Molecular basis for treatment of gastrointestinal stromal tumours

European Journal of Cancer, Supplement

Volumn 4, Issue 3, 2006, Pages 10-18

  Heinrich, Michael C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

activating mutations; clinical response resistance; Gastrointestinal stromal tumour; imatinib; KIT; management strategies; molecular mechanisms; PDGFR .

Indexed keywords

ABELSON KINASE; BCR ABL PROTEIN; FLUORODEOXYGLUCOSE F 18; IMATINIB; PHOSPHOTRANSFERASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; SUNITINIB;

ARTICLE; CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER PATIENT; CANCER RECURRENCE; CANCER RESISTANCE; CANCER SURGERY; CANCER SURVIVAL; CARCINOGENESIS; CLINICAL TRIAL; CORRELATION ANALYSIS; DISEASE COURSE; DISEASE FREE SURVIVAL; DISEASE SEVERITY; DOSE CALCULATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG RESEARCH; DRUG SENSITIVITY; DRUG TARGETING; DRUG TREATMENT FAILURE; ENZYME ACTIVITY; ENZYME INHIBITION; EXON; GASTROINTESTINAL STROMAL TUMOR; GASTROINTESTINAL TRACT; GENE MUTATION; GENETIC ANALYSIS; HUMAN; IMMUNOHISTOCHEMISTRY; MAXIMUM TOLERATED DOSE; METASTASIS; MOLECULAR CLONING; MOLECULAR DYNAMICS; PATIENT CARE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RARE DISEASE; SURVIVAL TIME; TREATMENT OUTCOME; TREATMENT RESPONSE;

EID: 33646377662     PISSN: 13596349     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1359-6349(06)80469-6     Document Type: Article

References (95)

1. Kindblom L.G., Remotti H.E., Aldenborg F., and Meis-Kindblom J.M. Gastrointestinal pacemaker cell tumor (GIPACT): gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am J Pathol 152 5 (1998) 1259-1269
2. Chen L.L., Sabripour M., Andtbacka R.H., et al. Imatinib resistance in gastrointestinal stromal tumors. Curr Oncol Rep 7 4 (2005) 293-299
3. Miettinen M., Virolainen M., and Maarit Sarlomo R. Gastrointestinal stromal tumors - value of CD34 antigen in their identification and separation from true leiomyomas and schwannomas. Am J Surg Pathol 19 2 (1995) 207-216
4. Bucher P., Villiger P., Egger J.F., Buhler L.H., and Morel P. Management of gastrointestinal stromal tumors: from diagnosis to treatment. Swiss Med Wkly 134 11-12 (2004) 145-153
5. discussion 1620, 1623, 1626 passim. Eisenberg B.L. Imatinib mesylate: a molecularly targeted therapy for gastrointestinal stromal tumors. Oncology (Williston Park) 17 11 (2003) 1615-1620
6. Miettinen M., and Lasota J. Gastrointestinal stromal tumors - definition, clinical, histological, immunohistochemical, and molecular genetic features and differential diagnosis. Virchows Arch 438 1 (2001) 1-12
7. Miettinen M., Monihan J.M., Sarlomo-Rikala M., et al. Gastrointestinal stromal tumors/smooth muscle tumors (GISTs) primary in the omentum and mesentery: clinicopathologic and immunohistochemical study of 26 cases. Am J Surg Pathol 23 9 (1999) 1109-1118
8. Nakama A., Hirota S., Okazaki T., et al. Disturbed pyloric motility in Ws/Ws mutant rats due to deficiency of c-kit-expressing interstitial cells of Cajal. Pathol Int 48 11 (1998) 843-849
9. Huizinga J.D., Thuneberg L., Kluppel M., Malysz J., Mikkelsen H.B., and Bernstein A. W/kit gene required for interstitial cells of Caj al and for intestinal pacemaker activity. Nature 373 6512 (1995) 347-349
10. Isozaki K., Hirota S., Nakama A., et al. Disturbed intestinal movement, bile reflux to the stomach, and deficiency of c-kit-expressing cells in Ws/Ws mutant rats. Gastroenterology 109 2 (1995) 456-464
