Role of chemotherapy and the receptor tyrosine kinases KIT, PDGFRα, PDGFRβ, and Met in large-cell neuroendocrine carcinoma of the lung

Journal of Clinical Oncology

Volumn 23, Issue 34, 2005, Pages 8774-8785

  Rossi, Giulio ^a   Cavazza, Alberto ^a   Marchioni, Alessandro ^a   Longo, Lucia ^a   Migaldi, Mario ^a   Sartori, Giuliana ^a   Bigiani, Nazzarena ^a   Schirosi, Laura ^a   Casali, Christian ^a   Morandi, Uliano ^a   Facciolongo, Nicola ^a   Maiorana, Antonio ^a   Bavieri, Mario ^a   Fabbri, Leonardo M ^a   Brambilla, Elisabeth ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ETOPOSIDE; GEMCITABINE; NAVELBINE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATINUM; PROTEIN TYROSINE KINASE; SCATTER FACTOR RECEPTOR; STEM CELL FACTOR RECEPTOR; TAXANE DERIVATIVE; ANTINEOPLASTIC AGENT; CARBOPLATIN; CISPLATIN; DEOXYCYTIDINE; DRUG DERIVATIVE; PACLITAXEL;

ADULT; AGED; ARTICLE; CANCER ADJUVANT THERAPY; CANCER CHEMOTHERAPY; CANCER STAGING; CANCER SURVIVAL; CLINICAL FEATURE; DRUG EFFICACY; EXON; FEMALE; GENE MUTATION; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; LARGE CELL CARCINOMA; LUNG SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; METASTASIS; MUTATIONAL ANALYSIS; NEUROENDOCRINE TUMOR; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TUMOR VOLUME; BIOSYNTHESIS; CARCINOMA; COMPARATIVE STUDY; ENZYMOLOGY; FOLLOW UP; GENETICS; LUNG TUMOR; MIDDLE AGED; MORTALITY; MULTIVARIATE ANALYSIS; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SMALL CELL CARCINOMA; SURVIVAL; SURVIVAL RATE; TREATMENT OUTCOME;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARBOPLATIN; CARCINOMA, LARGE CELL; CARCINOMA, NEUROENDOCRINE; CARCINOMA, SMALL CELL; CISPLATIN; DEOXYCYTIDINE; DNA MUTATIONAL ANALYSIS; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM STAGING; PACLITAXEL; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-KIT; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SURVIVAL ANALYSIS; SURVIVAL RATE; TREATMENT OUTCOME;

EID: 33644840322     PISSN: 0732183X     EISSN: None     Source Type: Journal    
DOI: 10.1200/JCO.2005.02.8233     Document Type: Article

References (95)

1. Travis WD, Linnoila IR, Tsokos MG, et al: Neuroendocrine tumors of the lung with proposed criteria for large-cell neuroendocrine carcinoma: An ultrastructural, immunohistochemical, and flow cytometric study of 35 cases. Am J Surg Pathol 15:529-553, 1991
2. Cerilli LA, Ritter JH, Mills SE, et al: Neuroendocrine neoplasms of the lung. Am J Clin Pathol 116:565-596, 2001 (suppl 1)
3. Colby TV, Koss MN, Travis WD: Small cell carcinoma and large cell neuroendocrine carcinoma, in Atlas of Tumor Pathology: Tumors of the Lower Respiratory Tract (series 3). Washington, DC, Armed Forces Institute of Pathology, 1995 pp 235-257
4. Travis WD, Brambilla E, Muller-Hermelink HK, et al: (eds): Tumours of the Lung, Pleura, Thymus and Heart: Pathology and Genetics. World Health Organization Classification of Tumours. Lyon, France, International Agency for Research on Cancer Press, 2004
5. Wick MR, Berg LC, Hertz MI: Large cell carcinoma of the lung with neuroendocrine differentiation: A comparison with large cell "undifferentiated" pulmonary tumors. Am J Clin Pathol 97:796-805, 1992
6. Travis WD, Rush W, Flieder DB, et al: Survival analysis of 200 pulmonary neuroendocrine tumors with clarification of criteria for atypical carcinoid and its separation from typical carcinoid. Am J Surg Pathol 22:934-944, 1998
7. Dresler CM, Ritter JH, Patterson AG, et al: Clinical-pathologic analysis of 40 patients with large cell neuroendocrine carcinoma of the lung. Ann Thorac Surg 63:180-185, 1997
8. Jiang SX, Kameya T, Shoji M, et al: Large cell neuroendocrine carcinoma of the lung: A histologic and immunohistochemical study of 22 cases. Am J Surg Pathol 22:526-537, 1998
