza CD, Harland M, Ramsay AJ, et al., POT1 loss-of-function variants predispose to familial melanoma. Nature Genet 2014; 46: 478-481.
13. Shi J, Yang XR, Ballew B, et al., Rare missense variants in POT1 predispose to familial cutaneous malignant melanoma. Nat Genet 2014; 46: 482-486.
14. Aoude LG, Pritchard AL, Robles-Espinoza CD, et al., Nonsense mutations in the shelterin complex genes ACD and TERF2IP in familial melanoma. J Natl Cancer Inst 2015; 107: dju408.
15. Harbour JW, Onken MD, Roberson EDO, et al., Frequent mutation of BAP1 in metastasizing uveal melanomas. Science 2010; 330: 1410-1413.
16. Battaglia A., The importance of multidisciplinary approach in early detection of BAP1 tumor predisposition syndrome: clinical management and risk assessment. Clin Med Insights Oncol 2014; 8: 37-47.
17. Bastian BC,. The molecular pathology of melanoma: an integrated taxonomy of melanocytic neoplasia. Annu Rev Pathol 2014; 9: 239-271.
18. Rosengren Pielberg G, Golovko A, Sundström E, et al., A cis-acting regulatory mutation causes premature hair graying and susceptibility to melanoma in the horse. Nature Genet 2008; 40: 1004-1009.
19. Dobson JM,. Breed-predispositions to cancer in pedigree dogs. ISRN Vet Sci 2013; 2013: 941275.
20. Puig S, Ruiz A, Lázaro C, et al., Chromosome 9p deletions in cutaneous malignant melanoma tumors: the minimal deleted region involves markers outside the p16 (CDKN2) gene. Am J Hum Genet 1995; 57: 395-402.
21. Guldberg P, thor Straten P, Birck A, et al., Disruption of the MMAC1/PTEN gene by deletion or mutation is a frequent event in malignant melanoma. Cancer Res 1997; 57: 3660-3663.
22. Chin L, Pomerantz J, Polsky D, et al., Cooperative effects of INK4a and ras in melanoma susceptibility in vivo. Genes Dev 1997; 11: 2822-2834.
23. Eskandarpour M, Hashemi J, Kanter L, et al., Frequency of UV-inducible NRAS mutations in melanomas of patients with germline CDKN2A mutations. J Natl Cancer Inst 2003; 95: 790-798.
24. Della Porta G., Cellular and molecular biology of melanoma. Semin Surg Oncol 1992; 8: 353-357.
25. van't Veer LJ, Burgering BM, Versteeg R, et al., N-ras mutations in human cutaneous melanoma from sun-exposed body sites. Mol Cell Biol 1989; 9: 3114-3116.
26. Davies H, Bignell GR, Cox C, et al., Mutations of the BRAF gene in human cancer. Nature 2002; 417: 949-954.
27. Dossett LA, Kudchadkar RR, Zager JS,. BRAF and MEK inhibition in melanoma. Expert Opin Drug Safety 2015; 14: 559-570.
28. Krauthammer M, Kong Y, Ha BH, et al., Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nature Genet 2012; 44: 1006-1014.
29. Cancer Genome Atlas Network,. Genomic classification of cutaneous melanoma. Cell 2015; 161: 1681-1696.
30. Hodis E, Watson IR, Kryukov GV, et al., A landscape of driver mutations in melanoma. Cell 2012; 150: 251-263.
31. Wilsker D, Probst L, Wain HM, et al., Nomenclature of the ARID family of DNA-binding proteins. Genomics 2005; 86: 242-251.
32. Hammond D, Zeng K, Espert A, et al., Melanoma-associated mutations in protein phosphatase 6 cause chromosome instability and DNA damage owing to dysregulated Aurora-A. J Cell Sci 2013; 126: 3429-3440.
33. Fecher LA, Amaravadi RK, Flaherty KT,. The MAPK pathway in melanoma. Curr Opin Oncol 2008; 20: 183-189.
34. Turajlic S, Furney SJ, Lambros MB, et al., Whole genome sequencing of matched primary and metastatic acral melanomas. Genome Res 2012; 22: 196-207.
35. Furney SJ, Turajlic S, Fenwick K, et al., Genomic characterisation of acral melanoma cell lines. Pigment Cell Melanoma Res 2012; 25: 488-492.
36. Pervaiz S, Cao J, Chao OS, et al., Activation of the RacGTPase inhibits apoptosis in human tumor cells. Oncogene 2001; 20: 6263-6268.