11. Kluppel M., Huizinga J.D., Malysz J., and Bernstein A. Developmental origin and Kit-dependent development of the interstitial cells of cajal in the mammalian small intestine. Dev Dyn 211 1 (1998) 60-71
12. Torihashi S., Horisawa M., and Watanabe Y. c-Kit immunoreactive interstitial cells in the human gastrointestinal tract. J Auton Nerv Syst 75 1 (1999) 38-50
13. Heinrich M.C., Rubin B.P., Longley B.J., and Fletcher J.A. Biology and genetic aspects of gastrointestinal stromal tumors: KIT activation and cytogenetic alterations. Hum Pathol 33 5 (2002) 484-495
14. Hirota S., Isozaki K., Moriyama Y., et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279 5350 (1998) 577-580
15. Rubin B.P., Singer S., Tsao C., et al. KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res 61 22 (2001) 8118-8121
16. Heinrich M.C., Corless C.L., Demetri G.D., et al. Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J Clin Oncol 21 23 (2003) 4342-4349
17. Miettinen M., Sobin L.H., and Lasota J. Gastrointestinal stromal tumors of the stomach: a clinicopathologic, immunohistochemical, and molecular genetic study of 1765 cases with long-term follow-up. Am J Surg Pathol 29 1 (2005) 52-68
18. Corless C.L., Fletcher J.A., and Heinrich M.C. Biology of gastrointestinal stromal tumors. J Clin Oncol 22 18 (2004) 3813-3825
19. Corless C.L., McGreevey L., Haley A., Town A., and Heinrich M.C. KIT mutations are common in incidental gastrointestinal stromal tumors one centimeter or less in size. Am J Pathol 160 5 (2002) 1567-1572
20. Nishida T., Hirota S., Taniguchi M., et al. Familial gastrointestinal stromal tumours with germline mutation of the KIT gene. Nat Genet 19 4 (1998) 323-324
21. Beghini A., Tibiletti M.G., Roversi G., et al. Germline mutation in the juxtamembrane domain of the kit gene in a family with gastrointestinal stromal tumors and urticaria pigmentosa. Cancer 92 3 (2001) 657-662
22. Maeyama H., Hidaka E., Ota H., et al. Familial gastrointestinal stromal tumor with hyperpigmentation: association with a germline mutation of the c-kit gene. Gastroenterology 120 1 (2001) 210-215
23. Hirota S., Isozaki K., Nishida T., and Kitamura Y. Effects ofloss-of-function and gain-of-function mutations of c-kit on the gastrointestinal tract. J Gastroenterol 35 Suppl 12 (2000) 75-79
24. Isozaki K., Terris B., Belghiti J., Schiffmann S., Hirota S., and Vanderwinden J.M. Germline-activating mutation in the kinase domain of KIT gene in familial gastrointestinal stromal tumors. Am J Pathol 157 5 (2000) 1581-1585
25. Hirota S., Nishida T., Isozaki K., et al. Familial gastrointestinal stromal tumors associated with dysphagia and novel type germline mutation of KIT gene. Gastroenterology 122 5 (2002) 1493-1499
26. Rubin B.P., Antonescu C.R., Scott-Browne J.P., et al. A knock-in mouse model of gastrointestinal stromal tumor harboring Kit K641E. Cancer Res 65 15 (2005) 6631-6639
27. Sommer G., Agosti V., Ehlers I., et al. Gastrointestinal stromal tumors in a mouse model by targeted mutation of the Kit receptor tyrosine kinase. Proc Natl Acad Sci USA 100 (2003) 6706-6711 11
28. Heinrich M.C., Corless C.L., Duensing A., et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299 5607 (2003) 708-710
29. Hirota S., Ohashi A., Nishida T., et al. Gain-of-function mutations of platelet-derived growth factor receptor alpha gene in gastrointestinal stromal tumors. Gastroenterology 125 3 (2003) 660-667
