Editorial The Significance of KIT (CD117) in Gastrointestinal Stromal Tumors
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1 International Journal of Surgical Pathology 12(2):93 97, 2004 Editorial The Significance of KIT (CD117) in Gastrointestinal Stromal Tumors Jason L. Hornick, MD, PhD, and Christopher D. M. Fletcher, MD, FRCPath With remarkable speed thus far seemingly unparalleled in cancer biology, the rapid transformation in our understanding of the pathogenesis of gastrointestinal stromal tumors (GISTs) has both refined diagnostic criteria and has led to rational targeted molecular therapies for this malignancy, which was previously untreatable once relapse occurred or metastatic disease developed. Since 1998, when activating mutations in the receptor tyrosine kinase c-kit were first identified in GISTs [1] and immunohistochemical detection of the protein product KIT (CD117) was recognized to be a virtually specific diagnostic marker for GISTs among mesenchymal tumors of the gastrointestinal tract [2], out of the formerly nebulous category of stromal tumors (that also included both benign and malignant smooth muscle tumors) emerged the diagnostically reproducible entity GIST. Histologically, GISTs may be spindled, epithelioid, or of mixed cell type with fibrillary cytoplasm and ill-defined cell borders, in contrast to true smooth muscle tumors, which typically have more brightly eosinophilic cytoplasm and more distinct cell borders [3]. GISTs usually also have remarkably uniform nuclear morphology, and nuclear pleomorphism is extremely uncommon. Recognition of the distinctive morphology of GISTs facilitates confirmation of the diagnosis by immunohistochemistry: not only are GISTs generally positive for KIT, but (in >99% of cases) they are also From the Department of Pathology, Brigham and Women s Hospital, and Harvard Medical School, Boston, MA. Reprint requests: Christopher D. M. Fletcher, MD, FRCPath, Department of Pathology, Brigham and Women s Hospital, 75 Francis Street, Boston, MA negative for desmin, which is the most useful marker for supporting true smooth muscle differentiation in this context and for the diagnosis of leiomyosarcoma, the most important differential diagnostic consideration. Mutations in c-kit, which have been found in around 90% of GISTs [4], lead to constitutive (ligand-independent) activation of the KIT tyrosine kinase, which is believed to be a primary oncogenic event in the development of GIST. The majority (approximately 70%) of c-kit mutations in GISTs occur in exon 11 [5], corresponding to the juxtamembrane domain (Fig. 1). Less frequent mutations are found in exons 9, 13, or 17 [6], corresponding to the extracellular and kinase domains. Distinguishing GISTs from other mesenchymal tumors has become critically important as selective small molecule tyrosine kinase inhibitors have been developed. Imatinib (Gleevec in the United States, Glivec in the rest of the world, Novartis, Basel, Switzerland), developed as a targeted inhibitor of the bcr-abl fusion protein of chronic myelogenous leukemia [7,8] and shown also, in preclinical studies, to inhibit the activity of mutant KIT isoforms common in GISTs [9,10], has demonstrated remarkable efficacy in patients with unresectable or metastatic GIST; most patients show a major clinical response following single agent imatinib therapy [11,12]. Moreover, preliminary (unpublished) evidence suggests that second-generation tyrosine kinase inhibitors, now being evaluated in patients whose GISTs become refractory to imatinib therapy, may also be efficacious in treating patients with advanced GISTs (G. Demetri, personal communication). The dramatic responses to imatinib in patients with GIST have prompted investigations into whether other tumors might demonstrate KIT over- 93