37. Fidler IJ,. Selection of successive tumour lines for metastasis. Nature New Biol 1973; 242: 148-149.
38. Maslow DE,. Tabulation of results on the heterogeneity of cellular characteristics among cells from B16 mouse melanoma cell lines with different colonization potentials. A summary of sixty reports. Invasion Metastasis 1989; 9: 182-191.
39. Pawlowski A, Lea PJ,. Human melanoma xenografts. Carcinog Compr Surv 1989; 11: 103-132.
40. Kerbel RS,. Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived-but they can be improved. Cancer Biol Ther 2003; 2: S134-S139.
41. Khaled WT, Liu P,. Cancer mouse models: past, present and future. Semin Cell Dev Biol 2014; 27: 54-60.
42. Quintana E, Piskounova E, Shackleton M, et al., Human melanoma metastasis in NSG mice correlates with clinical outcome in patients. Sci Transl Med 2012; 4:159ra149.
43. Einarsdottir BO, Bagge RO, Bhadury J, et al., Melanoma patient-derived xenografts accurately model the disease and develop fast enough to guide treatment decisions. Oncotarget 2014; 5: 9609-9618.
44. Tanaka S, Saito Y, Kunisawa J, et al., Development of mature and functional human myeloid subsets in hematopoietic stem cell-engrafted NOD/SCID/IL2rγKO mice. J Immunol 2012; 188: 6145-6155.
45. Arf predisposes mice to tumorigenesis. Nature 2001; 413: 86-91.
46. Campagne C, Reyes-Gomez E, Battistella M, et al., Histopathological atlas and proposed classification for melanocytic lesions in Tyr::NRas(Q61K); Cdkn2a(-/-) transgenic mice. Pigment Cell Melanoma Res 2013; 26: 735-742.
47. Dhomen N, Reis-Filho JS, da Rocha Dias S, et al., Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 2009; 15: 294-303.
48. Perna D, Karreth FA, Rust AG, et al., BRAF inhibitor resistance mediated by the AKT pathway in an oncogenic BRAF mouse melanoma model. Proc Natl Acad Sci U S A 2015; 112: E536-E545.
49. V600E cooperates with Pten loss to induce metastatic melanoma. Nature Genet 2009; 41: 544-552.
50. Noonan FP, Recio JA, Takayama H, et al., Neonatal sunburn and melanoma in mice. Nature 2001; 413: 271-272.
51. Gaffal E, Landsberg J, Bald T, et al., Neonatal UVB exposure accelerates melanoma growth and enhances distant metastases in Hgf-Cdk4(R24C) C57BL/6 mice. Int J Cancer 2011; 129: 285-294.
52. Bald T, Quast T, Landsberg J, et al., Ultraviolet-radiation-induced inflammation promotes angiotropism and metastasis in melanoma. Nature 2014; 507: 109-113.
53. Jarrett SG, Novak M, Harris N, et al., NM23 deficiency promotes metastasis in a UV radiation-induced mouse model of human melanoma. Clin Exp Metastasis 2013; 30: 25-36.
54. Ha L, Ichikawa T, Anver M, et al., ARF functions as a melanoma tumor suppressor by inducing p53-independent senescence. Proc Natl Acad Sci U S A 2007; 104: 10968-10973.
55. Moulton J, (ed). Tumors in Domestic Animals (3rd edn). University of California Press: Berkeley and Los Angeles, 1990.
56. Gillard M, Cadieu E, De Brito C, et al., Naturally occurring melanomas in dogs as models for non-UV pathways of human melanomas. Pigment Cell Melanoma Res 2014; 27: 90-102.
57. Withrow SJ, Vail DM, Page RL (eds). Withrow and MacEwen's Small Animal Clinical Oncology (5th edn). Elsevier Saunders: St Louis, 2013.
58. Suckow MA,. Cancer vaccines: harnessing the potential of anti-tumor immunity. Vet J 2013; 198: 28-33.
59. Grosenbaugh DA, Leard AT, Bergman PJ, et al., Safety and efficacy of a xenogeneic DNA vaccine encoding for human tyrosinase as adjunctive treatment for oral malignant melanoma in dogs following surgical excision of the primary tumor. Am J Vet Res 2011; 72: 1631-1638.
60. Vail DM,. Levels of evidence in canine oncology trials-a case in point. Vet Comp Oncol 2013; 11: 167-168.
61. Ottnod JM, Smedley RC, Walshaw R, et al., A retrospective analysis of the efficacy of Oncept vaccine for the adjunct treatment of canine oral malignant melanoma. Vet Comp Oncol 2013; 11: 219-229.