30. Lux M.L., Rubin B.P., Biase T.L., et al. KIT extracellular and kinase domain mutations in gastrointestinal stromal tumors. Am J Pathol 156 3 (2000) 791-795
31. Tarn C., Merkel E., Canutescu A.A., et al. Analysis of KIT mutations in sporadic and familial gastrointestinal stromal tumors: therapeutic implications through protein modeling. Clin Cancer Res 11 10 (2005) 3668-3677
32. Eisenberg B.L., and Judson I. Surgery and imatinib in the management of GIST: emerging approaches to adjuvant and neoadjuvant therapy. Ann Surg Oncol 11 5 (2004) 465-475
33. discussion 207. Heinrich M.C., and Corless C.L. Gastric GI stromal tumors (GISTs): the role of surgery in the era of targeted therapy. J Surg Oncol 90 3 (2005) 195-207
34. Ng E.H., Pollock R.E., Munsell M.F., Atkinson E.N., and Romsdahl M.M. Prognostic factors influencing survival in gastrointestinal leiomyosarcomas. Implications for surgical management and staging. Ann Surg 215 1 (1992) 68-77
35. DeMatteo R.P., Lewis J.J., Leung D., Mudan S.S., Woodruff J.M., and Brennan M.E. Two hundred gastrointestinal stromal tumors: recurrence patterns and prognostic factors for survival. Ann Surg 231 1 (2000) 51-58
36. DeMatteo R.P., Heinrich M.C., El-Rifai W.M., and Demetri G. Clinical management of gastrointestinal stromal tumors: before and after STI-571. Hum Pathol 33 5 (2002) 466-477
37. D'Amato G., Steinert D.M., McAuliffe J.C., and Trent J.C. Update on the biology and therapy of gastrointestinal stromal tumors. Cancer Control 12 1 (2005) 44-56
38. Buchdunger E., Cioffi C.L., Law N., et al. Ab1 protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and platelet-derived growth factor receptors. J Pharmacol Exp Ther 295 1 (2000) 139-145
39. Okuda K., Weisberg E., Gilliland D.G., and Griffin J.D. ARG tyrosine kinase activity is inhibited by STI571. Blood 97 8 (2001) 2440-2448
40. Mol C.D., Dougan D.R., Schneider T.R., et al. Structural basis for the autoinhibition and STI-571 inhibition of c-Kit tyrosine kinase. J Biol Chem 279 30 (2004) 31655-31663
41. Dewar A.L., Cambareri A.C., Zannettino A.C., et al. Macrophage colony stimulating factor receptor, c-fins, is a novel target of imatinib. Blood 105 8 (2005) 3127-3132
42. Dagher R., Cohen M., Williams G., et al. Approval summary: imatinib mesylate in the treatment of metastatic and/or umesectable malignant gastrointestinal stromal tumors. Clin Cancer Res 8 10 (2002) 3034-3038
43. Demetri G., Benjamin R., Blanke C.D., et al. NCCN Task Force Report: optimal management of patients with gastrointestinal stromal tumor (GIST) - expansion and update ofNCCN Clinical Practice Guidelines. JNCCN 2 Suppl 1 (2004) S1-S26
44. Heinrich M.C., Griffith D.J., Druker B.J., Wait C.L., Ott K.A., and Zigler A.J. Inhibition of c-kit receptor tyrosine kinase activity by STI 571, a selective tyrosine kinase inhibitor. Blood 96 3 (2000) 925-932
45. Tuveson D.A., Willis N.A., Jacks T., et al. STI571 inactivation of the gastrointestinal stromal tumor c-KIT oncoprotein: biological and clinical implications. Oncogene 20 36 (2001) 5054-5058
46. Joensuu H., Fletcher C., Dimitrijevic S., Silberman S., Roberts P., and Demetri G. Management of malignant gastrointestinal stromal tumours. Lancet Oncol 3 11 (2002) 655-664
47. Medeiros F., Corless C.L., Duensing A., et al. KIT negative gastrointestinal stromal tumors: proof of concept and therapeutic implications. Am J Surg Pathol 28 7 (2004) 889-894
