RAS, FLT3, and C-KIT mutations in immunophenotyped canine leukemias

Experimental Hematology

Volumn 37, Issue 1, 2009, Pages 65-77

  Usher, Suzanne G ^a   Radford, Alan D ^a   Villiers, Elizabeth J ^b   Blackwood, Laura ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; GENOMIC DNA; K RAS PROTEIN; RAS PROTEIN; STEM CELL FACTOR RECEPTOR;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC LEUKEMIA; CONTROLLED STUDY; CYTOLOGY; DOG; FLOW CYTOMETRY; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; IMMUNOPHENOTYPING; LEUKEMIA; LYMPHATIC LEUKEMIA; MISSENSE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE H RAS; ONCOGENE N RAS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROLYMPHOCYTIC LEUKEMIA; SEQUENCE ANALYSIS;

ACUTE DISEASE; ANIMALS; ANTIGENS, CD; CHRONIC DISEASE; DOG DISEASES; DOGS; FMS-LIKE TYROSINE KINASE 3; LEUKEMIA; MUTATION; PROTO-ONCOGENE PROTEINS C-KIT; RAS PROTEINS;

CANIS FAMILIARIS; TETRA;

EID: 57649126338     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2008.09.005     Document Type: Article

References (101)

1. Dorn C.R., Taylor D.O., and Hibbard H.H. Epizootiologic characteristics of canine and feline leukemia and lymphoma. Am J Vet Res 28 (1967) 993-1001
2. Vernau W., and Moore P.F. An immunophenotypic study of canine leukemias and preliminary assessment of clonality by polymerase chain reaction. Vet Immunol Immunopathol 69 (1999) 145-164
3. Villiers E., Baines S., Law A.M., and Mallows V. Identification of acute myeloid leukemia in dogs using flow cytometry with myeloperoxidase, MAC387, and a canine neutrophil-specific antibody. Vet Clin Pathol 35 (2006) 55-71
4. Pruitt K., and Der C.J. Ras and Rho regulation of the cell cycle and oncogenesis. Cancer Lett 171 (2001) 1-10
5. Malumbres M., and Barbacid M. RAS oncogenes: the first 30 years. Nat Rev Cancer 3 (2003) 459-465
6. Bos J.L. ras Oncogenes in human cancer: a review. Cancer Res 49 (1989) 4682-4689
7. Browett P.J., and Norton J.D. Analysis of ras gene mutations and methylation state in human leukemias. Oncogene 4 (1989) 1029-1036
8. Barletta E., Gorini G., Vineis P., et al. Ras gene mutations in patients with acute myeloid leukaemia and exposure to chemical agents. Carcinogenesis 25 (2004) 749-755
9. Miyauchi J., Asada M., Sasaki M., Tsunematsu Y., Kojima S., and Mizutani S. Mutations of the N-ras gene in juvenile chronic myelogenous leukemia. Blood 83 (1994) 2248-2254
10. Hirsch-Ginsberg C., LeMaistre A.C., Kantarjian H., et al. RAS mutations are rare events in Philadelphia chromosome-negative/bcr gene rearrangement-negative chronic myelogenous leukemia, but are prevalent in chronic myelomonocytic leukemia. Blood 76 (1990) 1214-1219
11. Richter A., Murua Escobar H., et al. RAS gene hot-spot mutations in canine neoplasias. J Hered 96 (2005) 764-765
12. Griffey S.M., Kraegel S.A., and Madewell B.R. Rapid detection of K-ras gene mutations in canine lung cancer using single-strand conformational polymorphism analysis. Carcinogenesis 19 (1998) 959-963
13. Griffey S.M., Kraegel S.A., Weller R.E., Watson C.R., and Madewell B.R. K-ras mutations in 239PuO2 canine lung neoplasms. Cancer Lett 132 (1998) 1-5
14. Kraegel S.A., Gumerlock P.H., Dungworth D.L., Oreffo V.I., and Madewell B.R. K-ras activation in non-small cell lung cancer in the dog. Cancer Res 52 (1992) 4724-4727