9. Garcia-Yuste M, Matilla JM, Alvarez-Gago T, et al: Prognostic factors in neuroendocrine lung tumors: A Spanish multicenter study. Ann Thorac Surg 70:258-263, 2000
10. Jung KJ, Lee KS, Han J, et al: Large cell neuroendocrine carcinoma of the lung: Clinical, CT, and pathologic findings in 11 patients. J Thorac Imaging 16:156-162, 2001
11. Takei H, Asamura H, Maeshima A, et al: Large cell neuroendocrine carcinoma of the lung: A clinicopathologic study of eighty-seven cases. J Thorac Cardiovasc Surg 124:285-292, 2002
12. Mazieres J, Daste G, Molinier L, et al: Large cell neuroendocrine carcinoma of the lung: Pathological study and clinical outcome of 18 resected cases. Lung Cancer 37:287-292, 2002
13. Iyoda A, Hiroshima K, Baba M, et al: Pulmonary large cell carcinomas with neuroendocrine features are high-grade neuroendocrine tumors. Ann Thorac Surg 73:1049-1054, 2002
14. Hage R, Seldenrijk K, de Bruin P, et al: Pulmonary large-cell neuroendocrine carcinoma (LCNEC). Eur J Cardiothorac Surg 23:457-460, 2003
15. Paci M, Cavazza A, Annessi V, et al: Large cell neuroendocrine carcinoma of the lung: A 10-year clinicopathologic retrospective study. Ann Thorac Surg 77:1163-1167, 2004
16. Battafarano RJ, Fernandez FG, Ritter J, et al: Large cell neuroendocrine carcinoma: An aggressive form of non-small cell lung cancer. J Thorac Cardiovasc Surg 130:166-172, 2005
17. Zacharias J, Nicholson AG, Ladas GP, et al: Large cell neuroendocrine carcinoma and large cell carcinomas with neuroendocrine morphology of the lung: Prognosis after complete resection and systematic nodal dissection. Ann Thorac Surg 75:348-352, 2003
18. Doddoli C, Barlesi F, Chetaille B, et al: Large cell neuroendocrine carcinoma of the lung: An aggressive disease potentially treatable with surgery. Ann Thorac Surg 77:1168-1172, 2004
19. Travis WD, Gal AA, Colby TV, et al: Reproducibility of neuroendocrine lung tumor classification. Hum Pathol 29:272-279, 1998
20. Marchevsky AM, Gal AA, Shah S, et al: Morphometry confirms the presence of considerable nuclear size overlap between "small cells" and "large cells" in high-grade pulmonary neuroendocrine neoplasms. Am J Clin Pathol 116:466-472, 2001
21. Sturm N, Rossi G, Lantuejoul S, et al: Expression of thyroid transcription factor-1 in the spectrum of neuroendocrine cell proliferations with special interest in carcinoids. Hum Pathol 33:175-182, 2002
22. Sturm N, Rossi G, Lantuejoul S, et al: 34betaE12 expression along the whole spectrum of neuroendocrine proliferations of the lung, from neuroendocrine cell hyperplasia to small cell carcinoma. Histopathology 42:156-166, 2003
23. Rusch VW, Klimstra DS, Venkatraman ES: Molecular markers help characterize neuroendocrine lung tumors. Ann Thorac Surg 62:798-810, 1996
24. Przygodzki RM, Finkelstein SD, Langer JC, et al: Analysis of p53, K-ras-2, and C-raf-1 in pulmonary neuroendocrine tumors: Correlation with histologie subtype and clinical outcome. Am J Pathol 148:1531-1541, 1996
25. Brambilla E, Negoescu A, Gazzeri S, et al: Apoptosis-related factors p53, Bcl2 and Bax in neuroendocrine lung tumors. Am J Pathol 149:1941-1952, 1996
26. Barbareschi M, Girlando S, Mauri FA, et al: Humour suppressor gene products, proliferation, and differentiation markers in lung neuroendocrine neoplasms. J Pathol 166:343-350, 1992
27. Cagle PT, El-Naggar AK, Xu HJ, et al: Differential retinoblastoma protein expression in neuroendocrine tumors of the lung. Am J Pathol 150:393-400, 1997
28. Gouyer V, Gazzeri S, Bolon I, et al: Mechanism of retinoblastoma gene inactivation in the spectrum of neuroendocrine lung tumors. Am J Respir Cell Mol Biol 18:188-196, 1998