62. Finocchiaro LME, Fondello C, Gil-Cardeza ML, et al., Cytokine-enhanced vaccine and interferon-β plus suicide gene therapy as surgery adjuvant treatments for spontaneous canine melanoma. Hum Gene Ther 2015; 26: 367-376.
63. Riccardo F, Iussich S, Maniscalco L, et al., CSPG4-specific immunity and survival prolongation in dogs with oral malignant melanoma immunized with human CSPG4 DNA. Clin Cancer Res 2014; 20: 3753-3762.
64. London CA,. Tyrosine kinase inhibitors in veterinary medicine. Top Companion Anim Med 2009; 24: 106-112.
65. Lindblad-Toh K, Wade CM, Mikkelsen TS, et al., Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 2005; 438: 803-819.
66. Mochizuki H, Kennedy K, Shapiro SG, et al., BRAF mutations in canine cancers. PloS One 2015; 10:e0129534.
67. Poorman K, Borst L, Moroff S, et al., Comparative cytogenetic characterization of primary canine melanocytic lesions using array CGH and fluorescence in situ hybridization. Chromosome Res 2015; 23: 171-186.
68. Hutchinson L, Kirk R,. High drug attrition rates-where are we going wrong? Nature Rev Clin Oncol 2011; 8: 189-190.
69. Khanna C, Lindblad-Toh K, Vail D, et al., The dog as a cancer model. Nature Biotechnol 2006; 24: 1065-1066.
70. Gordon I, Paoloni M, Mazcko C, et al., The Comparative Oncology Trials Consortium: using spontaneously occurring cancers in dogs to inform the cancer drug development pathway. PLoS Med 2009; 6:e1000161.
71. Khanna C, London C, Vail D, et al., Guiding the optimal translation of new cancer treatments from canine to human cancer patients. Clin Cancer Res 2009; 15: 5671-5677.
72. Paoloni M, Khanna C,. Translation of new cancer treatments from pet dogs to humans. Nature Rev Cancer 2008; 8: 147-156.
73. Simpson RM, Bastian BC, Michael HT, et al., Sporadic naturally occurring melanoma in dogs as a preclinical model for human melanoma. Pigment Cell Melanoma Res 2014; 27: 37-47.
74. Knowles EJ, Tremaine WH, Pearson GR, et al., A database survey of equine tumours in the United Kingdom. Equine Vet J 2015; DOI: 10.1111/evj.12421.
75. Johnson PJ,. Dermatologic tumors (excluding sarcoids). Vet Clin North Am Equine Pract 1998; 14: 625-658, viii.
76. Valentine BA,. Survey of equine cutaneous neoplasia in the Pacific Northwest. J Vet Diagn Invest 2006; 18: 123-126.
77. Smith SH, Goldschmidt MH, McManus PM,. A comparative review of melanocytic neoplasms. Vet Pathol 2002; 39: 651-678.
78. Valentine BA,. Equine melanocytic tumors: a retrospective study of 53 horses (1988 to 1991). J Vet Intern Med 1995; 9: 291-297.
79. Schöniger S, Summers BA,. Equine skin tumours in 20 horses resembling three variants of human melanocytic naevi. Vet Dermatol 2009; 20: 165-173.
80. MacFadyean J., Equine melanomatosis. J Comp Pathol Ther 1933; 46: 186-204.
81. Knottenbelt DC, Patterson-Kane JC, Snalune KL. Clinical Equine Oncology. Elsevier: Amsterdam, 2015.
82. MacGillivray KC, Sweeney RW, Del Piero F,. Metastatic melanoma in horses. J Vet Intern Med 2002; 16: 452-456.
83. Campagne C, Julé S, Bernex F, et al., RACK1, a clue to the diagnosis of cutaneous melanomas in horses. BMC Vet Res 2012; 8: 95.
84. Barnett KC, Platt H,. Intraocular melanomata in the horse. Equine Vet J Suppl 1990; 22: 76-82.
85. Dixon PM, Head KW,. Equine nasal and paranasal sinus tumours: part 2: a contribution of 28 case reports. Vet J 1999; 157: 279-294.
86. Head KW, Dixon PM,. Equine nasal and paranasal sinus tumours. Part 1: review of the literature and tumour classification. Vet J 1999; 157: 261-278.
87. Jiang L, Campagne C, Sundström E, et al., Constitutive activation of the ERK pathway in melanoma and skin melanocytes in Grey horses. BMC Cancer 2014; 14: 857.