48. Fletcher C.D., Berman J.J., Corless C., et al. Diagnosis of gastrointestinal stromal tumors: a consensus approach. Hum Pathol 33 5 (2002) 459-465
49. Miettinen M., Furlong M., Sarlomo-Rikala M., Burke A., Sobin L.H., and Lasota J. Gastrointestinal stromal tumors, intramural leiomyomas, and leiomyosarcomas in the rectum and anus: a clinicopathologic, immunohistochemical, and molecular genetic study of 144 cases. Am J Surg Pathol 25 9 (2001) 1121-1133
50. Hubbard S.R. Juxtamembrane autoinhibition in receptor tyrosine kinases. Nat Rev Mot Cell Biol 5 6 (2004) 464-471
51. Corless C.L., Schroeder A., Griffith D., et al. PDGFRA mutations in gastrointestinal stromal tumors: frequency, spectrum and in vitro sensitivity to imatinib. J Clin Oncol 23 23 (2005) 5357-5364
52. Debiec-Rychter M., Wasag B., Stul M., et al. Gastrointestinal stromal tumours (GISTs) negative for KIT (CD117 antigen) immunoreactivity. J Pathol 202 4 (2004) 430-438
53. Sakurai S., Hasegawa T., Sakuria Y., et al. Myxoid epithelioid gastrointestinal stromal tumor (GIST) with mast cell infiltrations: a subtype of GIST with mutations of platelet-derived growth factor receptor alpha gene. Hum Pathol 35 10 (2004) 1223-1230
54. Wardelmann E., Hrychyk A., Merkelbach-Bruse S., et al. Association of platelet-derived growth factor receptor alpha mutations with gastric primary site and epithelioid or mixed cell morphology in gastrointestinal stromal tumors. J Mot Diag 6 3 (2004) 197-204
55. Miettinen M., Sobin L.H., and Sarlomo-Rikala M. Immunohistochemical spectrum of GISTs at different sites and their differential diagnosis with a reference to CD117 (KIT). Mod Pathol 13 10 (2000) 1134-1142
56. Antonescu C.R., Sommer G., Sarran L., et al. Association of KIT exon 9 mutations with nongastric primary site and aggressive behavior: KIT mutation analysis and clinical correlates of 120 gastrointestinal stromal tumors. Clin Cancer Res 9 9 (2003) 3329-3337
57. Lasota J., Wozniak A., Sarlomo-Rikala M., et al. Mutations in exons 9 and 13 of KIT gene are rare events in gastrointestinal stromal tumors. A study of 200 cases. Am J Pathol 157 4 (2000) 1091-1095
58. Sakurai S., Oguni S., Hironaka M., Fukayama M., Morinaga S., and Saito K. Mutations in c-kit gene exons 9 and 13 in gastrointestinal stromal tumors among Japanese. Jpn J Cancer Res 92 5 (2001) 494-498
59. Lasota J., Dansonka-Mieszkowska A., Sobin L.H., and Miettinen M. A great majority of GISTs with PDGFRA mutations represent gastric tumors of low or no malignant potential. Lab Invest 84 7 (2004) 874-883
60. Wasag B., Debiec-Rychter M., Pauwels P., et al. Differential expression of KIT/PDGFRA mutant isoforms in epithelioid and mixed variants of gastrointestinal stromal tumors depends predominantly on the tumor site. Mod Pathol 17 8 (2004) 889-894
61. Prakash S., Sarran L., Socci N., et al. Gastrointestinal stromal tumors in children and young adults: a clinicopathologic, molecular, andgenomic study of 15 cases and review of the literature. J Pediatr Hematol Oncol 27 4 (2005) 179-187
62. Yantiss R.K., Rosenberg A.E., Sarran L., Besmer P., and Antonescu C.R. Multiple gastrointestinal stromal tumors in type I neurofibromatosis: a pathologic and molecular study. Mod Pathol 18 4 (2005) 475-484
63. Diment J., Tamborini E., Casali P., Gronchi A., Carney J.A., and Colecchia M. Carney triad: case report and molecular analysis of gastric tumor. Hum Pathol 36 1 (2005) 112-116
64. Takazawa Y., Sakurai S., Sakuma Y., et al. Gastrointestinal stromal tumors of neurofibromatosis type I (von Recklinghausen's disease). Am J Surg Pathol 29 6 (2005) 755-763
65. Kinoshita K., Hirota S., Isozaki K., et al. Absence of c-kit gene mutations in gastrointestinal stromal tumours from neurofibromatosis type 1 patients. J Pathol 202 1 (2004) 80-85
66. Taniguchi M., Nishida T., Hirota S., et al. Effect of c-kit mutation on prognosis of gastrointestinal stromal tumors. Cancer Res 59 17 (1999) 4297-4300
67. Singer S., Rubin B.P., Lux M.L., et al. Prognostic value of KIT mutation type, mitotic activity, and histologic subtype in gastrointestinal stromal tumors. J Clin Oncol 20 18 (2002) 3898-3905
68. Kim T.W., Lee H., Kang Y.K., et al. Prognostic significance of c-kit mutation in localized gastrointestinal stromal tumors. Clin Cancer Res 10 9 (2004) 3076-3081
69. Hirota S., Nishida T., Isozaki K., et al. Gain-of-function mutation at the extracellular domain of KIT in gastrointestinal stromal tumours. J Pathol 193 4 (2001) 505-510
70. Joensuu H., Roberts P.J., Sarlomo-Rikala M., et al. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N Engl J Med 344 14 (2001) 1052-1056
71. van Oosterom A.T., Judson I., Verweij J., et al. Safety and efficacy of imatinib (ST1571) in metastatic gastrointestinal stromal tumours: a phase I study. Lancet 358 9291 (2001) 1421-1423
72. Verweij J., van Oosterom A., Blay J.Y., et al. Imatinib mesylate (STI-571 Glivec®, Gleevec) is an active agent for gastrointestinal stromal tumours, but does not yield responses in other soft-tissue sarcomas that are unselected for a molecular target. Results from an EORTC Soft Tissue and Bone Sarcoma Group phase II study. Eur J Cancer 39 14 (2003) 2006-2011
73. Verweij J., Casali P.G., Zalcberg J., et al. Progression-free survival in gastrointestinal stromal tumours with high-dose imatinib: randomised trial. Lancet 364 9440 (2004) 1127-1134
74. Demetri G.D., von Mehren M., Blanke C.D., et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 347 7 (2002) 472-480
75. [Abstract.]. Rankin C., Von Mehren M., Blanke C., et al. Dose effect of imatinib (IM) in patients (pts) with metastatic GIST-Phase III Sarcoma Group Study 50033. Proc Am Soc Clin Oncol 23 (2004) 815
76. van Oosterom A.T., Judson I.R., Verweij J., et al. Update of phase I study of imatinib (ST1571) in advanced soft tissue sarcomas and gastrointestinal stromal tumors: a report of the EORTC Soft Tissue and Bone Sarcoma Group. Eur J Cancer 38 Suppl 5 (2002) S83-S87
77. San Francisco, CA, USA, Abstract 2. Blanke C., Joensuu H., Demetri G., et al. Long-term follow up of advanced gastrointestinal stromal tumor (GIST) patients treated with imatinib mesylate. ASCO 2004 Gastrointestinal Cancers Symposium (January 22-24, 2004)
78. Vienna, Austria, p. iii202, Abstract 764E. Demetri G., von Mehren M., Joensuu H., et al. Lack of progression is the most clinically significant measure of a patients clinical benefit: Correlating the effects of imatinib mesylate therapy in gastrointestinal stromal tumor (GIST) with survival benefits. ESMO 2004 (October 29-November 2, 2004)
79. 2006. Blanke C., Joensuu H., Demetri G., et al. Outcome of advanced gastrointestinal stromal tumor (GIST) patients treated with imatinib mesylate: four-year follow-up of a phase II randomized trial. Proc Am Soc Clin Oncol GI (2006)
80. Debiec-Rychter M., Dumez H., Judson I., et al. Use of c-KIT/PDGFRA mutational analysis to predict the clinical response to imatinib in patients with advanced gastrointestinal stromal tumours entered on phase I and II studies of the EORTC Soft Tissue and Bone Sarcoma Group. Eur J Cancer 40 5 (2004) 689-695
81. 2005, p. Heinrich M., Shoemaker J., Corless C., et al. Correlation of target kinase genotype with clinical activity of imatinib mesylate in patients with metastatic GI stromal tumors expressing KIT. Proc Am Soc Clin Oncol (2005) 3s
82. Bauer S., Corless C.L., Heinrich M.C., et al. Response to imatinib mesylate of a gastrointestinal stromal tumor with very low expression of KIT. Cancer Chemother Pharmacol 51 3 (2003) 261-265
83. 2005. Blackstein M., Rankin C., Fletcher C., et al. Clinical benefit of imatinib in patients with metastatic gastrointestinal stromal tumors negative for the expression of CD117 in the 50033 trial. ASCO (2005) 818s
84. Sihto H., Sarlomo-Rikala M., Tynninen O., et al. KIT and platelet-derived growth factor receptor alpha tyrosine kinase gene mutations and KIT amplifications in human solid tumors. J Clin Oncol 23 1 (2005) 49-57
85. Burger H., den Bakker M.A., Kros J.M., et al. Activating mutations in c-KIT and PDGFRα are exclusively found in gastrointestinal stromal tumors and not in other tumors overexpressing these imatinib mesylate target genes. Cancer Biol Ther 4 11 (2005) 1270-1274
86. 2004. Desai J., Shankar S., Heinrich M.C., et al. Clonal evolution of resistance to imatinib in patients with gastrointestinal stromal tumor (GIST): Molecular and radiologic evaluation of new lesions. ASCO (2004) 197
87. Shankar S., Vansonnenberg E., Desai J., Dipiro P.J., Van Den Abbeele A., and Demetri G.D. Gastrointestinal stromal tumor: new nodule-within-a-mass pattern of recurrence after partial response to imatinib mesylate. Radiology 235 3 (2005) 892-898
88. Vanel D., Albiter M., Shapeero L., et al. Role of computed tomography in the follow-up of hepatic and peritoneal metastases of GIST under imatinib mesylate treatment: a prospective study of 54 patients. Eur J Radiol 54 1 (2005) 118-123
89. Choi H., Charnsangavej C., Faria Sde C., et al. CT evaluation of the response of gastrointestinal stromal tumors after imatinib mesylate treatment: a quantitative analysis correlated with FDG PET findings. Am J Roentgenol 183 6 (2004) 1619-1628
90. Antonescu C.R., Besmer P., Guo T., et al. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res 11 11 (2005) 4182-4190
91. Debiec-Rychter M., Cools J., Dumez H., et al. Mechanisms of resistance to imatinib mesylate in gastrointestinal stromal tumors and activity of the PKC412 inhibitor against imatinib-resistant mutants. Gastroenterology 128 2 (2005) 270-279
92. Chen L.L., Trent J.C., Wu E.F., et al. A missense mutation in KIT kinase domain 1 correlates with imatinib resistance in gastrointestinal stromal tumors. Cancer Res 64 17 (2004) 5913-5919
93. Tamborini E., Bonadiman L., Greco A., et al. A new mutation in the KIT ATP pocket causes acquired resistance to imatinib in a gastrointestinal stromal tumor patient. Gastroenterology 127 1 (2004) 294-299
94. Wardelmann E., Thomas N., Merkelbach-Brase S., et al. Acquired resistance to imatinib in gastrointestinal stromal tumours caused by multiple KIT mutations. Lancet Oncol 6 4 (2005) 249-251
95. Wakaf T., Kanda T., Hirota S., Ohashi A., Shirai Y., and Hatakeyama K. Late resistance to imatinib therapy in a metastatic gastrointestinal stromal tumour is associated with a second KIT mutation. Br J Cancer 90 11 (2004) 2059-2061