29. Jiang SX, Kameya T, Shinada J, et al: The significance of frequent and independent p53 and bcl-2 expression in large-cell neuroendocrine carcinomas of the lung. Mod Pathol 12:362-369, 1999
30. Jiang SX, Kameya T, Sato Y, et al: Bcl-2 protein expression in lung cancer and close correlation with neuroendocrine differentiation. Am J Pathol 148:837-846, 1996
31. Onuki N, Wistuba II, Travis WD, et al: Genetic changes in the spectrum of neuroendocrine lung tumors. Cancer 85:600-607, 1999
32. Michelland S, Gazzeri S, Brambilla E, et al: Comparison of chromosomal imbalances in neuroendocrine and non-small-cell lung carcinomas. Cancer Genet Cytogenet 114:22-30, 1999
33. Gugger M, Burckhardt E, Kappeler A, et al: Quantitative expansion of structural genomic alterations in the spectrum of neuroendocrine lung carcinomas. J Pathol 196:408-415, 2002
34. Iyoda A, Hiroshima K, Moriya Y, et al: Pulmonary large cell neuroendocrine carcinoma demonstrates high proliferative activity. Ann Thorac Surg 77:1891-1895, 2004
35. Hiroshima K, Iyoda A, Shibuya K, et al: Genetic alterations in early-stage pulmonary large cell neuroendocrine carcinoma. Cancer 100:1190-1198, 2004
36. Welborn J, Jenks H, Taplett J, et al: High-grade neuroendocrine carcinomas display unique cytogenetic aberrations. Cancer Genet Cytogenet 155:33-41, 2004
37. Beasley MB, Lantuejoul S, Abbondanzo S, et al: The p16/cyclin D1/Rb pathway in neuroendocrine tumors of the lung. Hum Pathol 34:136-142, 2003
38. Araki K, Ishii G, Yokose T, et al: Frequent overexpression of the c-kit protein in large cell neuroendocrine carcinoma of the lung. Lung Cancer 40:173-180, 2003
39. Pelosi G, Fasullo M, Leon ME, et al: CD117 immunoreactivity in high-grade neuroendocrine tumors of the lung: A comparative study of 39 large-cell neuroendocrine carcinomas and 27 surgically resected small-cell carcinomas. Virchows Arch 445:449-455, 2004
40. Rossi G, Cavazza A, Marchioni A, et al: Kit expression in small cell carcinomas of the lung: Effects of chemotherapy. Mod Pathol 16:1041-1047, 2003
41. Casali C, Stefani A, Rossi G, et al: The prognostic role of c-kit expression in resected large cell neuroendocrine carcinomas of the lung. Ann Thorac Surg 77:247-253, 2004
42. Fletcher JA: Role of KIT and Platelet-derived growth factor receptors as oncoproteins. Semin Oncol 31:4-11, 2004 (suppl 6)
43. Hibi K, Takahashi T, Sekido Y, et al: Coexpression of stem cell factor and the c-kit genes in small-cell lung cancer. Oncogene 6:2291-2296, 1991
44. Rygaard K, Nakamura T, Spang-Thomsen M: Expression of the proto-oncogene c-met and c-kit and their ligands, hepatocyte growth factor/ scatter factor and stem cell factor in SCLC cell lines and xenografts. Br J Cancer 67:37-46, 1993
45. Krystal GW, Mines SJ, Organ CP: Autocrine growth of small cell lung cancer mediated by coexpression of c-kit and stem cell factor. Cancer Res 56:370-376, 1996
46. Blume-Jensen P, Hunter T: Oncogenic kinase signalling. Nature 411:355-365, 2001
47. Heldin CH, Ostman A, Ronnstrand L: Signal transduction via platelet-derived growth factor receptors. Biochim Biochim Biophys Acta 1378:F79-F113, 1998
48. Maulik G, Shrikhande A, Kijima T, et al: Role of the hepatocyte growth factor receptor, c-Met, in the oncogenesis and potential for therapeutic inhibition. Cytokine Growth Factor Rev 13:41-59, 2002
49. Ma PC, Maulik G, Christensen J, et al: C-Met: Structure, functions and potential for therapeutic inhibition. Cancer Metastasis Rev 22:309-325, 2003
50. Trusolino L, Comoglio PM: Scatter-factor and semaphorin receptors: Cell signalling for invasive growth. Nat Rev 2:289-300, 2002
51. Forgacs E, Zochbauer-Muller S, Olah E, et al: Molecular genetic abnormalities in the pathogenesis of human lung cancer. Pathol Oncol Res 7:6-13, 2001
