Pulmonary mucinous adenocarcinomas: architectural patterns in correlation with genetic changes, prognosis and survival

Virchows Archiv

Volumn 467, Issue 6, 2015, Pages 675-686

  Geles, Abidin ^a,d   Gruber Moesenbacher, Ulrike ^b   Quehenberger, Franz ^a   Manzl, Claudia ^c   Al Effah, Mohamed ^a   Grygar, Elisabeth ^a   Juettner Smolle, Freyja ^a   Popper, Helmut H ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b Institute of Pathology Teaching Hospital Feldkirch   (Austria)

^c MEDICAL UNIVERSITY OF INNSBRUCK   (Austria)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Architectural pattern; EML4ALK rearrangement; KRAS mutation; MUC proteins; Mucinous adenocarcinoma; Overall survival; p14; p16

Indexed keywords

CYTOKERATIN 20; CYTOKERATIN 7; EML4ALK PROTEIN; K RAS PROTEIN; MUCIN 1; MUCIN 5AC; PROTEIN; PROTEIN P14; PROTEIN P16; ROS1 PROTEIN; TRANSCRIPTION FACTOR CDX2; TTF1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CODON; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE MUTATION; GENE REARRANGEMENT; GENETIC TRAIT; GOBLET CELL; HUMAN; HUMAN TISSUE; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; MALE; MUTATIONAL ANALYSIS; ONCOGENE K RAS; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PULMONARY MUCINOUS ADENOCARCINOMA;

EID: 84949530272     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-015-1852-2     Document Type: Article

References (47)

