Gastrointestinal stromal tumors: Overview of pathologic features, molecular biology, and therapy with imatinib mesylate

Histology and Histopathology

Volumn 19, Issue 2, 2004, Pages 565-574

  Koh, J S ^a   Trent, J ^a   Chen, L ^a   El Naggar, A ^a   Hunt, K ^a   Pollock, R ^a   Zhang, Wei ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

GIST; Imatinib mesylate; KIT

Indexed keywords

DOXORUBICIN; IFOSFAMIDE; IMATINIB; PLATELET DERIVED GROWTH FACTOR RECEPTOR; STEM CELL FACTOR RECEPTOR; TUMOR MARKER; TYROSINE KINASE RECEPTOR;

CHROMOSOME ABERRATION; CLINICAL TRIAL; DIFFERENTIAL DIAGNOSIS; DRUG EFFICACY; DRUG RECEPTOR BINDING; DRUG RESISTANCE; DRUG TARGETING; EXON; GASTROINTESTINAL STROMAL TUMOR; GENE MUTATION; GENETIC CODE; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; INTESTINE CELL; LEIOMYOSARCOMA; MALIGNANT TRANSFORMATION; MITOSIS; MOLECULAR BIOLOGY; MUSCLE TUMOR; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PROGNOSIS; PROTEIN EXPRESSION; PROTO ONCOGENE; RETROSPECTIVE STUDY; REVIEW; SIGNAL TRANSDUCTION; STOMACH TUMOR; TREATMENT FAILURE; TUMOR VOLUME; WILD TYPE;

ANTINEOPLASTIC AGENTS; BINDING SITES; GASTROINTESTINAL NEOPLASMS; HUMANS; IMMUNOHISTOCHEMISTRY; MUTATION; PIPERAZINES; PROGNOSIS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-KIT; PYRIMIDINES; STROMAL CELLS;

EID: 1842558973     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (77)

1. Al-Bozom I.A. (2001). p53 expression in gastrointestinal stromal tumors. Pathol. Int. 51, 519-523.
2. Allander S.V., Nupponen N.N., Ringner M., Hostetter G., Maher G.W., Goldberger N., Chen Y., Carpten J., Elkahloun A.G. and Meltzer P.S. (2001). Gastrointestinal stromal tumors with KIT mutations exhibit a remarkably homogeneous gene expression profile. Cancer Res. 61, 8624-8668.
3. Andersson J., Sjogren H., Meis-Kindblom J.M., Stenman G., Aman P. and Kindblom L.G. (2002). The complexity of KIT gene mutations and chromosome rearrangements and their clinical correlation in gastrointestinal stromal (pacemaker cell) tumors. Am. J. Pathol. 160, 15-22.
4. Bauer S., Corless C.L., Heinrich M.C., Dirsch O., Antoch G., Kanja J., Seeber S. and Schutte J. (2003). Response to imatinib mesylate of a gastrointestinal stromal tumor with very low expression of KIT. Cancer Chemother. Pharmacol. 51, 261-265.
5. Beghini A., Tibiletti M.G., Roversi G., Chiaravalli A.M., Serio G., Capella C. and Larizza L. (2001). Germline mutation in the juxtamembrane domain of the kit gene in a family with gastrointestinal stromal tumors and urticaria pigmentosa. Cancer 92, 657-662.
6. Blume-Jensen P., Claesson-Welsh L., Siegbahn A., Zsebo K.M., Westermark B. and Heldin C.H. (1991). Activation of the human c-kit product by ligand-induced dimerization mediates circular actin reorganization and chemotaxis. EMBO J. 10, 4121-4128.
7. Buchdunger E., Cioffi C.L., Law N., Stover D., Ohno-Jones S., Druker B.J. and Lydon N.B. (2000). Abl 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, 139-145.
8. Chian R., Young S., Danilkovitch-Miagkova A., Ronnstrand L., Leonard E., Ferrao P., Ashman L. and Linnekin D. (2001). Phosphatidylinositol 3 kinase contributes to the transformation of hematopoietic cells by the D816V c-Kit mutant. Blood 98, 1365-1373.
9. Choi Y.R., Kim H.K., Kang H.J., Kim N.G., Kim J.J., Park K.S., Paik Y.K., Kim H.O. and Kim H. (2003). Overexpression of high mobility group box 1 in gastrointestinal stromal tumors with KIT mutation. Cancer Res. 63, 2188-2193.
10. Corless C.L., McGreevey L., Haley A., Town A. and Heinrich M.C. (2002). KIT mutations are common in incidental gastrointestinal stromal tumors one centimeter or less in size. Am. J. Pathol. 160, 1567-1572.
11. Demetri G.D., von Mehren M., Blanke C.D., Van den Abbeele A.D., Eisenberg B., Roberts P.J., Heinrich M.C., Tuveson D.A., Singer S., Janicek M., Fletcher J.A., Silverman S.G., Silberman S.L., Capdeville R., Kiese B., Peng B., Dimitrijevic S., Druker B..J., Corless C., Fletcher C.D. and Joensuu H. (2002). Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N. Engl. J. Med. 347, 472-480.
12. De Miguel M.P., Cheng L., Holland E.C., Federspiel M.J., and Donovan P.J. (2002). Dissection of the c-Kit signaling pathway in mouse primordial germ cells by retroviral-mediated gene transfer. Proc. Natl. Acad. Sci. USA 99, 10458-10463.
13. De Silva C.M. and Reid R. (2003). Gasrointestinal stromal tumors (GIST): C-kit mutations, CD117 expression, differential diagnosis and targeted cancer therapy with imatinib. Pathol. Oncol. Res. 9, 13-19.
14. DeMatteo R.P., Lewis J.J., Leung D., Mudan S.S., Woodruff J.M. and Brennan M.F. (2000). Two hundred gastrointestinal stromal tumors: Recurrence patterns and prognostic factors for survival. Ann. Surg. 231, 51-58.
15. Dematteo R.P., Heinrich M.C., El-Rifai W.M. and Demetri G. (2002). Clinical management of gastrointestinal stromal tumors: Before and after STI-571. Hum. Pathol. 33, 466-477.
16. El-Rifai W., Sarlomo-Rikala M., Andersson L.C., Knuutila S. and Miettinen M. (2000). DNA sequence copy number changes in gastrointestinal stromal tumors: Tumor progression and prognostic significance. Cancer Res. 60, 3899-3903.
17. Ernst S.I., Hubbs A.E., Przygodzki R.M., Emory T.S., Sobin L.H. and O'Leary T.J. (1998). KIT mutation portends poor prognosis in gastrointestinal stromal/smooth muscle tumors. Lab. Invest. 78, 1633-1636.
18. Fleischman R.A. (1993). From white spots to stem cells: The role of the KIT receptor in mammalian development. Trends Genet. 9, 285-290.
19. Fletcher C.D., Berman J.J., Corless C., Gorstein F., Lasota J., Longley B.J., Miettinen M., O'Leary T.J., Remotti H., Rubin B.P., Shmookler B., Sobin L.H. and Weiss S.W. (2002). Diagnosis of gastrointestinal stromal tumors: A consensus approach. Hum. Pathol. 33, 459-465.
20. Furitsu T., Tsujimura T., Tono T., Ikeda H., Kitayama H., Koshimizu U., Sugahara H., Butterfield J.H., Ashman L.K. and Kanayama Y. (1993). Identification of mutations in the coding sequence of the proto-oncogene c-kit in a human mast cell leukemia cell line causing ligand-independent activation of c-kit product. J. Clin. Invest. 92, 1736-1744.
21. Greenson J.K. (2003). Gasrointestinal stromal tumors and other mesenchymal lesions of the gut. Mod. Pathol. 16, 366-375.