15. Mayr B., Schaffner G., and Reifinger M. K-ras mutations in canine pancreatic cancers. Vet Rec 153 (2003) 87-89
16. Edwards M.D., Pazzi K.A., Gumerlock P.H., and Madewell B.R. c-N-ras is activated infrequently in canine malignant lymphoma. Toxicol Pathol 21 (1993) 288-291
17. Mayr B., Holzheu M., Schaffner G., and Reifinger M. N-ras mutation in a canine lymphoma: short communication. Acta Vet Hung 51 (2003) 91-94
18. Mayr B., Winkler G., Schaffner G., Reifinger M., and Brem G. N-ras mutation in a feline lymphoma. Low frequency of N-ras mutations in a series of feline, canine and bovine lymphomas. Vet J 163 (2002) 326-328
19. Watzinger F., Mayr B., Gamerith R., Vetter C., and Lion T. Comparative analysis of ras proto-oncogene mutations in selected mammalian tumors. Mol Carcinog 30 (2001) 190-198
20. Gumerlock P.H., Meyers F.J., Foster B.A., Kawakami T.G., and deVere White R.W. Activated c-N-ras in radiation-induced acute nonlymphocytic leukemia: twelfth codon aspartic acid. Radiat Res 117 (1989) 198-206
21. Gilliland D.G., and Griffin J.D. The roles of FLT3 in hematopoiesis and leukemia. Blood 100 (2002) 1532-1542
22. Birg F., Courcoul M., Rosnet O., et al. Expression of the FMS/KIT-like gene FLT3 in human acute leukemias of the myeloid and lymphoid lineages. Blood 80 (1992) 2584-2593
23. Mizuki M., Fenski R., Halfter H., et al. Flt3 mutations from patients with acute myeloid leukemia induce transformation of 32D cells mediated by the Ras and STAT5 pathways. Blood 96 (2000) 3907-3914
24. Spiekermann K., Dirschinger R.J., Schwab R., et al. The protein tyrosine kinase inhibitor SU5614 inhibits FLT3 and induces growth arrest and apoptosis in AML-derived cell lines expressing a constitutively activated FLT3. Blood 101 (2003) 1494-1504
25. Schnittger S., Schoch C., Dugas M., et al. Analysis of FLT3 length mutations in 1003 patients with acute myeloid leukemia: correlation to cytogenetics, FAB subtype, and prognosis in the AMLCG study and usefulness as a marker for the detection of minimal residual disease. Blood 100 (2002) 59-66
26. Nakao M., Janssen J.W., Erz D., Seriu T., and Bartram C.R. Tandem duplication of the FLT3 gene in acute lymphoblastic leukemia: a marker for the monitoring of minimal residual disease. Leukemia 14 (2000) 522-524
27. Xu F., Taki T., Yang H.W., et al. Tandem duplication of the FLT3 gene is found in acute lymphoblastic leukaemia as well as acute myeloid leukaemia but not in myelodysplastic syndrome or juvenile chronic myelogenous leukaemia in children. Br J Haematol 105 (1999) 155-162
28. Stirewalt D.L., Meshinchi S., Kussick S.J., et al. Novel FLT3 point mutations within exon 14 found in patients with acute myeloid leukaemia. Br J Haematol 124 (2004) 481-484
29. Andersson A., Johansson B., Lassen C., Mitelman F., Billstrom R., and Fioretos T. Clinical impact of internal tandem duplications and activating point mutations in FLT3 in acute myeloid leukemia in elderly patients. Eur J Haematol 72 (2004) 307-313
30. Yamamoto Y., Kiyoi H., Nakano Y., et al. Activating mutation of D835 within the activation loop of FLT3 in human hematologic malignancies. Blood 97 (2001) 2434-2439
31. Taketani T., Taki T., Sugita K., et al. FLT3 mutations in the activation loop of tyrosine kinase domain are frequently found in infant ALL with MLL rearrangements and pediatric ALL with hyperdiploidy. Blood 103 (2004) 1085-1088