88. Sundström E, Komisarczuk AZ, Jiang L, et al., Identification of a melanocyte-specific, microphthalmia-associated transcription factor-dependent regulatory element in the intronic duplication causing hair greying and melanoma in horses. Pigment Cell Melanoma Res 2012; 25: 28-36.
89. Teixeira RBC, Rendahl AK, Anderson SM, et al., Coat color genotypes and risk and severity of melanoma in gray quarter horses. J Vet Intern Med 2013; 27: 1201-1208.
90. Seltenhammer MH, Sundström E, Meisslitzer-Ruppitsch C, et al., Establishment and characterization of a primary and a metastatic melanoma cell line from Grey horses. In Vitro Cell Dev Biol Anim 2014; 50: 56-65.
91. Zembowicz A, Carney JA, Mihm MC,. Pigmented epithelioid melanocytoma: a low-grade melanocytic tumor with metastatic potential indistinguishable from animal-type melanoma and epithelioid blue nevus. Am J Surg Pathol 2004; 28: 31-40.
92. Ludgate MW, Fullen DR, Lee J, et al., Animal-type melanoma: a clinical and histopathological study of 22 cases from a single institution. Br J Dermatol 2010; 162: 129-136.
93. Zhao ZZ, Duffy DL, Thomas SA, et al., Polymorphisms in the syntaxin 17 gene are not associated with human cutaneous malignant melanoma. Melanoma Res 2009; 19: 80-86.
94. Howe K, Clark MD, Torroja CF, et al., The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496: 498-503.
95. Ablain J, Durand EM, Yang S, et al., A CRISPR/Cas9 vector system for tissue-specific gene disruption in zebrafish. Dev Cell 2015; 32: 756-764.
96. Irion U, Krauss J, Nüsslein-Volhard C,. Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system. Development 2014; 141: 4827-4830.
97. Jao L-E, Wente SR, Chen W,. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A 2013; 110: 13904-13909.
98. Chang N, Sun C, Gao L, et al., Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res 2013; 23: 465-472.
99. Hwang WY, Fu Y, Reyon D, et al., Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnol 2013; 31: 227-229.
100. Patton EE, Widlund HR, Kutok JL, et al., BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr Biol 2005; 15: 249-254.
101. Ceol CJ, Houvras Y, Jane-Valbuena J, et al., The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 2011; 471: 513-517.
102. White RM, Zon LI,. Melanocytes in development, regeneration, and cancer. Cell Stem Cell 2008; 3: 242-252.
103. Zeng Z, Johnson SL, Lister JA, et al., Temperature-sensitive splicing of mitfa by an intron mutation in zebrafish. Pigment Cell Melanoma Res 2015; 28: 229-232.
104. Lister JA, Capper A, Zeng Z, et al., A conditional zebrafish MITF mutation reveals MITF levels are critical for melanoma promotion vs. regression in vivo. J Invest Dermatol 2014; 134: 133-140.
105. Taylor KL, Lister JA, Zeng Z, et al., Differentiated melanocyte cell division occurs in vivo and is promoted by mutations in Mitf. Development 2011; 138: 3579-3589.
106. Michailidou C, Jones M, Walker P, et al., Dissecting the roles of Raf- and PI3K-signalling pathways in melanoma formation and progression in a zebrafish model. Dis Model Mech 2009; 2: 399-411.
107. Dalton LE, Kamarashev J, Barinaga-Rementeria Ramirez I, et al., Constitutive RAC activation is not sufficient to initiate melanocyte neoplasia but accelerates malignant progression. J Invest Dermatol 2013; 133: 1572-1581.
108. Santoriello C, Gennaro E, Anelli V, et al., Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PloS One 2010; 5:e15170.
109. Dovey M, White RM, Zon LI,. Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish 2009; 6: 397-404.
110. Yen J, White RM, Wedge DC, et al., The genetic heterogeneity and mutational burden of engineered melanomas in zebrafish models. Genome Biol 2013; 14: R113.
111. 2. Curr Biol 2012; 22: 1253-1259.
112. Feng Y, Santoriello C, Mione M, et al., Live imaging of innate immune cell sensing of transformed cells in zebrafish larvae: parallels between tumor initiation and wound inflammation. PLoS Biol 2010; 8:e1000562.
113. Taylor AM, Zon LI,. Zebrafish tumor assays: the state of transplantation. Zebrafish 2009; 6: 339-346.
114. Díez-Torre A, Andrade R, Eguizábal C, et al., Reprogramming of melanoma cells by embryonic microenvironments. Int J Dev Biol 2009; 53: 1563-1568.
