Receptor tyrosine kinase inhibitors: Molecularly targeted drugs for veterinary cancer therapy

Veterinary and Comparative Oncology

Volumn 10, Issue 3, 2012, Pages 163-173

  Bavcar, S ^a   Argyle, D J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cancer; Receptor tyrosine kinase inhibitors; Targeted therapy; Tyrosine kinases

Indexed keywords

ANTINEOPLASTIC AGENT; INDOLE DERIVATIVE; MASITINIB; PROTEIN TYROSINE KINASE; PYRROLE DERIVATIVE; THIAZOLE DERIVATIVE; TOCERANIB;

ANIMAL; ANIMAL DISEASE; ARTICLE; DRUG ANTAGONISM; DRUG COMBINATION; DRUG EFFECT; ENZYMOLOGY; HUMAN; NEOPLASM; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG THERAPY, COMBINATION; HUMANS; INDOLES; NEOPLASMS; PYRROLES; RECEPTOR PROTEIN-TYROSINE KINASES; THIAZOLES;

EID: 84864861624     PISSN: 14765810     EISSN: 14765829     Source Type: Journal    
DOI: 10.1111/j.1476-5829.2012.00342.x     Document Type: Article

References (76)

1. Lemmon MA and Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010; 141: 1117-1134.
2. London CA. Signal transduction and cancer. In: Small Animal Clinical Oncology. Philadelphia, W.B. Saunders Co, 2007: 242-251.
3. Robinson DR, Wu YM and Lin SF. The protein tyrosine kinase family of the human genome. Oncogene 2000; 19: 5548-5557.
4. Manning G, Whyte DB, Martinez R, Hunter T and Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298: 1912-1934.
5. Krupa A and Srinivasan N. The repertoire of protein kinases encoded in the draft version of the human genome: atypical variations and uncommon domain combinations. Genome Biology 2002; 3: research0066.1-research0066.14.
6. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000; 103: 211-225.
7. London CA. Kinase inhibitors in cancer therapy. Veterinary and Comparative Oncology 2004; 2: 177-193.
8. Shchemelinin I, Sefc L and Necas E. Protein kinases, their function and implication in cancer and other diseases. Folia Biologica (Praha) 2006; 52: 81-100.
9. Ma PC, Maulik G, Christensen J and Salgia R. c-Met: structure, functions and potential for therapeutic inhibition. Cancer and Metastasis Reviews 2003; 22: 309-325.
10. Laskin JJ and Sandler AB. Epidermal growth factor receptor: a promising target in solid tumours. Cancer Treatment Reviews 2004; 30: 1-17.
11. Fletcher JA. Role of KIT and platelet-derived growth factor receptors as oncoproteins. Seminars in Oncology 2004; 31: 4-11.
12. Neubauer A, Burchert A, Maiwald C, Gruss HJ, Serke S, Huhn D, Wittig B and Liu E. Recent progress on the role of Axl, a receptor tyrosine kinase, in malignant transformation of myeloid leukemias. Leukemia and Lymphoma 1997; 25: 91-96.
13. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR and Futreal PA. Mutations of the BRAF gene in human cancer. Nature 2002; 417: 949-954.
14. Kumar R, Angelini S, Snellman E and Hemminki K. BRAF mutations are common somatic events in melanocytic nevi. Journal of Investigative Deramatology 2004; 122: 342-348.
15. Mercer KE and Pritchard CA. Raf proteins and cancer: B-Raf is identified as a mutational target. Bichimica et Biophysica Acta 2003; 1653: 25-40.
16. Madhusudan S and Ganesan TS. Tyrosine kinase inhibitors in cancer therapy. Clinical Biochemistry 2004; 37: 618-635.
17. Alvarez RH, Kantarjian H and Cortes JE. The biology of chronic myelogenous leukemia: implications for imatinib therapy. Seminars in Hematology 2007; 44: 4-14.
18. Moen MD, McKeage K, Plosker GL and Siddiqui MA. Imatinib: a review of its use in chronic myeloid leukaemia. Drugs 2007; 67: 299-320.
19. Galli SJ, Zsebo KM and Geissler EN. The kit ligand, stem cell factor. Advances in Immunology 1994; 55: 1-95.
20. Gotlib J. KIT mutations in mastocytosis and their potential as therapeutic targets. Immunology and Allergy Clinics of North America 2006; 26: 575-592.
21. Advani AS. C-kit as a target in the treatment of acute myelogenous leukemia. Current Hematology Reports 2005; 4: 51-58.
22. Lasota J and Miettinen M. KIT and PDGFRA mutations in gastrointestinal stromal tumors (GISTs). Seminars in Diagnostic Pathology 2006; 23: 91-102.