32. Thiede C., Steudel C., Mohr B., et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood 99 (2002) 4326-4335
33. Syampurnawati M., Tatsumi E., Furuta K., and Hayashi Y. Four novel point mutations in exons 12, 13, and 14 of the FLT3 gene. Leuk Res (2007) 31 877
34. Bianchini M., Ottaviani E., Grafone T., et al. Rapid detection of Flt3 mutations in acute myeloid leukemia patients by denaturing HPLC. Clin Chem 49 (2003) 1642-1650
35. Zavodovskaya R., Liao A.T., Jones C.L., et al. Evaluation of dysregulation of the receptor tyrosine kinases Kit, Flt3, and Met in histiocytic sarcomas of dogs. Am J Vet Res 67 (2006) 633-641
36. Escribano L., Ocqueteau M., Almeida J., Orfao A., and San Miguel J.F. Expression of the c-kit (CD117) molecule in normal and malignant hematopoiesis. Leuk Lymphoma 30 (1998) 459-466
37. Sperling C., Schwartz S., Buchner T., Thiel E., and Ludwig W.D. Expression of the stem cell factor receptor C-KIT (CD117) in acute leukemias. Haematologica 82 (1997) 617-621
38. Kitayama H., Tsujimura T., Matsumura I., et al. Neoplastic transformation of normal hematopoietic cells by constitutively activating mutations of c-kit receptor tyrosine kinase. Blood 88 (1996) 995-1004
39. Beghini A., Ripamonti C.B., Cairoli R., et al. KIT activating mutations: incidence in adult and pediatric acute myeloid leukemia, and identification of an internal tandem duplication. Haematologica 89 (2004) 920-925
40. Shimada A., Taki T., Tabuchi K., et al. KIT mutations, and not FLT3 internal tandem duplication, are strongly associated with a poor prognosis in pediatric acute myeloid leukemia with t(8;21): a study of the Japanese Childhood AML Cooperative Study Group. Blood 107 (2006) 1806-1809
41. Shimada A., Taki T., Kubota C., et al. N822 mutation of KIT gene was frequent in pediatric acute myeloid leukemia patients with t(8;21) in Japan: a study of the Japanese childhood AML cooperative study group. Leukemia 21 (2007) 2218-2219
42. Goemans B.F., Zwaan C.M., Miller M., et al. Mutations in KIT and RAS are frequent events in pediatric core-binding factor acute myeloid leukemia. Leukemia 19 (2005) 1536-1542
43. Care R.S., Valk P.J., Goodeve A.C., et al. Incidence and prognosis of c-KIT and FLT3 mutations in core binding factor (CBF) acute myeloid leukaemias. Br J Haematol 121 (2003) 775-777
44. Lennartsson J., Jelacic T., Linnekin D., and Shivakrupa R. Normal and oncogenic forms of the receptor tyrosine kinase kit. Stem Cells 23 (2005) 16-43
45. London C.A., Galli S.J., Yuuki T., Hu Z.Q., Helfand S.C., and Geissler E.N. Spontaneous canine mast cell tumors express tandem duplications in the proto-oncogene c-kit. Exp Hematol 27 (1999) 689-697
46. Corbacioglu S., Kilic M., Westhoff M.A., Reinhardt D., Fulda S., and Debatin K.M. Newly identified c-KIT receptor tyrosine kinase ITD in childhood AML induces ligand-independent growth and is responsive to a synergistic effect of imatinib and rapamycin. Blood 108 (2006) 3504-3513
47. Wang Y.Y., Zhou G.B., Yin T., et al. AML1-ETO and C-KIT mutation/overexpression in t(8;21) leukemia: implication in stepwise leukemogenesis and response to Gleevec. Proc Natl Acad Sci U S A 102 (2005) 1104-1109
48. Lorenzo F., Nishii K., Monma F., Kuwagata S., Usui E., and Shiku H. Mutational analysis of the KIT gene in myelodysplastic syndrome (MDS) and MDS-derived leukemia. Leuk Res 30 (2006) 1235-1239