115. Haldi M, Ton C, Seng WL, et al., Human melanoma cells transplanted into zebrafish proliferate, migrate, produce melanin, form masses and stimulate angiogenesis in zebrafish. Angiogenesis 2006; 9: 139-151.
116. Topczewska JM, Postovit L-M, Margaryan NV, et al., Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nature Med 2006; 12: 925-932.
117. Lee LMJ, Seftor EA, Bonde G, et al., The fate of human malignant melanoma cells transplanted into zebrafish embryos: assessment of migration and cell division in the absence of tumor formation. Dev Dyn 2005; 233: 1560-1570.
118. Lawson ND, Weinstein BM,. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 2002; 248: 307-318.
119. Hoffman SJ, Psaltis PJ, Clark KJ, et al., An in vivo method to quantify lymphangiogenesis in zebrafish. PloS One 2012; 7:e45240.
120. Chapman A, Fernandez del Ama L, Ferguson J, et al., Heterogeneous tumor subpopulations cooperate to drive invasion. Cell Rep 2014; 8: 688-695.
121. Spaink HP, Cui C, Wiweger MI, et al., Robotic injection of zebrafish embryos for high-throughput screening in disease models. Methods 2013; 62: 246-254.
122. He S, Lamers GE, Beenakker J-WM, et al., Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model. J Pathol 2012; 227: 431-445.
123. Li P, White RM, Zon LI,. Transplantation in zebrafish. Methods Cell Biol 2011; 105: 403-417.
124. White RM, Sessa A, Burke C, et al., Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2008; 2: 183-189.
125. Rennekamp AJ, Peterson RT,. 15 years of zebrafish chemical screening. Curr Opin Chem Biol 2015; 24: 58-70.
126. White RM, Cech J, Ratanasirintrawoot S, et al., DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 2011; 471: 518-522.
127. Zhou L, Ishizaki H, Spitzer M, et al., ALDH2 mediates 5-nitrofuran activity in multiple species. Chem Biol 2012; 19: 883-892.
128. White R, Rose K, Zon L,. Zebrafish cancer: the state of the art and the path forward. Nature Rev Cancer 2013; 13: 624-636.
129. Zon L., Translational research: the path for bringing discovery to patients. Cell Stem Cell 2014; 14: 146-148.
130. Millikan LE, Boylon JL, Hook RR, et al., Melanoma in Sinclair swine: a new animal model. J Invest Dermatol 1974; 62: 20-30.
131. Vincent-Naulleau S, Le Chalony C, Leplat J-J, et al., Clinical and histopathological characterization of cutaneous melanomas in the melanoblastoma-bearing Libechov minipig model. Pigment Cell Res 2004; 17: 24-35.
132. Chudnovsky Y, Adams AE, Robbins PB, et al., Use of human tissue to assess the oncogenic activity of melanoma-associated mutations. Nature Genet 2005; 37: 745-749.
133. Patton EE, Mitchell DL, Nairn RS,. Genetic and environmental melanoma models in fish. Pigment Cell Melanoma Res 2010; 23: 314-337.
134. Harrington M., Marsupials that model melanoma. Lab Anim 2015; 44: 53.
135. Ackermann J, Frutschi M, Kaloulis K, et al., Metastasizing melanoma formation caused by expression of activated N-RasQ61K on an INK4a-deficient background. Cancer Res 2005; 65: 4005-4011.
136. Iwamoto T, Takahashi M, Ito M, et al., Aberrant melanogenesis and melanocytic tumour development in transgenic mice that carry a metallothionein/ret fusion gene. EMBO J 1991; 10: 3167-3175.
137. Kato M, Takahashi M, Akhand AA, et al., Transgenic mouse model for skin malignant melanoma. Oncogene 1998; 17: 1885-1888.
138. Kumasaka MY, Yajima I, Hossain K, et al., A novel mouse model for de novo melanoma. Cancer Res 2010; 70: 24-29.
139. Takayama H, LaRochelle WJ, Sharp R, et al., Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc Natl Acad Sci U S A 1997; 94: 701-706.
140. Noonan FP, Recio JA, Takayama H, et al., Neonatal sunburn and melanoma in mice. Nature 2001; 413: 271-272.
141. Tormo D, Ferrer A, Bosch P, et al., Therapeutic efficacy of antigen-specific vaccination and toll-like receptor stimulation against established transplanted and autochthonous melanoma in mice. Cancer Res 2006; 66: 5427-5435.
142. Vidwans SJ, Flaherty KT, Fisher DE, et al., A melanoma molecular disease model. PloS One 2011; 6: e18257.