23. Siddiqui MA and Scott LJ. Imatinib: a review of its use in the management of gastrointestinal stromal tumours. Drugs 2007; 67: 805-820.
24. Thurston G and Gale NW. Vascular endothelial growth factor and other signaling pathways in developmental and pathologic angiogenesis. International Journal of Hematology 2004; 80: 7-20.
25. Eskens FA. Angiogenesis inhibitors in clinical development; where are we now and where are we going? British Journal of Cancer 2004; 90: 1-7.
26. Cherrington JM, Strawn LM and Shawver LK. New paradigms for the treatment of cancer: the role of anti-angiogenesis agents. Advances in Cancer Research 2000; 79: 1-38.
27. McCarty MF, Liu W, Fan F, Parikh A, Reimuth N, Stoeltzing O and Ellis LM. Promises and pitfalls of anti-angiogenic therapy in clinical trials. Trends in Molecular Medicine 2003; 9: 53-58.
28. Ashman LK. The biology of stem cell factor and its receptor C-kit. The International Journal of Biochemistry & Cell Biology 1999; 31: 1037-1051.
29. Galli SJ and Kitamura Y. Genetically mast cell deficient w/wv and sl/sld mice. The American Journal of Pathology 1987; 127: 191-198.
30. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, Atkins HL, Hsu RY, Birkett NC, Okino KH and Murdock DC. Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 1990; 633: 213-224.
31. Zsebo KM, Wypych J, McNiece IK, Lu HS, Smith KA, Karkare SB, Sachdev RK, Yuschenkoff VN, Birkett NC and Williams LR. Identification, purification, and biological characterization of hematopoeitic stem cell factor from buffalo rat liver-conditioned medium. Cell 1990; 63: 195-201.
32. Tsai M, Takeishi T, Thompson H, Langley KE, Zsebo KM, Metcalfe DD, Geissler EN and Galli SJ. Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor. Proceedings of the National Academy of Sciences of the United States of America 1991; 88: 6382-6386.
33. Taylor ML and Metcalfe DD. Kit signal transduction. Hematology/Oncology Clinics of North America 2000; 14: 517-535.
34. Zemke D, Yamini B and Yuzbasiyan-Gurkan V. Characterization of an undifferentiated malignancy as a mast cell tumor using mutation analysis in the proto-oncogene c-KIT. Journal of Veterinary Diagnostic Investigation 2001; 13: 341-345.
35. London CA, Galli SJ, Yuuki T, Hu ZQ, Helfand SC and Geissler EN. Spontaneous canine mast cell tumors express tandem duplications in the proto-oncogene c-kit. Experimental Hematology 1999; 27: 689-697.
36. Ma Y, Longley BJ, Wang X, Blount JL, Langley K and Caughey GH. Clustering of activating mutations in c-KIT's juxtamembrane coding region of canine mast cell neoplasms. The Journal of Investigative Dermatology 1999; 112: 165-170.
37. Downing S, Chien MB, Kass PH, Moore PE and London CA. Prevalence and importance of internal tandem duplications in exons 11 and 12 of c-kit in mast cell tumors of dogs. American Journal of Veterinary Research 2002; 63: 1718-1723.
38. Zemke D, Yamini B and Yuzbasiyan-Gurkan V. Mutation in the juxtamembrane domain of c-KIT are associated with higher grade mast cell tumors in dogs. Veterinary Pathology 2002; 39: 529-535.
39. Demetri GD. Differential properties of current tyrosine kinase inhibitors in gastrointestinal stromal tumors. Seminars in Oncology 2011; 38: 10-19.
40. 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. Veterinary Pathology 2003; 40: 42-54.
41. Zwick E, Bange J and Ullrich A. Receptor tyrosine kinases as targets for anticancer drugs. Trends in Molecular Medicine 2002; 8.
42. Levitzki A. Protein tyrosine kinase inhibitors as novel therapeutic agents. Pharmacology and Therapeutics 1999; 82: 231-239.
43. Ogilvie GK, Hensel P, Kitchell BE, Dubreuil P and Ahn A. Masitinib - a targeted therapy with applications in veterinary oncology and inflammatory diseases. CAB Reviews 2011: 021.
44. Pegram MD, Weber BL, Baselga JM, Tripathy D, Baly D, Baughman SA, Twaddell T, Glaspy JA and Slamon DJ. Phase II study of receptor-enhanced chemosensitivity using recombinant humanized anti-p185HER2/neu monoclonal antibody plus cisplatin in patients with HER2/neu-overexpressing metastatic breast cancer refractory to chemotherapy treatment. Journal of Clinical Oncology 1998; 16: 2659-2671.