49. Kimura A., Nakata Y., Katoh O., and Hyodo H. c-kit Point mutation in patients with myeloproliferative disorders. Leuk Lymphoma 25 (1997) 281-287
50. Cairoli R., Grillo G., Beghini A., Cornacchini G., Larizza L., and Morra E. Chronic myelogenous leukemia with acquired c-kit activating mutation and transient bone marrow mastocytosis. Hematol J 5 (2004) 273-275
51. Webster J.D., Yuzbasiyan-Gurkan V., Miller R.A., Kaneene J.B., and Kiupel M. Cellular proliferation in canine cutaneous mast cell tumors: associations with c-KIT and its role in prognostication. Vet Pathol 44 (2007) 298-308
52. Frost D., Lasota J., and Miettinen M. Gastrointestinal stromal tumors and leiomyomas in the dog: a histopathologic, immunohistochemical, and molecular genetic study of 50 cases. Vet Pathol 40 (2003) 42-54
53. Auewarakul C.U., Lauhakirti D., and Tocharoentanaphol C. Frequency of RAS gene mutation and its cooperative genetic events in Southeast Asian adult acute myeloid leukemia. Eur J Haematol 77 (2006) 51-56
54. Ahuja H.G., Foti A., Bar-Eli M., and Cline M.J. The pattern of mutational involvement of RAS genes in human hematologic malignancies determined by DNA amplification and direct sequencing. Blood 75 (1990) 1684-1690
55. Rovera G., Reichard B.A., Hudson S., et al. Point mutations in both transforming and non-transforming codons of the N-ras proto-oncogene of Ph+ leukemias. Oncogene 4 (1989) 867-872
56. Bowen D.T., Frew M.E., Hills R., et al. RAS mutation in acute myeloid leukemia is associated with distinct cytogenetic subgroups but does not influence outcome in patients younger than 60 years. Blood 106 (2005) 2113-2119
57. Stirewalt D.L., Kopecky K.J., Meshinchi S., et al. FLT3, RAS, and TP53 mutations in elderly patients with acute myeloid leukemia. Blood 97 (2001) 3589-3595
58. Bacher U., Haferlach T., Schoch C., Kern W., and Schnittger S. Implications of NRAS mutations in AML: a study of 2502 patients. Blood 107 (2006) 3847-3853
59. Nakamura H., Inokuchi K., Yamaguchi H., and Dan K. Abnormalities of p51, p53, FLT3 and N-ras genes and their prognostic value in relapsed acute myeloid leukemia. J Nippon Med Sch 71 (2004) 270-278
60. Bar-Eli M., Ahuja H., Foti A., and Cline M.J. N-RAS mutations in T-cell acute lymphocytic leukaemia: Analysis by direct sequencing detects a novel mutation. Br J Haematol 72 (1989) 36-39
61. Cogswell P.C., Morgan R., Dunn M., et al. Mutations of the ras protooncogenes in chronic myelogenous leukemia: a high frequency of ras mutations in bcr/abl rearrangement-negative chronic myelogenous leukemia. Blood 74 (1989) 2629-2633
62. Neubauer A., Dodge R.K., George S.L., et al. Prognostic importance of mutations in the ras proto-oncogenes in de novo acute myeloid leukemia. Blood 83 (1994) 1603-1611
63. Browett P.J., Yaxley J.C., and Norton J.D. Activation of Harvey ras oncogene by mutation at codon 12 is very rare in hemopoietic malignancies. Leukemia 3 (1989) 86-88
64. Imamura N., Kuramoto A., Ishihara H., and Shimizu S. Detection of high incidence of H-RAS oncogene point mutations in acute myelogenous leukemia. Am J Hematol 43 (1993) 151-153
65. Watzinger F., Mayr B., Haring E., and Lion T. High sequence similarity within ras exons 1 and 2 in different mammalian species and phylogenetic divergence of the ras gene family. Mamm Genome 9 (1998) 214-219