22. Gorre M.E., Mohammed M., Ellwood K., Hsu N., Paquette R., Rao P.N. and Sawyers C.L. (2001). Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293, 876-880.
23. Gottlieb J.A., Benjamin R.S., Baker L.H., O'Bryan R.M., Sinkovics J.G., Hoogstraten B., Quagliana J.M., Rivkin S.E., Bodey G.P. Sr, Rodriguez V., Blumenschein G.R., Saiki J.H., Coltman C. Jr, Burgess M.A., Sullivan P., Thigpen T., Bottomley R., Balcerzak S. and Moon T.E. (1976) Role of DTIC (NSC-45388) in the chemotherapy of sarcomas. Cancer Treat Rep. 60, 199-203.
24. Gunawan B., Bergmann F., Hoer J., Langer C., Schumpelick V., Becker H. and Fuzesi L. (2002). Biological and clinical significance of cytogenetic abnormalities in low-risk and high-risk gastrointestinal stromal tumors. Hum. Pathol. 33, 316-321.
25. Hasegawa T., Matsuno Y., Shimoda T. and Hirohashi S. (2002). Gastrointestinal stromal tumor: Consistent CD117 immunostaining for diagnosis and prognostic classification based on tumor size and MIB-1 grade. Hum. Pathol. 33, 669-676.
26. Heinrich M.C., Rubin B.P., Longley B.J. and Fletcher J.A. (2002). Biology and genetic aspects of gastrointestinal stromal tumors: KIT activation and cytogenetic alterations. Hum. Pathol. 33, 484-495.
27. Heinrich M.C., Corless C.L., Duensing A., McGreevey L., Chen C.J., Joseph N., Singer S., Griffith D.J., Haley A., Town A., Demetri G.D., Fletcher C.D., Fletcher J.A. (2003). DGFRA activating mutations in gastrointestinal stromal tumors. Science 299, 708-710.
28. Hirota S., Isozaki K., Moriyama Y., Hashimoto K., Nishida T., Ishiguro S., Kawano K., Hanada M., Kurata A., Takeda M., Muhammad Tunio G., Matsuzawa Y., Kanakura Y., Shinomura Y. and Kitamura Y. (1998). Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279, 577-580.
29. Hirota S., Nishida T., Isozaki K., Taniguchi M., Nakamura J., Okazaki T. and Kitamura Y. (2001). Gain-of-function mutation at the extracellular domain of KIT in gastrointestinal stromal tumours. J. Pathol. 193, 505-510.
30. Hirota S., Nishida T., Isozaki K., Taniguchi M., Nishikawa K., Ohashi A., Takabayashi A., Obayashi T., Okuno T., Kinoshita K., Chen H., Shinomura Y. and Kitamura Y. (2002). Familial gastrointestinal stromal tumors associated with dysphagia and novel type germline mutation of KIT gene. Gastroenterology 122, 1493-1499.
31. Hornick J.L. and Fletcher C.D. (2002). Immunohistochemical staining for KIT (CD117) in soft tissue sarcomas is very limited in distribution. Am. J. Clin. Pathol. 117, 188-193.
32. Huizinga J.D., Thuneberg L., Kluppel M., Malysz J., Mikkelsen H.B. and Bernstein A. (1995). W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373, 347-349.
33. Isozaki K., Hirota S., Nakama A., Miyagawa J., Shinomura Y., Xu Z., Nomura S. and Kitamura Y. (1995). Disturbed intestinal movement, bile reflux to the stomach, and deficiency of c-kit-expressing cells in Ws/Ws mutant rats. Gastroenterology 109, 456-464.
34. Isozaki K., Terris B., Belghiti J., Schiffmann S., Hirota S. and Vanderwinden J.M. (2000). Germline-activating mutation in the kinase domain of KIT gene in familial gastrointestinal stromal tumors. Am. J. Pathol. 157, 1581-1585.
35. Joensuu H., Roberts P.J., Sarlomo-Rikala M., Andersson L.C., Tervahartiala P., Tuveson D., Silberman S., Capdeville R., Dimitrijevic S., Druker B. and Demetri G.D. (2001). Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N. Engl. J. Med. 344, 1052-1056.
36. Kindblom L.G., Remotti H.E., Aldenborg F. and Meis-Kindblom J.M. (1998). Gastrointestinal pacemaker cell tumor (GIPACT): Gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am. J. Pathol. 152, 1259-1269.
37. Kluppel M., Huizinga J.D., Malysz J. and Bernstein A. (1998). Developmental origin and KIT-dependent development of the interstitial cells of Cajal in the mammalian small intestine. Dev. Dyn. 211, 60-71.
38. Kozlowski M., Larose L., Lee F., Le D.M., Rottapel R. and Siminovitch K.A. (1998). SHIP-1 binds and negatively modulates the c-Kit receptor by interaction with tyrosine 569 in the c-Kit juxtamembrane domain. Mol. Cell. Biol. 18, 2089-2099.
39. Lasota J., Carlson J.A. and Miettinen M. (2000). Spindle cell tumor of urinary bladder serosa with phenotypic and genotypic features of gastrointestinal stromal tumor. Arch. Pathol. Lab. Med. 124, 894-897.
40. Lasota J., Jasinski M., Sarlomo-Rikala M. and Miettinen M. (1999). Mutations in exon 11 of c-Kit occur preferentially in malignant versus benign gastrointestinal stromal tumors and do not occur in leiomyomas or leiomyosarcomas. Am. J. Pathol. 154, 53-60.
41. Lee J.R., Joshi V., Griffin J.W. Jr., Lasota J. and Miettinen M. (2001). Gastrointestinal autonomic nerve tumor: Immunohistochemical and molecular identity with gastrointestinal stromal tumor. Am. J. Surg. Pathol. 25, 979-987.
42. Linnekin D. (1999). Early signaling pathways activated by c-Kit in hematopoietic cells. Int. J. Biochem. Cell. Biol. 31, 1053-1074.
43. Longley B.J., Reguera M.J. and Ma Y. (2001). Classes of c-KIT activating mutations: Proposed mechanisms of action and implications for disease classification and therapy. Leuk. Res. 25, 571-576.
44. Ma Y., Cunningham M.E., Wang X., Ghosh I., Regan L. and Longley B.J. (1999). Inhibition of spontaneous receptor phosphorylation by residues in a putative alphahelix in the KIT intracellular juxtamembrane region. J. Biol. Chem. 274, 13399-13402.
45. Ma Y., Zeng S., Metcalfe D.D., Akin C., Dimitrijevic S., Butterfield J.H., McMahon G. and Longley B.J. (2002). The c-kit mutation causing human mastocytosis is resistant to STI-571 and other KIT kinase inhibitors: Kinases with enzymatic site mutations show different inhibitor sensitivity profiles than wild-type kinases and those with regulatory-type mutations. Blood 99, 1741-1744.
46. Maeyama H., Hidaka E., Ota H., Minami S., Kajiyama M., Kuraishi A., Mori H., Matsuda Y., Wada S., Sodeyama H., Nakata S., Kawamura N., Hata S., Watanabe M., Iijima Y. and Katsuyama T. (2001). Familial gastrointestinal stromal tumor with hyperpigmentation: Association with a germline mutation of the c-kit gene. Gastroenterology 120, 210-215.
47. Majumder S., Brown K., Qiu F.H. and Besmer P. (1998). c-kit protein, a transmembrane kinase: Identification in tissues and characterization. Mol. Cell. Biol. 8, 4896-4903.
48. Mazur M.T. and Clark H.B. (1983). Gastric stromal tumors: Reappraisal of histogenesis. Am. J. Surg. Pathol. 7, 507-519.