1. Carretta A, Canneto B, Calori G, Ceresoli GL, Campagnoli E, Arrigoni G, Vagani A, Zannini P (2001) Evaluation of radiological and pathological prognostic factors in surgically-treated patients with bronchoalveolar carcinoma. Eur J Cardiothorac Surg 20:367–371
2. Chen Y, Thai P, Zhao YH, Ho YS, DeSouza MM, Wu R (2003) Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem 278:17036–17043
3. Copin MC, Buisine MP, Devisme L, Leroy X, Escande F, Gosselin B, Aubert JP, Porchet N (2001) Normal respiratory mucosa, precursor lesions and lung carcinomas: differential expression of human mucin genes. Front Biosci 6:D1264–D1275
4. Dabbagh K, Takeyama K, Lee HM, Ueki IF, Lausier JA, Nadel JA (1999) IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo. J Immunol 162:6233–6237
5. Dacic S, Shuai Y, Yousem S, Ohori P, Nikiforova M (2010) Clinicopathological predictors of EGFR/KRAS mutational status in primary lung adenocarcinomas. Mod Pathol 23:159–168
6. Dammrich J, Vollmers H, Silber R, Buchwald J, Papadopoulos T, Mullerhermelink H (1997) Postoperative prognosis of pulmonary adenocarcinoma subtypes correlates with HLA-DR expression and the number of tumor-infiltrating cells. Oncol Rep 4:59–64
7. Grabner B, Schramek D, Mueller KM, Moll HP, Svinka J, Hoffmann T, Bauer E, Blaas L, Hruschka N, Zboray K, Stiedl P, Nivarthi H, Bogner E, Gruber W, Mohr T, Zwick RH, Kenner L, Poli V, Aberger F, Stoiber D, Egger G, Esterbauer H, Zuber J, Moriggl R, Eferl R, Gyorffy B, Penninger JM, Popper H, Casanova E (2015) Disruption of STAT3 signalling promotes KRAS-induced lung tumorigenesis. Nat Commun 6:6285
8. Hansen J (1998) Common cancers in the elderly. Drugs Aging 13:467–478
9. Harkema JR, Wagner JG (2002) Non-allergic models of mucous cell metaplasia and mucus hypersecretion in rat nasal and pulmonary airways. Novartis Found Symp 248:181–197, discussion 197-200, 277-182
10. Kato T, Ishikawa K, Aragaki M, Sato M, Okamoto K, Ishibashi T, Kaji M (2012) Angiolymphatic invasion exerts a strong impact on surgical outcomes for stage I lung adenocarcinoma, but not non-adenocarcinoma. Lung Cancer 77:394–400
11. Kunii R, Jiang S, Hasegawa G, Yamamoto T, Umezu H, Watanabe T, Tsuchida M, Hashimoto T, Hamakubo T, Kodama T, Sasai K, Naito M (2011) The predominant expression of hepatocyte nuclear factor 4alpha (HNF4alpha) in thyroid transcription factor-1 (TTF-1)-negative pulmonary adenocarcinoma. Histopathology 58:467–476
12. Licciulli S, Avila JL, Hanlon L, Troutman S, Cesaroni M, Kota S, Keith B, Simon MC, Pure E, Radtke F, Capobianco AJ, Kissil JL (2013) Notch1 is required for Kras-induced lung adenocarcinoma and controls tumor cell survival via p53. Cancer Res 73:5974–5984
13. Louahed J, Toda M, Jen J, Hamid Q, Renauld JC, Levitt RC, Nicolaides NC (2000) Interleukin-9 upregulates mucus expression in the airways. Am J Respir Cell Mol Biol 22:649–656
14. Maeshima A, Miyagi A, Hirai T, Nakajima T (1997) Mucin-producing adenocarcinoma of the lung, with special reference to goblet cell type adenocarcinoma: immunohistochemical observation and Ki-ras gene mutation. Pathol Int 47:454–460
15. McWilliams A, MacAulay C, Gazdar AF, Lam S (2002) Innovative molecular and imaging approaches for the detection of lung cancer and its precursor lesions. Oncogene 21:6949–6959
16. Mesquita P, Almeida R, Van Seuningen I, David L (2004) Coordinated expression of MUC2 and CDX-2 in mucinous carcinomas of the lung can be explained by the role of CDX-2 as transcriptional regulator of MUC2. Am J Surg Pathol 28:1254–1255
17. Musteanu M, Blaas L, Zenz R, Svinka J, Hoffmann T, Grabner B, Schramek D, Kantner HP, Muller M, Kolbe T, Rulicke T, Moriggl R, Kenner L, Stoiber D, Penninger JM, Popper H, Casanova E, Eferl R (2012) A mouse model to identify cooperating signaling pathways in cancer. Nat Methods 9:897–900
18. Park KS, Korfhagen TR, Bruno MD, Kitzmiller JA, Wan H, Wert SE, Khurana Hershey GK, Chen G, Whitsett JA (2007) SPDEF regulates goblet cell hyperplasia in the airway epithelium. J Clin Invest 117:978–988
19. Pelizzoli R, Tacchetti C, Luzzi P, Strangio A, Bellese G, Zappia E, Guazzi S (2008) TTF-1/NKX2.1 up-regulates the in vivo transcription of nestin. Int J Dev Biol 52:55–62
20. Rice SJ, Lai SC, Wood LW, Helsley KR, Runkle EA, Winslow MM, Mu D (2013) MicroRNA-33a mediates the regulation of high mobility group AT-hook 2 gene (HMGA2) by thyroid transcription factor 1 (TTF-1/NKX2-1). J Biol Chem 288:16348–16360
21. Riely GJ, Johnson ML, Medina C, Rizvi NA, Miller VA, Kris MG, Pietanza MC, Azzoli CG, Krug LM, Pao W, Ginsberg MS (2011) A phase II trial of Salirasib in patients with lung adenocarcinomas with KRAS mutations. J Thorac Oncol 6:1435–1437