2 94 International Journal of Surgical Pathology Vol. 12 No. 2 April 2004 expression, in the hopes that other tumors might also be candidates for imatinib therapy. Some initial reports described several other soft tissue tumors with immunohistochemical positivity for KIT [13,14], including Ewing s sarcoma/peripheral neuroectodermal tumor (PNET), angiosarcoma, metastatic melanoma, and desmoid fibromatosis. In our experience, KIT can indeed be found in a subset of these tumors [15]. It has become clear, however, that technical factors including antibody selection and experimental techniques (principally, antibody dilutions and the use of heat-induced antigen retrieval) significantly impact the results of KIT immunohistochemistry. An illustrative example is desmoid fibromatosis. Highly variable immunohistochemical findings with respect to KIT have been reported, ranging from a study that described nearly all desmoid tumors positive for KIT [14] to our report showing only rare KIT positivity in such lesions [15]. A recent study thoroughly evaluated KIT expression in desmoids by testing both of the widely used commercial antibodies against KIT at different dilutions, with and without heat-induced antigen retrieval [16]. The investigators demonstrated that at low dilutions, significant numbers of cases were positive for KIT, accompanied by background stromal staining, which was eliminated at higher dilutions. Similarly, at higher dilutions, nearly all desmoid tumors were negative for KIT. From this study, it now appears that desmoids are in fact generally KIT negative and that, not surprisingly, without careful elimination of background staining, misleading nonspecific KIT positivity may be seen. Moreover, antigen retrieval should not be applied indiscriminately, but instead reserved for those antibodies found to require such pretreatment. Despite the absence of genuine KIT expression in virtually all cases of desmoid fibromatosis, a pilot study demonstrated partial responses to imatinib in 2 patients with multiply recurrent extraabdominal desmoid tumors [17], likely due to the inhibitory effects of imatinib on platelet-derived growth factor receptor (PDGFR) tyrosine kinases (rather than on mutant KIT, which has never been identified in desmoids). Given the potential clinical importance of KIT immunohistochemistry, optimization of experimental techniques and reproducibility are critical. It is not yet clear how standardization of such therapeutically relevant immunohistochemical testing should be established or maintained. Notable examples of other tumors that usually contain c-kit-activating mutations (and are immunopositive for KIT) include mast cell tumors and seminomas. However, since human systemic mastocytosis and seminoma usually contain a c-kit mutation in the enzymatic site (unlike the mutations found in GIST) (Fig. 1), which is resistant to imatinib [18,19], the majority of patients with such tumors are unlikely to benefit from imatinib, and, furthermore, seminomas rarely require second-line therapies such as this. Additionally, it is important to remember that immunohistochemical detection of KIT does not necessarily imply KIT activation. In this regard, as indicated above, there are several examples of soft tissue tumors other than GIST that show occasional KIT expression by immunohistochemistry (e.g., angiosarcoma, Ewing s sarcoma/ PNET, extraskeletal myxoid chondrosarcoma) [13,15]. Importantly, neither c-kit-activating mutations nor KIT oncoprotein activity have been identified in these tumors, and responses to imatinib have not been seen. This underscores the importance of confirming KIT oncoprotein activity in tumors in which KIT has been detected by immunohistochemistry before offering false hope to clinicians and patients that tyrosine kinase inhibitor therapies are warranted. Recent data from a phase II clinical trial indicate that the specific site of the c-kit mutation in GISTs has prognostic relevance with respect to sensitivity to imatinib therapy [20] (Table 1). In this study, nearly 85% of patients whose GISTs harbor the most common exon 11 mutations had at least a partial response to imatinib, compared to approximately 50% of those with exon 9 mutations. In contrast, no partial responses were observed in the small number of patients with GISTs containing wild-type c-kit, i.e., lacking c-kit