49. Miettinen M. (2001). Are desmoid tumors KIT positive? Am. J. Surg. Pathol. 25, 549-550.
50. Miettinen M., Monihan J.M., Sarlomo-Rikala M., Kovatich A.J., Carr N.J., Emory T.S. and Sobin L.H. (1999). 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, 1109-1118.
51. Miettinen M., Sobin L.H. and Sarlomo-Rikala M. (2000). Immunohistochemical spectrum of GISTs at different sites and their differential diagnosis with a reference to CD117 (KIT). Mod. Pathol. 13, 1134-1142.
52. Montgomery E., Torbenson M.S., Kaushal M., Fisher C. and Abraham S.C. (2002). b-catenin immunohistochemistry separates mesenteric fibromatosis from gastrointestinal stromal tumor and sclerosing mesenteritis. Am. J. Surg. Pathol. 26, 1296-1301.
53. Moskaluk C.A., Tian Q., Marshall C.R., Rumpel C.A., Franquemont D.W. and Frierson H.F. Jr. (1999). Mutations of c-kit JM domain are found in a minority of human gastrointestinal stromal tumors. Oncogene 18, 1897-1902.
54. Nakahara M., Isozaki K., Hirota S., Miyagawa J., Hase-Sawada N., Taniguchi M., Nishida T., Kanayama S., Kitamura Y., Shinomura Y. and Matsuzawa Y. (1998). A novel gain-of function mutation of c-kit gene in gastrointestinal stromal tumors. Gastroenterology 115, 1090-1095.
55. Ng E.H., Pollock R.E., Munsell M.F., Atkinson E.N. and Romsdahl M.M. (1992). Prognostic factors influencing survival in gastrointestinal leiomyosarcomas. Implications for surgical management and staging. Ann. Surg. 215, 68-77.
56. Nishida T., Hirota S., Taniguchi M., Hashimoto K., Isozaki K., Nakamura H., Kanakura Y., Tanaka T., Takabayashi A., Matsuda H. and Kitamura Y. (1998). Familial gastrointestinal stromal tumours with germline mutation of the KIT gene. Nat. Genet. 19, 323-324.
57. Ortiz-Hidalgo C., de Leon Bojorge B. and Albores-Saavedra J. (2000). Stromal tumor of the gallbladder with phenotype of interstitial cells of Cajal. A previously unrecognized neoplasm. Am. J. Surg. Pathol. 24, 1420-1423.
58. Panizo-Santos A., Sola I., Vega F., de Alava E., Lozano M.D., Idoate M.A. and Pardo-Mindan J. (2000). Predicting metastatic risk of gastrointestinal stromal tumors: Role of cell proliferation and cell cycle regulatory proteins. Int. J. Surg. Pathol. 8, 133-144.
59. Piao X., Paulson R., van der Geer P., Pawson T. and Bernstein A. (1996). Oncogenic mutation in the Kit receptor tyrosine kinase alters substrate specificity and induces degradation of the protein tyrosine phosphatase SHP-1. Proc. Natl. Acad. Sci. USA 93, 14665-14669.
60. Reith J.D., Goldblum J.R., Lyles R.H. and Weiss S.W. (2000). Extragastrointestinal (soft tissue) stromal tumors: An analysis of 48 cases with emphasis on histological predictors of outcome. Mod. Pathol. 13, 577-585.
61. Rubin B.P., Singer S., Tsao C., Duensing A., Lux M.L., Ruiz R., Hibbard M.K., Chen C.J., Xiao S., Tuveson D.A., Demetri G.D., Fletcher C.D. and Fletcher J.A. (2001). KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res. 81, 8118-8121.
62. Sakurai S., Fukasawa T., Chong J.M., Tanaka A. and Fukayama M. (1999). C-kit gene abnormalities in gastrointestinal stromal tumors (tumors of interstitial cells of Cajal). Jpn. J. Cancer Res. 90, 1321-1328.