22. Riquet M, Foucault C, Berna P, Assouad J, Dujon A, Danel C (2006) Prognostic value of histology in resected lung cancer with emphasis on the relevance of the adenocarcinoma subtyping. Ann Thorac Surg 81:1988–1995
23. Rose MC, Piazza FM, Chen YA, Alimam MZ, Bautista MV, Letwin N, Rajput B (2000) Model systems for investigating mucin gene expression in airway diseases. J Aerosol Med 13:245–261
24. Rossi G, Murer B, Cavazza A, Losi L, Natali P, Marchioni A, Migaldi M, Capitanio G, Brambilla E (2004) Primary mucinous (so-called colloid) carcinomas of the lung: a clinicopathologic and immunohistochemical study with special reference to CDX-2 homeobox gene and MUC2 expression. Am J Surg Pathol 28:442–452
25. Sakamoto H, Shimizu J, Horio Y, Ueda R, Takahashi T, Mitsudomi T, Yatabe Y (2007) Disproportionate representation of KRAS gene mutation in atypical adenomatous hyperplasia, but even distribution of EGFR gene mutation from preinvasive to invasive adenocarcinomas. J Pathol 212:287–294
26. Sakuma Y, Matsukuma S, Yoshihara M, Nakamura Y, Noda K, Nakayama H, Kameda Y, Tsuchiya E, Miyagi Y (2007) Distinctive evaluation of nonmucinous and mucinous subtypes of bronchioloalveolar carcinomas in EGFR and K-ras gene-mutation analyses for Japanese lung adenocarcinomas: confirmation of the correlations with histologic subtypes and gene mutations. Am J Clin Pathol 128:100–108
27. Sato K, Ueda Y, Shikata H, Katsuda S (2006) Bronchioloalveolar carcinoma of mixed mucinous and nonmucinous type: immunohistochemical studies and mutation analysis of the p53 gene. Pathol Res Pract 202:751–756
28. Shah RN, Badve S, Papreddy K, Schindler S, Laskin WB, Yeldandi AV (2002) Expression of cytokeratin 20 in mucinous bronchioloalveolar carcinoma. Hum Pathol 33:915–920
29. Smit EF, Dingemans AM, Thunnissen FB, Hochstenbach MM, van Suylen RJ, Postmus PE (2010) Sorafenib in patients with advanced non-small cell lung cancer that harbor K-ras mutations: a brief report. J Thorac Oncol 5:719–720
30. Snyder EL, Watanabe H, Magendantz M, Hoersch S, Chen TA, Wang DG, Crowley D, Whittaker CA, Meyerson M, Kimura S, Jacks T (2013) Nkx2-1 represses a latent gastric differentiation program in lung adenocarcinoma. Mol Cell 50:185–199
31. Stacher E, Ullmann R, Halbwedl I, Gogg-Kammerer M, Boccon-Gibod L, Nicholson AG, Sheppard MN, Carvalho L, Franca MT, Macsweeney F, Morresi-Hauf A, Popper HH (2004) Atypical goblet cell hyperplasia in congenital cystic adenomatoid malformation as a possible preneoplasia for pulmonary adenocarcinoma in childhood: a genetic analysis. Hum Pathol 35:565–570
32. Takeyama K, Dabbagh K, Lee HM, Agusti C, Lausier JA, Ueki IF, Grattan KM, Nadel JA (1999) Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci U S A 96:3081–3086
33. Thunnissen FB, Prinsen C, Hol B, Van der Drift M, Vesin A, Brambilla C, Montuenga L, Field JK (2012) Smoking history and lung carcinoma: KRAS mutation is an early hit in lung adenocarcinoma development. Lung Cancer 75:156–160
34. Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG (2015) WHO classification of tumours of the lung, pleura, thymus and heart. IARC, WHO Press, Geneva
35. Travis WD, Brambilla E, Müller-Hermelink HK, Harris CC (2004) Pathology and genetics of tumours of the lung, pleura, thymus and heart IARC WHO classification of tumours. IARC Press, Lyon, 10
36. Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger K, Yatabe Y, Powell CA, Beer D, Riely G, Garg K, Austin JH, Rusch VW, Hirsch FR, Jett J, Yang PC, Gould M (2011) International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society: international multidisciplinary classification of lung adenocarcinoma: executive summary. Proc Am Thorac Soc 8:381–385
37. Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, Beer DG, Powell CA, Riely GJ, Van Schil PE, Garg K, Austin JH, Asamura H, Rusch VW, Hirsch FR, Scagliotti G, Mitsudomi T, Huber RM, Ishikawa Y, Jett J, Sanchez-Cespedes M, Sculier JP, Takahashi T, Tsuboi M, Vansteenkiste J, Wistuba I, Yang PC, Aberle D, Brambilla C, Flieder D, Franklin W, Gazdar A, Gould M, Hasleton P, Henderson D, Johnson B, Johnson D, Kerr K, Kuriyama K, Lee JS, Miller VA, Petersen I, Roggli V, Rosell R, Saijo N, Thunnissen E, Tsao M, Yankelewitz D (2011) International association for the study of lung cancer/American thoracic society/European respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 6:244–285
38. Tsuta K, Ishii G, Nitadori J, Murata Y, Kodama T, Nagai K, Ochiai A (2006) Comparison of the immunophenotypes of signet-ring cell carcinoma, solid adenocarcinoma with mucin production, and mucinous bronchioloalveolar carcinoma of the lung characterized by the presence of cytoplasmic mucin. J Pathol 209:78–87
39. Tsutsumida H, