A subset of lung adenocarcinomas and atypical adenomatous hyperplasia-associated foci are genotypically related: An EGFR, HER2, and K-ras mutational analysis

American Journal of Clinical Pathology

Volumn 129, Issue 2, 2008, Pages 202-210

  Sartori, Giuliana ^a   Cavazza, Alberto ^d   Bertolini, Federica ^a   Longo, Lucia ^b   Marchioni, Alessandro ^c   Costantini, Matteo ^a   Barbieri, Fausto ^a   Migaldi, Mario ^a   Rossi, Giulio ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b Ramazzini Hospital   (Italy)

^c Civic Hospital of Mirandola   (Italy)

^d Operative Unit of Pathologic Anatomy   (Italy)

Author keywords

Adenocarcinoma; Atypical adenomatous hyperplasia; EGFR; Epidermal growth factor receptor; HER2; K ras; Lung

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; K RAS PROTEIN;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CODON; EXON; FEMALE; GENE MUTATION; GENE SEQUENCE; GENOTYPE; HUMAN; HUMAN TISSUE; LUNG ADENOCARCINOMA; LUNG ADENOMA; LUNG CARCINOGENESIS; MALE; MUTATIONAL ANALYSIS; ONCOGENE K RAS; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SMOKING; WILD TYPE; ADENOCARCINOMA; COMPARATIVE STUDY; GENETICS; HYPERPLASIA; LUNG TUMOR; MIDDLE AGED; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; ONCOGENE RAS; PRECANCER; PROTO ONCOGENE;

ADENOCARCINOMA; ADENOMATOSIS, PULMONARY; ADULT; AGED; BASE SEQUENCE; DNA MUTATIONAL ANALYSIS; FEMALE; GENES, ERBB-2; GENES, RAS; HUMANS; HYPERPLASIA; LUNG NEOPLASMS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PRECANCEROUS CONDITIONS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 40449103502     PISSN: 00029173     EISSN: None     Source Type: Journal    
DOI: 10.1309/THU13F3JRJVWLM30     Document Type: Article

References (83)