52. Schrump DS, Nguyen DM: Targets for molecular intervention in multistep pulmonary carcinogenesis. World J Surg 25:174-183, 2001
53. Fong KM, Minna JD: Molecular biology of lung cancer: Clinical implications. Clin Chest Med 23:83-100, 2002
54. Wang WL, Healy ME, Sattler M, et al: Growth inhibition and modulation of kinase pathways on small cell lung cancer cell lines by the novel tyrosine kinase inhibitor STI571. Oncogene 19:3521-3528, 2000
55. Krystal GW, Honsawek S, Litz J, et al: The selective tyrosine kinase inhibitor STI571 inhibits small cell lung cancer growth. Clin Cancer Res 6:3319-3326, 2000
56. Krystal GW, Honsawek S, Kiewlich D, et al: Indolinone tyrosine kinase inhibitors block Kit activation and growth of small cell lung cancer cells. Cancer Res 61:3660-3668, 2001
57. Maulik G, Kijima T, Ma PC, et al: Modulation of the c-met/hepatocyte growth factor pathway in small cell lung cancer. Clin Cancer Res 8:620-627, 2002
58. Abrams TJ, Lee LB, Murray LJ, et al: SU 11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol Cancer Ther 2:471-478, 2003
59. Buchdunger E, Cioffi CL, Law N, et al: 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, 2000
60. Bondzi C, Litz J, Dent P, et al: Src family kinase activity is required for Kit-mediated mitogen-activated protein (MAP) kinase activation, however loss of functional retinoblastoma protein makes MAP kinase activation unnecessary for growth of small cell lung cancer cells. Cell Growth Differ 11:305-314, 2000
61. WHO: The World Health Organization histological typing of lung tumours: Second Edition. Am J Clin Pathol 77:123-136, 1982
62. Greene FL, Page DL, Fleming ID, et al: (eds): AJCC Cancer Staging Manual (ed 6). New York, NY, Springer-Verlag, 2002
63. Miller VA, Kris MG, Shah N, et al: Bronchioloalveolar pathologic subtype and smoking history predict sensitivity to gefitinib in advanced non-small cell lung cancer. J Clin Oncol 22:1103-1109, 2004
64. Harada M, Yokose T, Yoshida J, et al: Immunohistochemical neuroendocrine differentiation is an independent prognostic factor in surgically resected large cell carcinoma of the lung. Lung Cancer 38:177-184, 2002
65. Pelosi G, Pasini F, Sonzogni A, et al: Prognostic implications of neuroendocrine differentiation and hormone production in patients with stage I nonsmall cell lung carcinoma. Cancer 97:2487-2497, 2003
66. Yamazaki S, Sekine I, Matsuno Y, et al: Clinical responses of large cell neuroendocrine carcinoma of the lung to cisplatin-based chemotherapy. Lung Cancer 49:217-223, 2005
67. Filosso PL, Ruffini E, Oliaro A, et al: Large-cell neuroendocrine carcinoma of the lung: A clinicopathologic study of eighteen cases and the efficacy of adjuvant treatment with octreotide. J Thorac Cardiovasc Surg 129:819-824, 2005
68. Shepherd FA, Ginsberg R, Patterson GA, et al: Is there ever a role for salvage operations in limited small-cell lung cancer? J Thorac Cardiovasc Surg 101:196-200, 1991
69. Jones MH, Virtanen C, Honjoh D, et al: Two prognostically significant subtypes of high-grade lung neuroendocrine tumours independent of small-cell and large-cell neuroendocrine carcinomas identified by gene expression profiles. Lancet 363:775-781, 2004
70. Bhattacharjee A, Richards WG, Staunton J, et al: Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 98:13790-13795, 2001
71. Garber ME, Troyanskaya OG, Schluens K, et al: Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci U S A 98:13784-13789, 2001
72. Chua YJ, Steer C, Yip D: Recent advances in management of small cell lung cancer. Cancer Treat Rev 30:521-543, 2004
73. Pfister DG, Johnson DH, Azzoli CG, et al: American Society of Clinical Oncology treatment of unresectable non-small-cell lung cancer guideline: Update 2003. J Clin Oncol 22:330-353, 2004