45. Bange J, Zwick E and Ullrich A. Molecular targets for breast cancer therapy and prevention. Nature Medicine 2001; 7: 548-552.
46. Harris M. Monoclonal antibodies as therapeutic agents for cancer. The Lancet Oncology 2004; 5: 292-302.
47. Brand TM, Iida M and Wheeler DL. Molecular mechanism of resistance to the EGFR monoclonal antibody cetuximab. Cancer Biology & Therapy 2011; 11: 777-792.
48. Zhang J, Yang PL and Gray NS. Targeting cancer with small molecule kinase inhibitors. Nature Reviews Cancer 2009; 9: 28-39.
49. Druker BJ, Guilhot F, O'Brien SG, Gathmann I, Kantarjian H, Gattermann N, Deininger MW, Silver RT, Goldman JM, Stone RM, Cervantes F, Hochhaus A, Powell BL, Gabrilove JL, Rousselot P, Reiffers J, Cornelissen JJ, Hughes T, Agis H, Fischer T, Verhoef G, Shepherd J, Saglio G, Gratwohl A, Nielsen JL, Radich JP, Simonsson B, Taylor K, Baccarani M, So C, Letvak L, Larson RA and IRIS Investigators. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. The New England Journal of Medicine 2006; 355: 2408-2417.
50. Miettinen M, Sarlomo - Rikala M and Lasota J. Gastrointestinal stromal tumours: recent advances in understanding of their biology. Human Pathology 1999; 30: 1213-1220.
51. Miettinen M, Sarlomo-Rikala M and Lasota J. Gastrointestinal stromal tumours. Annales Chirurgiae et Gynaecologiae 1998; 87: 278-281.
52. Bang YJ. The potential for crizotinib in non-small cell lung cancer: a perspective review. Therapeutic Advances in Medical Oncology 2011; 3: 279-291.
53. Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, Engelman JA, Shapiro GI, Costa DB, Ou SH, Butaney M, Salgia R, Maki RG, Varella-Garcia M, Doebele RC, Bang YJ, Kulig K, Selaru P, Tang Y, Wilner KD, Kwak EL, Clark JW, Iafrate AJ and Camidge DR. Effect of crizotinib on overall survival in patients with advancer non-small cell cancer harbouring ALK gene rearrangement: a retrospective analysis. The Lancet Oncology 2011; 12: 1004-1012.
54. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, O'Day SJ, Sosman JA, Kirkwood JM, Eggermont AM, Dreno B, Nolop K, Li J, Nelson B, Hou J, Lee RJ, Flaherty KT, McArthur GA and BRIM-3 Study Group. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. The New England Journal of Medicine 2011; 364: 2507-2516.
55. Markman B, Dienstmann R and Tabernero J. Targeting the PI3K/Akt/mTOR pathway - beyond rapalogs. Oncotarget 2010; 1: 530-543.
56. Vilar E, Perez-Garcia J and Tabarnero J. Pushing the envelope in the mTOR pathway: the second generation of inhibitors. Molecular Cancer Therapeutics 2011; 10: 395-403.
57. Papaetis GS and Syrigos KN. Sunitinib: a multitargeted receptor tyrosine kinase inhibitor in the era of molecular cancer therapies. BioDrugs 2009; 23: 377-389.
58. London CA, Malpas PB, Wood-Follis SL, Boucher JF, Rusk AW, Rosenberg MP, Henry CJ, Mitchener KL, Klein MK, Hintermeister JG, Bergman PJ, Couto GC, Mauldin GN and Michels GM. Multi-center, placebo-controlled, double-blind, randomized study of oral toceranib phosphate (SU11654), a receptor tyrosine kinase inhibitor, for the treatment of dogs with recurrent (either local or distant) mast cell tumor following surgical excision. Clinical Cancer Research 2009; 15: 3856-3865.
59. Hahn KA, Ogilvie G, Rusk T, Devauchelle P, Leblanc A, Legendre A, Powers B, Leventhal PS, Kinet JP, Palmerini F, Dubreuil P, Moussy A and Hermine O. Masitinib is safe and effective for the treatment of canine mast cell tumors. Journal of Veterinary Internal Medicine 2008; 22: 1301-1309.
60. Mitchell BL, Thamm DH and Biller BJ. Clinical and immunomodulatory effects of toceranib combined with low-dose cyclophosphamide in dogs with cancer. Journal of Veterinary Internal Medicine 2012; 26: 355-362.
61. Liao AT, Chien MB, Shenoy N, Mendel DB, McMahon G, Cherrington JM and London CA. Inhibition of constitutively active forms of mutant kit by multitargeted indolinone tyrosine kinase inhibitors. Blood 2002; 100: 585-593.