1. Travis WD, Brambilla E, Muller-Hermelink HK, et al, eds. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. Lyon, France: IARC Press; 2004. World Health Organization Classification of Tumours.
2. Kerr KM. Pulmonary preinvasive neoplasia. J Clin Pathol. 2001;54:257-271.
3. Kerr KM. Morphology and genetics of pre-invasive pulmonary disease. Curr Diagn Pathol. 2004;10:259-268.
4. Colby T V, Wistuba II, Gazdar A F. Precursors to pulmonary neoplasia. Adv Anat Pathol. 1998;4:205-215.
5. Lopez JI, Colby T V, Gazdar A F. Current status of small peripheral adenocarcinomas of the lung and their importance to pathologists. Ann Diagn Pathol. 2005;9:115-122.
6. Park CM, Goo JM, Lee HJ, et al. CT findings of atypical adenomatous hyperplasia in the lung. Korean J Radiol. 2006;7:80-86.
7. Kerr KM, Carey FA, King G, et al. Atypical alveolar hyperplasia: relationship with pulmonary adenocarcinoma, p53, and cerbB2 expression. J Pathol. 1994;174:249-256.
8. Westra WH, Baas IO, Hruban RH, et al. K-ras oncogene activation in atypical alveolar hyperplasias of the human lung. Cancer Res. 1996;56:2224-2228.
9. Mori M, Tezuka F, Chiba R, et al. Atypical adenomatous hyperplasia and adenocarcinoma of the human lung: their heterology in form and analogy in immunohistochemical characteristics. Cancer. 1996;77:665-674.
10. Kitamura H, Kameda Y, Ito T, et al. Cytodifferentiation of atypical adenomatous hyperplasia and bronchioloalveolar lung carcinoma: immunohistochemical and ultrastructural studies. Virchows Arch. 1997;431:415-424.
11. Kurasono Y, Ito T, Kameda Y, et al. Expression of cyclin D1, retinoblastoma gene protein, and p16MTS1 protein in atypical adenomatous hyperplasia and adenocarcinoma of the lung: an immunohistochemical analysis. Virchows Arch. 1998;432:207-215.
12. Slebos RJ, Baas IO, Clement MJ, et al. p53 alterations in atypical alveolar hyperplasia of the human lung. Hum Pathol. 1998;29:801-808.
13. Niho S, Yokose T, Suzuki K, et al. Monoclonality of atypical adenomatous hyperplasias of the lung. Am J Pathol. 1999;154:249-254.
14. Kitamura H, Kameda Y, Ito T, et al. Atypical adenomatous hyperplasia of the lung; implications for the pathogenesis of peripheral lung adenocarcinoma. Am J Clin Pathol. 1999;111:610-622.
15. Chapman AD, Kerr KM. The association between atypical adenomatous hyperplasia and primary lung cancer. Br J Cancer. 2000;83:632-636.
16. Yamasaki M, Takeshima Y, Fujii S, et al. Correlation between genetic alterations and histopathological subtypes in bronchiolo-alveolar carcinoma and atypical adenomatous hyperplasia of the lung. Pathol Int. 2000;50:778-785.
17. Yamasaki M, Takeshima Y, Fujii S, et al. Correlation between morphological heterogeneity and genetic alteration within one tumor in adenocarcinomas of the lung. Pathol Int. 2000;50:891-896.
18. Takamochi K, Ogura T, Suzuki K, et al. Loss of heterozygosity on chromosome 9q and 16p in atypical adenomatous hyperplasia concomitant with adenocarcinoma of the lung. Am J Pathol. 2001;159:1941-1948.
19. Kayser K, Nwoye JO, Kosjerina Z, et al. Atypical adenomatous hyperplasia of lung: its incidence and analysis of clinical, glycohistochemical and structural features including newly defined growth regulators and vascularization. Lung Cancer. 2003;42:171-182.
20. Kawai T, Hiroi S, Nakanishi K, et al. Telomere length and telomerase expression in atypical adenomatous hyperplasia and small bronchioloalveolar carcinoma of the lung. Am J Clin Pathol. 2007;127:254-262.
21. Nakanishi K, Matsuo H, Kanai Y, et al. LAT1 expression in normal lung and in atypical adenomatous hyperplasia and adenocarcinoma of the lung. Virchows Arch. 2006;448:142-150.
22. Sano T, Kitayama Y, Igarashi H, et al. Chromosomal numerical abnormalities in early stage lung adenocarcinoma. Pathol Int. 2006;56:117-125.
23. Morandi L, Asioli S, Cavazza A, et al. Genetic relationship among atypical adenomatous hyperplasia, bronchioloalveolar carcinoma and adenocarcinoma of the lung. Lung Cancer. 2007;56:35-42.
24. Tomida S, Yatabe Y, Yanagisawa K, et al. Throwing new light on lung cancer pathogenesis: updates on three recent topics. Cancer Sci. 2005;96:63-68.
25. Fukuoka M, Yano S, Giaccone G, et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small cell lung cancer (the IDEAL 1 trial) [published correction appears in J Clin Oncol. 2004;22:4811]. J Clin Oncol. 2003;21:2237-2246.
26. Kris MG, Natale RB, Herbst RS, et al. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA. 2003;290:2149-2158.
27. Shepherd FA, Rodrigues PJ, Ciuleanu T, et al. Erlotinib in previously treated non-small cell lung cancer. N Engl J Med. 2005;353:123-132.
28. Sridhar SS, Seymour L, Shepherd FA. Inhibitors of EGFRs: a review of clinical research with a focus on non-small cell lung cancer. Lancet Oncol. 2003;4:397-406.
29. Prudkin L, Wistuba II. EGFR abnormalities in lung cancer: pathogenetic and clinical implications. Ann Diagn Pathol. 2006;10:306-315.
30. Pao W, Miller VA. EGFR mutations, small-molecule kinase inhibitors, and non-small cell lung cancer: current knowledge and future directions. J Clin Oncol. 2005;23:2556-2568.
31. Yatabe Y, Mitsudomi T. Epidermal growth factor receptor mutations in lung cancer. Pathol Int. 2007;57:233-244.
32. 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. 2004;22:1103-1109.
33. Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350:2129-2139.
34. Paez JG, Janne PA, Lee J, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004;304:1497-1500.
35. Pao W, Miller VA, Zakowski M, et al. EGFR gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A. 2004;101:13306-13311.
36. Dowell JE, Caplan NM, Palmer BF. EGFR mutations in non-small cell lung cancer: a basic science discovery with immediate clinical impact. Am J Med Sci. 2006;331:139-149.
37. Mitsudomi T, Kosaka T, Yatabe Y. Biological and clinical implications of EGFR mutations in lung cancer. Int J Clin Oncol. 2006;11:190-198.
38. Taron M, Ichinose Y, Rosell R, et al. Activating mutations in the tyrosine kinase domain of the EGFR are associated with improved survival in gefitinib-treated chemorefractory lung adenocarcinoma. Clin Cancer Res. 2005;11:5878-5885.
39. Johnson BE, Jänne PA. Epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Cancer Res. 2005;65:7525-7529.
40. Chan SK, Gullick WJ, Hill ME. Mutations of the EGFR in non-small cell lung cancer: search and destroy. Eur J Cancer. 2006;42:17-23.
41. Murray S, Timotheadou E, Linardou H, et al. Mutations of the EGFR tyrosine kinase domain and associations with clinicopathologic features in non-small cell lung cancer patients. Lung Cancer. 2006;52:225-233.
42. Shigematsu H, Kin L, Takahashi T, et al. Clinical and biological features associated with EGFR gene mutations in lung cancers. J Natl Cancer Inst. 2005;97:339-346.
43. Gazdar A F, Shigematsu H, Herz J, et al. Mutations and addiction to EGFR: the Achilles "heal" of lung cancers? Trends Mol Med. 2004;10:481-486.
44. Riely GJ, Pao W, Pham DK, et al. Clinical course of patients with non-small cell lung cancer and EGFR exon 19 and exon 21 mutations treated with gefitinib or erlotinib. Clin Cancer Res. 2006;12:839-844.
45. Sequist LV, Joshi VA, Janne PA, et al. Epidermal growth factor receptor mutation testing in the care of lung cancer patients. Clin Cancer Res. 2006;12(14 pt 2):4403s-4408s.
46. Pao W, Wang TY, Riely GJ, et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med. 2005;2:e17. doi:10.1371/journal.pmed.0020017.
47. Eberhard DA, Johnson BE, Amler LC, et al. Mutations in the EGFR and in KRAS are predictive and prognostic indicators in patients with NSCLC treated with chemotherapy alone or in combination with erlotinib. J Clin Oncol. 2005;23:5900-5909.
48. Tam IY, Chung L P, Suen WS, et al. Distinct epidermal growth factor receptor and KRAS mutation patterns in non-small-cell lung cancer patients with different tobacco exposure and clinicopathologic features. Clin Cancer Res. 2006;12:1647-1653.
49. Han SW, Kim TY, Jeon YK, et al. Optimization of patient selection for gefitinib in non-small-cell lung cancer by combined analysis of epidermal growth factor receptor mutation, K-ras mutation, and Akt phosphorylation. Clin Cancer Res. 2006;12:2538-2544.
50. Stephens P, Hunter C, Bignell G, et al. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature. 2004;431:525-526.
51. Shigematsu H, Takahashi T, Nomura M, et al. Somatic mutations of the HER2 kinase domain in lung adenocarcinomas. Cancer Res. 2005;65:1642-1646.
52. Buttitta F, Barassi F, Fresu G, et al. Mutational analysis of the HER2 gene in lung tumors from Caucasian patients: mutations are mainly present in adenocarcinomas with bronchioloalveolar features. Int J Cancer. 2006;119:2586-2591.
53. Shimosato Y, Kodama T, Kameya T. Morphogenesis of peripheral type adenocarcinoma of the lung. In: Shimosato Y, Melamed MR, Nettesheim P, eds. Morphogenesis of Lung Cancer. Boca Raton, FL: CRC Press; 1982.
54. Kodama T, Biyajima S, Watanabe S, et al. Morphometric study of adenocarcinomas and hyperplastic epithelial lesions in the peripheral lung. Am J Clin Pathol. 1986;85:146-151.
55. Weng SY, Tsuchiya E, Kasuga T, et al. Incidence of atypical bronchioloalveolar cell hyperplasia of the lung: relation to histological subtypes of lung cancer. Virchows Arch. 1992;420:463-471.
56. Carey FA, Wallace WAH, Fergusson RJ, et al. Alveolar atypical adenomatous hyperplasia in association with primary pulmonary adenocarcinoma: a clinicopathological study of 10 cases. Thorax. 1992;47:1041-1043.
57. Colby T V, Koss M, Travis WD. Tumors of the Lower Respiratory Tract. Washington, DC: Armed Forces Institute of Pathology; 1995. Atlas of Tumor Pathology; Third series, Fascicle 13.
58. Suzuki K, Nagai K, Yoshida J, et al. The prognosis of resected lung carcinoma associated with atypical adenomatous hyperplasia: a comparison of the prognosis of well-differentiated adenocarcinoma associated with atypical adenomatous hyperplasia and intrapulmonary metastasis. Cancer. 1997;79:1521-1526.
59. Takigawa N, Segawa Y, Nakata M, et al. Clinical investigation of atypical adenomatous hyperplasia of the lung. Lung Cancer. 1999;25:115-121.
60. Mori M, Rao SK, Popper HH, et al. Atypical adenomatous hyperplasia of the lung: a probable forerunner in the development of adenocarcinoma of the lung. Mod Pathol. 2001;14:72-84.
61. Greenberg AK, Yee H, Rom WN. Preneoplastic lesions of the lung. Respir Res. 2002;3:20-30.
62. Ohshima S, Shimizu Y, Takahama M. Detection of c-Ki-ras gene mutation in paraffin sections of adenocarcinoma and atypical bronchioloalveolar cell hyperplasia of human lung. Virchows Arch. 1994;424:129-134.
63. Cooper CA, Carby FA, Bubb VJ, et al. The pattern of K-ras mutation in pulmonary adenocarcinoma defines a new pathway of tumour development in the human lung. J Pathol. 1997;181:401-404.
64. Ullman R, Bongiovanni M, Halbwedl I, et al. Is high-grade adenomatous hyperplasia an early bronchioloalveolar carcinoma? J Pathol. 2003;201:371-376.
65. Marchetti A, Martella C, Felicioni L, et al. EGFR mutations in non-small-cell lung cancer: analysis of a large series of cases and development of a rapid and sensitive method for diagnostic screening with potential implications on pharmacologic treatment. J Clin Oncol. 2005;23:857-865.
66. Toyooka S, Tokumo M, Shigematsu H, et al. Mutational and epigenetic evidence for independent pathways for lung adenocarcinomas arising in smokers and never smokers. Cancer Res. 2006;66:1371-1375.
67. Yatabe Y, Kosaka T, Takahashi T, et al. EGFR mutation is specific for terminal respiratory unit type adenocarcinoma. Am J Surg Pathol. 2005;29:633-639.
68. Haneda H, Sasaki H, Shimizu S, et al. Epidermal growth factor receptor gene mutation defines distinct subsets among small adenocarcinomas of the lung. Lung Cancer. 2005;52:47-52.
69. Yoshida Y, Shibata T, Kokubu A, et al. Mutations of the epidermal growth factor receptor gene in atypical adenomatous hyperplasia and bronchioloalveolar carcinoma of the lung. Lung Cancer. 2005;50:1-8.
70. Rodenhuis S, Slebos RJC, Evers SG, et al. K-ras oncogene activation on adenocarcinoma of the lung: frequency and possible clinical significance. Cancer Res. 1998;48:5738-5741.
71. Sagawa M, Saito Y, Fujimura S, et al. K-ras point mutation occurs in the early stage of carcinogenesis in lung cancer. Br J Cancer. 1998;77:720-723.
72. Nelson HH, Cristiani DC, Mark EJ, et al. Implications and prognostic value of k-ras mutation for early-stage lung cancer in women. J Natl Cancer Inst. 1999;91:2032-2038.
73. Kim YH, Ishii G, Goto K, et al. Dominant papillary subtype is a significant predictor of the response to gefitinib in adenocarcinoma of the lung. Clin Cancer Res. 2004;10:7311-7317.
74. Silver SA, Askin FB. True papillary carcinoma of the lung: a distinct clinicopathologic entity. Am J Surg Pathol. 1997;21:43-51.
75. Miyoshi T, Satoh Y, Okumura S, et al. Early-stage lung adenocarcinoma with a micropapillary pattern: a distinct pathological marker for a significantly poor prognosis. Am J Surg Pathol. 2003;27:101-109.
76. Aida S, Shimazaki H, Sato M, et al. Prognostic analysis of pulmonary adenocarcinoma subclassification with special consideration of papillary and bronchioloalveolar types. Histopathology. 2004;45:468-476.
77. Costa DB, Schumer ST. Three-year survival in metastatic non-small cell lung cancer treated with gefitinib [letter]. Lung Cancer. 2006;53:123-124.
78. Jian Z, Tomizawa Y, Yanagitani N, et al. Papillary adenocarcinoma of the lung is a more advanced adenocarcinoma than bronchioloalveolar carcinoma that is composed of two distinct histological subtypes. Pathol Int. 2005;55:619-625.
79. Ruiz MI, van Cruijsen H, Smit E F, et al. Genetic heterogeneity in patients with multiple neoplastic lung lesions: a report of three cases. J Thorac Oncol. 2007;2:12-21.
80. Milton D T, Riely GJ, Pao W, et al. Molecular on/off switch. J Clin Oncol. 2006;24:4940-4942.
81. Ryoo BY, Na II, Yang SH, et al. Synchronous multiple primary lung cancers with different responses to gefitinib. Lung Cancer. 2006;53:245-248.
82. Giaccone G, Gallegos Ruiz M, Le Chevalier T, et al. Erlotinib for frontline treatment of advanced non-small cell lung cancer: a phase II study. Clin Cancer Res. 2006;12:6049-6055.
83. Inoue A, Suzuki T, Fukuhara T, et al. Prospective phase II study of gefitinib for chemotherapy-naive patients with advanced non-small cell lung cancer with epidermal growth factor receptor gene mutations. J Clin Oncol. 2006;24:3340-3346.