63. Sakurai S., Oguni S., Hironaka M., Fukayama M., Morinaga S. and Saito K. (2001). Mutations in c-kit gene exons 9 and 13 in gastrointestinal stromal tumors among Japanese. Jpn. J. Cancer Res. 92, 494-498.
64. Sarlomo-Rikala M., Kovatich A.J., Barusevicius A. and Miettinen M. (1998). CD117: A sensitive marker for gastrointestinal stromal tumors that is more specific than CD34. Mod. Pathol. 11, 728-734.
65. Savage D.G. and Antman K.H. (2002). Imatinib mesylate - a new oral targeted therapy. N. Engl. J. Med. 346, 683-693.
66. Schneider-Stock R., Boltze C., Lasota J., Miettinen M., Peters B., Pross M., Roessner A. and Gunther T. (2003). High prognostic value of p16INK4 alterations in gastrointestinal stromal tumors. J. Clin. Oncol. 21, 1688-1697.
67. Shidham V.B., Chivukula M., Gupta D., Rao R.N. and Komorowski R. (2002). Immunohistochemical comparison of gastrointestinal stromal tumor and solitary fibrous tumor. Arch. Pathol. Lab. Med. 126, 1189-1192.
68. Sircar K., Hewlett B.R., Huizinga J.D., Chorneyko K., Berezin I. and Riddell R.H. (1999). Interstitial cells of Cajal as precursors of gastrointestinal tumors. Am. J. Surg. Pathol. 23, 377-389.
69. Takahashi R., Tanaka S., Kitadai Y., Sumii M., Yoshihara M., Haruma K. and Chayama K. (2003). Expression of vascular endothelial growth factor and angiogenesis in gastrointestinal stromal tumor of the stomach. Oncology 64, 266-274.
70. Taniguchi M., Nishida T., Hirota S., Taniguchi M., Nishida T., Hirota S., Isozaki K., Ito T., Nomura T., Matsuda H. and Kitamura Y. (1999). Effect of c-kit mutation on prognosis of gastrointestinal stromal tumors. Cancer Res. 59, 4297-4300.
71. Taylor M.L. and Metcalfe D.D. (2000). Kit signal transduction. Hematol Oncol Clin. North Am. 14, 517-535.
72. Tuveson D.A., Willis N.A., Jacks T., Griffin J.D., Singer S., Fletcher C.D., Fletcher J.A. and Demetri G.D. (2001). STI571 inactivation of the gastrointestinal stromal tumor c-KIT oncoprotein: Biological and clinical implications. Oncogene 20, 5054-5058.
73. Van de Rijn M., Hendrickson M.R. and Rouse R.V. (1994). The CD34 expression by gastrointestinal stromal tumors. Hum. Pathol. 25, 766-771.
74. Van Oosterom A.T., Judson I., Verweij J., Stroobants S., Donato di Paola E., Dimitrijevic S., Martens M., Webb A., Sciot R., Van Glabbeke M., Silberman S. and Nielsen O.S. European Organisation for Research and Treatment of Cancer Soft Tissue and Bone Sarcoma Group. (2001). Safety and efficacy of imatinib (STI571) in metastatic gastrointestinal stromal tumors: A phase I study. Lancet 358, 1421-1423.
75. Walker P. and Dvorak A.M. (1986). Gastrointestinal autonomic nerve (GAN) tumor: Ultrastructural evidence for a newly recognized entity. Arch. Pathol. Lab. Med. 110, 309-316.
76. Yantiss R.K., Spiro I.J., Compton C.C. and Rosenberg A.E. (2000). Gastrointestinal stromal tumor versus intra-abdominal fibromatosis of the bowel wall. Am. J. Surg. Pathol. 24, 947-957.
77. Zhang Z., Zhang R., Joachimiak A., Schlessinger J. and Kong X.P. (2000). Crystal structure of human stem cell factor: Implication for stem cell factor receptor dimerization and activation. Proc. Natl. Acad. Sci. USA 97, 7732-7737.