mutations. These results demonstrate that genetic subtyping of GISTs can predict sensitivity to imatinib. Although the majority of GISTs contain c-kit-activating mutations, in a significant subset (perhaps up to 15%), c-kit mutations are absent. Recent studies have shown that homologous mutations in the receptor tyrosine kinase PDGFRA can be found in a significant subset of GISTs lacking c-kit mutations [20 22]. Mutations in PDGFRA provide an alternative mechanism in GIST oncogenesis. Since imatinib inhibits not only KIT but also other receptor tyrosine kinases including PDGFRA, it is not surprising that some patients whose GISTs contain PDGFRA mutations also respond to imatinib therapy [22]. The oncogenic mechanisms in GISTs lacking both c-kit and PDGFRA mutations remain obscure. Given the fact that immunohistochemical detection of KIT has been regarded as the single most important diagnostic criterion for GISTs [3], whether tumors that lack KIT overexpression are in fact GISTs has been controversial. We have found that approxi-
3 Significance of KIT (CD117) in GISTs Hornick and Fletcher 95 Fig. 1. Schematic diagram of sites of KIT mutations in GIST, mastocytosis, and seminoma. See also Table 1 for correlation with treatment data. Table 1. Clinical Response of GISTs to Imatinib Correlated with Mutational Status (See Also Ref 22) Genotype % of Cases Imatinib Response KIT exon 11 mutation 65 70% 80 85% KIT exon 9 mutation 15 20% 45 50% KIT exon 13 mutation <5% Some (few data) KIT exon 17 mutation <5% Some (few data) PDGFRA mutation ~5% Variable No KIT or PDGFRA mutation 5 10% None mately 4% of GISTs with otherwise typical clinicopathologic, immunohistochemical, and cytogenetic features are negative for KIT by immunohistochemistry. The majority of these GISTs harbor PDGFRA mutations [23]. Interestingly, it appears that KITnegative GISTs show an unusual predominance of epithelioid cell morphology, as well as more frequent omental/peritoneal origin. Thus, not surprisingly, the relationship between KIT and GIST has not proved to be as straightforward as it first appeared. Clearly, since the vast majority of GISTs are positive for KIT, and other mesenchymal tumors of the gastrointestinal tract in the differential diagnosis are not, then immunohistochemical testing for KIT has a critical role in routine clinical practice. However, since it now appears that a subset of GISTs lack detectable KIT expression by immunohistochemistry and/or harbor alternative oncogenic PDGFRA mutations, which may also be responsive to targeted tyrosine kinase inhibitor
4 96 International Journal of Surgical Pathology Vol. 12 No. 2 April 2004 therapy, whether KIT detection should be required for treatment eligibility for tyrosine kinase inhibitors such as imatinib is uncertain. So long as strict morphologic criteria are applied, it is likely that patients with tumors that have otherwise typical clinicopathologic features of GIST, except for KIT negativity by immunohistochemistry, should not be denied imatinib (or other tyrosine kinase inhibitor) therapy at this time. Conversely, at least so far, it seems that KIT immunopositivity in mesenchymal tumors other than GIST has no relevance with regard to imatinib therapy. In the absence of prior evidence of activating c-kit mutations in a given tumor type, speculative immunostaining for KIT appears quite pointless and should be discouraged. References 1. 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, Kitamura Y. Gain-offunction mutations of c-kit in human gastrointestinal stromal tumors. Science 279: , Sarlomo-Rikala M, Kovatich AJ, Barusevicius A, Miettinen M. CD117: A sensitive marker for gastrointestinal stromal tumors that is more specific than CD34. Mod Pathol 11: , Fletcher CDM, Berman JJ, Corless C, Gorstein F, Lasota J, Longley BJ, Miettinen M, O Leary TJ, Remotti H, Rubin BP, Shmookler B, Sobin LH, Weiss SW. Diagnosis of gastrointestinal stromal tumors: A consensus approach. Hum Pathol 33: , Heinrich MC, Rubin BP, Longley BJ, Fletcher JA. Biology and genetic aspects of gastrointestinal stromal tumors: KIT activation and cytogenetic alterations. Hum Pathol 33: , Rubin BP, Singer S, Tsao C, Duensing A, Lux ML, Ruiz R, Hibbard MK, Chen CJ, Xiao S, Tuveson DA, Demetri GD, Fletcher CD, Fletcher JA. KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res 61: , Lux ML, Rubin BP, Biase TL, Chen CJ, Maclure T, Demetri G, Xiao S, Singer S, Fletcher CD, Fletcher JA. KIT extracellular and kinase domain mutations in gastrointestinal stromal tumors. Am J Pathol 156: , Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, Zimmermann J, Lydon NB. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 2: , Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno-Jones S, Sawyers CL. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 344: , Heinrich MC, Griffith DJ, Druker BJ, Wait CL, Ott KA, Zigler AJ. Inhibition of c-kit receptor tyrosine kinase activity by STI 571, a selective tyrosine kinase inhibitor. Blood 96: , Tuveson DA, Willis NA, Jacks T, Griffin JD, Singer S, Fletcher CD, Fletcher JA, Demetri GD. STI571 inactivation of the gastrointestinal stromal tumor c-kit oncoprotein: Biological and clinical implications. Oncogene 20: , van Oosterom AT, Judson I, Verweij J, Stroobants S, Donato di Paola E, Dimitrijevic S, Martens M, Webb A, Sciot R, Van Glabbeke M, Silberman S, Nielsen OS. European Organisation for Research and Treatment of Cancer Soft Tissue and Bone Sarcoma Group. Safety and efficacy of imatinib (STI571) in metastatic gastrointestinal stromal tumours: A phase I study. Lancet 358: , Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, Heinrich MC, Tuveson DA, Singer S, Janicek M, Fletcher JA, Silverman SG, Silberman SL, Capdeville R, Kiese B, Peng B, Dimitrijevic S, Druker BJ, Corless C, Fletcher CDM, Joensuu H. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 347: , Miettinen M, Sobin LH, Sarlomo-Rikala M. Immunohistochemical spectrum of GISTs at different sites and their differential diagnosis with reference to CD117 (KIT). Mod Pathol 13: , Yantiss RK, Spiro IJ, Compton CC, Rosenberg AE. Gastrointestinal stromal tumor versus intra-abdominal fibromatosis of the bowel wall: A clinically important differential diagnosis. Am J Surg Pathol 24: , Hornick JL, Fletcher CDM. Immunohistochemical staining for KIT (CD117) in soft tissue sarcomas is very limited in distribution. Am J Clin Pathol 117: , Lucas DR, al-abbadi M, Tabaczka P, Hamre MR, Weaver DW, Mott MJ. c-kit expression in desmoid fibromatosis: Comparative immunohistochemical evaluation of two commercial antibodies. Am J Clin Pathol 119: , Mace J, Sybil Biermann J, Sondak V, McGinn C, Hayes C, Thomas D, Baker L. Response of extraabdominal desmoid tumors to therapy with imatinib mesylate. Cancer 95: , Ma Y, Zeng S, Metcalfe DD, Akin C, Dimitrijevic S, Butterfield JH, McMahon G, Longley BJ. The c-kit mutation causing human mastocytosis is resistant to STI571 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: , Tian Q, Frierson HF Jr, Krystal GW, Moskaluk CA. Activating c-kit gene mutations in human germ cell tumors. Am J Pathol 154: , 1999
5 Significance of KIT (CD117) in GISTs Hornick and Fletcher Heinrich MC, Corless CL, Duensing A, McGreevey L, Chen CJ, Joseph N, Singer S, Griffith DJ, Haley A, Town A, Demetri GD, Fletcher CD, Fletcher JA. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299: , Hirota S, Ohashi A, Nishida T, Isozaki K, Kinoshita K, Shinomura Y, Kitamura Y. Gain-of-function mutations of platelet-derived growth factor receptor alpha gene in gastrointestinal stromal tumors. Gastroenterology 125: , Heinrich MC, Corless CL, Demetri GD, Blanke CD, von Mehren M, Joensuu H, McGreevey LS, Chen C-J, Van den Abbeele AD, Druker BJ, Kiese B, Eisenberg B, Roberts PJ, Singer S, Fletcher CDM, Silberman S, Simitrijevic S, Fletcher JA. Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J Clin Oncol 21: , Medeiros F, Corless C, Duensing A, Mornick JL, Oliveira AM, Heinrich MC, Fletcher JA, Fletcher CAM. KIT-negative gastrointestinal stromal tumors: Proof of concept and therapeutic implications. Am J Surg Pathol 2004, in press
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