62. London CA, Hannah AL, Zadovoskaya R, Chien MB, Kollias-Baker C, Rosenberg M, Downing S, Post G, Boucher J, Shenoy N, Mendel DB, McMahon G and Cherrington JM. Phase I dose-escalating study of SU11654, a small molecule receptor tyrosine kinase inhibitor, in dogs with spontaneous malignancies. Clinical Cancer Research 2003; 9: 2755-2768.
63. London CA, Mathie T, Stingle N, Clifford C, Haney S, Klein MK, Beaver L, Vickery K, Vail DM, Hershey B, Ettinger S, Vaughan A, Alvarez F, Hillman L, Kiselow M, Thamm D, Higginbotham ML, Gauthier M, Krick E, Phillips B, Ladue T, Jones P, Bryan J, Gill V, Novasad A, Fulton L, Carreras J, McNeill C, Henry C and Gillings S. Preliminary evidence for biologic activity of toceranib phosphate (Palladia) in solid tumors. Veterinary and Comparative Oncology 2011; doi: 10.1111/j.1476-5829.2011.00275.x.
64. Ozao-Choy J, Ma G, Kao J, Wang GX, Meseck M, Sung M, Schwartz M, Divino CM, Pan PY and Chen SH . The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Research 2009; 69: 2514-2522.
65. Dubreuil P, Letard S, Ciufolini M, Gros L, Humbert M, Castéran N, Borge L, Hajem B, Lermet A, Sippl W, Voisset E, Arock M, Auclair C, Leventhal PS, Mansfield CD, Moussy A and Hermine O. Masitinib (AB1010), a potent and selective tyrosine kinase inhibitor targeting KIT. PLoS One 2009; 4: e7258.
66. Ogilvie G and Ahn A. Masitinib - the efficacy of targeted therapy in veterinary medicine. Veterinary Cancer Society Newsletter Summer 2010; 34: 6-11.
67. London CA. Tyrosine kinase inhibitors in veterinary medicine - topical review. Topics in Companion Animal Medicine 2009; 24: 106-112.
68. Thamm DH, Rose B, Kow K, Humbert M, Mansfield CD, Moussy A, Hermine O and Dubreuil P. Masitinib as a chemosensitizer of canine tumor cell lines: a proof of concept study. The Veterinary Journal 2012; 191: 131-134.
69. Robat C, London CA, Bunting L, McCartan L, Stingle N, Selting K, Kurzman I and Vail DM. Safety evaluation of combination vinblastine and toceranib phosphate (Palladia®) in dogs: a phase I dose-finding study. Journal of Veterinary Internal Medicine 2011; 25: 745-746.
70. Carlsten KS, London CA, Haney S, Burnett R, Avery AC and Thamm DH. Multicenter prospective trial of hypofractionated radiation treatment, toceranib, and prednisone for measurable canine mast cell tumors. Journal of Veterinary Internal Medicine 2012; 26: 135-141.
71. Robat C, London C, Bunting L, McCartan L, Stingle N, Selting K, Kurzman I and Vail DM. Safety evaluation of combination vinblastine and toceranib phosphate (Palladia) in dogs: a phase I dose-finding study. Veterinary and Comparative Oncology 2012; 10: 174-183.
72. Chon E, McCartan L, Kubicek LN and Vail DM. Safety evaluation of combination toceranib phosphate (Palladia) and piroxicam in tumour-bearing dogs (excluding mast cell tumours): a phase I dose-finding study. Veterinary and Comparative Oncology 2012; 10: 184-193.
73. de Vos J, Ramos Vega S, Noorman E and de Vos P. Primary frontal sinus squamous cell carcinoma in three dogs treated with piroxicam combined with carboplatin or toceranib. Veterinary and Comparative Oncology 2012; 10: 206-213.
74. Lyles SE, Milner RJ, Kow K and Salute ME. In vitro effects of the tyrosine kinase inhibitor, masitinib mesylate, on canine hemangiosarcoma cell lines. Veterinary and Comparative Oncology 2012; 10: 223-235.
75. London C, Mathie T, Stingle N, Clifford C, Haney S, Klein MK, Beaver L, Vickery K, Vail DM, Hershey B, Ettinger S, Vaughan A, Alvarez F, Hillman L, Kiselow M, Thamm D, Higginbotham ML, Gauthier M, Krick E, Phillips B, Ladue T, Jones P, Bryan J, Gill V, Novasad A, Fulton L, Carreras J, McNeill C, Henry C and Gillings S. Preliminary evidence for biologic activity of toceranib phosphate (Palladia) in solid tumours. Veterinary and Comparative Oncology 2012; 10: 194-205.
76. Blackwood LB, Murphy S, Burraco P, De Vos JP, De Vos J, De Fornel-Thibaud P, Hirschberger J, Kessler M, Savary-Bataille K, Pastor J, Ponce F and Argyle DJ. European consensus document on mast tumours in dogs and cats. Veterinary and Comparative Oncology 2012; 10: 236.