66. Boissel N., Leroy H., Brethon B., et al. Incidence and prognostic impact of c-Kit, FLT3, and Ras gene mutations in core binding factor acute myeloid leukemia (CBF-AML). Leukemia 20 (2006) 965-970
67. Yamamoto T., Isomura M., Xu Y., et al. PTPN11, RAS and FLT3 mutations in childhood acute lymphoblastic leukemia. Leuk Res 30 (2006) 1085-1089
68. Abu-Duhier F.M., Goodeve A.C., Wilson G.A., Care R.S., Peake I.R., and Reilly J.T. Identification of novel FLT-3 Asp835 mutations in adult acute myeloid leukaemia. Br J Haematol 113 (2001) 983-988
69. Miettinen M., and Lasota J. Gastrointestinal stromal tumors (GISTs): definition, occurrence, pathology, differential diagnosis and molecular genetics. Pol J Pathol 54 (2003) 3-24
70. Ma Y., Longley B.J., Wang X., Blount J.L., Langley K., and Caughey G.H. Clustering of activating mutations in c-KIT's juxtamembrane coding region in canine mast cell neoplasms. J Invest Dermatol 112 (1999) 165-170
71. Liao A.T., Chien M.B., Shenoy N., et al. Inhibition of constitutively active forms of mutant kit by multitargeted indolinone tyrosine kinase inhibitors. Blood 100 (2002) 585-593
72. Gotlib J., Berube C., Growney J.D., et al. Activity of the tyrosine kinase inhibitor PKC412 in a patient with mast cell leukemia with the D816V KIT mutation. Blood 106 (2005) 2865-2870
73. Hongyo T., Li T., Syaifudin M., et al. Specific c-kit mutations in sinonasal natural killer/T-cell lymphoma in China and Japan. Cancer Res 60 (2000) 2345-2347
74. Riva F., Brizzola S., Stefanello D., Crema S., and Turin L. A study of mutations in the c-kit gene of 32 dogs with mastocytoma. J Vet Diagn Invest 17 (2005) 385-388
75. Zemke D., Yamini B., and Yuzbasiyan-Gurkan V. Mutations in the juxtamembrane domain of c-KIT are associated with higher grade mast cell tumors in dogs. Vet Pathol 39 (2002) 529-535
76. De Melo M.B., Lorand-Metze I., Lima C.S., Saad S.T., and Costa F.F. N-ras gene point mutations in Brazilian acute myelogenous leukemia patients correlate with a poor prognosis. Leuk Lymphoma 24 (1997) 309-317
77. Abu-Duhier F.M., Goodeve A.C., Wilson G.A., et al. FLT3 internal tandem duplication mutations in adult acute myeloid leukaemia define a high-risk group. Br J Haematol 111 (2000) 190-195
78. Pui C.H., and Jeha S. New therapeutic strategies for the treatment of acute lymphoblastic leukaemia. Nat Rev Drug Discov 6 (2007) 149-165
79. Kantarjian H.M., and Talpaz M. Imatinib mesylate: clinical results in Philadelphia chromosome-positive leukemias. Semin Oncol 28 (2001) 9-18
80. Piccaluga P.P., Paolini S., and Martinelli G. Tyrosine kinase inhibitors for the treatment of Philadelphia chromosome-positive adult acute lymphoblastic leukemia. Cancer 110 (2007) 1178-1186
81. Cairoli R., Beghini A., Morello E., et al. Imatinib mesylate in the treatment of Core Binding Factor leukemias with KIT mutations. A report of three cases. Leuk Res 29 (2005) 397-400
82. London C.A., Hannah A.L., Zadovoskaya R., et al. Phase I dose-escalating study of SU11654, a small molecule receptor tyrosine kinase inhibitor, in dogs with spontaneous malignancies. Clin Cancer Res 9 (2003) 2755-2768
83. Dobson J., Villiers E., and Morris J. Diagnosis and management of leukaemia in dogs and cats. In Pract 28 (2006) 22-31
84. Lee Y.Y., Kim W.S., Bang Y.J., et al. Analysis of mutations of neurofibromatosis type 1 gene and N-ras gene in acute myelogenous leukemia. Stem Cells 13 (1995) 556-563
85. Loriaux M.M., Levine R.L., Tyner J.W., et al. High-throughput sequence analysis of the tyrosine kinome in acute myeloid leukemia. Blood 111 (2008) 4788-4796
86. Lee J.W., Kim Y.G., Soung Y.H., et al. The JAK2 V617F mutation in de novo acute myelogenous leukemias. Oncogene 25 (2006) 1434-1436
87. Falini B., Mecucci C., Tiacci E., et al. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N Engl J Med 352 (2005) 254-266
88. Tartaglia M., Niemeyer C.M., Fragale A., et al. Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat Genet 34 (2003) 148-150
89. Christiansen D.H., Andersen M.K., Desta F., and Pedersen-Bjergaard J. Mutations of genes in the receptor tyrosine kinase (RTK)/RAS-BRAF signal transduction pathway in therapy-related myelodysplasia and acute myeloid leukemia. Leukemia 19 (2005) 2232-2240
90. Thorn J., Molloy P., and Iland H. SSCP detection of N-ras promoter mutations in AML patients. Exp Hematol 23 (1995) 1098-1103
91. Pabst T., Mueller B.U., Zhang P., et al. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-alpha (C/EBPalpha), in acute myeloid leukemia. Nat Genet 27 (2001) 263-270
92. Roumier C., Eclache V., Imbert M., et al. M0 AML, clinical and biologic features of the disease, including AML1 gene mutations: a report of 59 cases by the Groupe Francais d'Hematologie Cellulaire (GFHC) and the Groupe Francais de Cytogenetique Hematologique (GFCH). Blood 101 (2003) 1277-1283
93. Forbes L.V., Gale R.E., Pizzey A., Pouwels K., Nathwani A., and Linch D.C. An activating mutation in the transmembrane domain of the granulocyte colony-stimulating factor receptor in patients with acute myeloid leukemia. Oncogene 21 (2002) 5981-5989
94. Breen M., Bullerdiek J., and Langford C.F. The DAPI banded karyotype of the domestic dog (Canis familiaris) generated using chromosome-specific paint probes. Chromosome Res 7 (1999) 401-406
95. Horsting N., Wohlsein P., Reimann N., Bartnitzke S., Bullerdiek J., and Nolte I. Cytogenetic analysis of three oropharyngeal malignant melanomas in dogs. Res Vet Sci 67 (1999) 149-151
96. Reimann N., Bartnitzke S., Bullerdiek J., Mischke R., and Nolte I. Trisomy 1 in a canine acute leukemia indicating the pathogenetic importance of polysomy 1 in leukemias of the dog. Cancer Genet Cytogenet 101 (1998) 49-52
97. Grindem C.B., and Buoen L.C. Cytogenetic analysis of leukaemic cells in the dog. A report of 10 cases and a review of the literature. J Comp Pathol 96 (1986) 623-635
98. Nolte M., Werner M., Nolte I., and Georgii A. Different cytogenetic findings in two clinically similar leukaemic dogs. J Comp Pathol 108 (1993) 337-342
99. Nolte I., Reimann N., Bullerdiek J., Bartnitzke S., Mischke R., and Nolte M. Importance of cytogenetic investigations in canine leukemias]. Tierarztl Prax 25 (1997) 393-397
100. Darre R., Queinnec G., Guelfi J.-F., Florio R., Colombies P., and Berland H.M. Constance d'un chromosome particulier dans un cas de leukemie chez le chien. Ann Recherches Vet 1 (1970) 93-106
101. Breen M., and Modiano J.F. Evolutionarily conserved cytogenetic changes in hematological malignancies of dogs and humans: man and his best friend share more than companionship. Chromosome Res 16 (2008) 145-154