74. Iyoda A, Hiroshima K, Toyozaki T, et al: Adjuvant chemotherapy for large cell carcinoma with neuroendocrine features. Cancer 92:1108-1112, 2001
75. Kozuky T, Fujimoto N, Ueoka H, et al: Complexity in the treatment of pulmonary large cell neuroendocrine carcinoma. J Cancer Res Clin Oncol 131:147-151, 2005
76. The International Adjuvant Lung Cancer Trial Collaborative Group: Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small cell lung cancer. N Engl J Med 350:351-360, 2004
77. Strauss GM, Herndon J, Maddaus MA, et al: Randomized clinical trial of adjuvant chemotherapy with paclitaxel and carboplatin following resection in stage IB non-small cell lung cancer (NSCLC): Report of Cancer and Leukemia Group B (CALGB) protocol 9633. J Clin Oncol 22:621s, 2004 (suppl 14, abstr 7019)
78. Winton T, Livingston R, Johnson D, et al: Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 352:2589-2597, 2005
79. Dy GK, Adjei AA: Novel targets for lung cancer therapy: Part I. J Clin Oncol 20:2881-2894, 2002
80. Sattler M, Salgia R: Molecular and cellular biology of small cell lung cancer. Semin Oncol 30:57-71, 2003
81. Tamborini E, Bonadiman L, Negri T, et al: Detection of overexpression and phosphorylation wild-type Kit receptor in surgical specimens of small cell lung cancer. Clin Cancer Res 10:8214-8219, 2004
82. Savage DG, Amman KH: Imatinib mesylate: A new oral targeted therapy. N Engl J Med 346:683-693, 2002
83. Johnson BE, Fisher T, Fisher B, et al: Phase II study of imatinib in patients with small cell lung cancer. Clin Cancer Res 9:5880-5887, 2003
84. Heinrich MC: Is KIT an important therapeutic target in small cell lung cancer? Clin Cancer Res 9:5825-5828, 2003
85. Murray N, Salgia R, Fossella FV: Targeted molecules in small cell lung cancer. Semin Oncol 31:106-111, 2004 (suppl 1)
86. Antoniades HN, Galanopoulos T, Neville-Golden J, et al: Malignant epithelial cells in primary human lung carcinomas coexpress in vivo platelet-derived growth factor (PDGF) and PDGF receptor mRNAs and their protein products. Proc Natl Acad Sci U S A 89:3942-3946, 1992
87. Kawai T, Hiroi S, Torikata C: Expression in lung carcinomas of platelet-derived growth factor and its receptors. Lab Invest 77:431-436, 1997
88. Harvey P, Warn A, Newman P, et al: Immunoreactivity for hepatocyte growth factor/ scatter factor and its receptor, met, in human lung carcinomas and malignant mesotheliomas. J Pathol 180:389-394, 1996
89. Masuya D, Huang C, Liu D, et al: The tumour-stromal interaction between intratumoral c-Met and stromal hepatocyte growth factor associated with tumour growth and prognosis in non-small cell lung cancer patients. Br J Cancer 90:1555-1562, 2004
90. Christensen JG, Schreck R, Burrows J, et al: A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo. Cancer Res 63:7345-7355, 2003
91. Ma PC, Kijima T, Maulik G, et al: C-MET mutational analysis in small cell lung cancer: Novel juxtamembrane domain mutations regulating cytoskeletal functions. Cancer Res 63:6272-6281, 2003
92. Lantuejoul S, Moro D, Michalides RJ, et al: Neural cell adhesion molecules (NCAM) and NCAM-PSA expression in neuroendocrine lung tumors. Am J Surg Pathol 22:1267-1276, 1998
93. Rossi G, Marchioni A, Milani M, et al: TTF-1, cytokeratin 7, 34beta E12, and CD56/ NCAM immunostaining in the subclassification of large cell carcinomas of the lung. Am J Clin Pathol 122:884-893, 2004
94. Kaufmann O, Georgi T, Dietel M: Utility of 123C3 monoclonal antibody against CD56 (NCAM) for the diagnosis of small cell carcinomas on paraffin sections. Hum Pathol 28:1373-1378, 1997
95. Fossella FV, Tolcher A, Elliott M, et al: Phase I trial of the monoclonal antibody conjugate, BB-10901, for relapsed/refractory small cell cancer (SCUC) and other neuroendocrine (NE) tumors. Proc Am Soc Clin Oncol 21:309a, 2002 (abstr 1232)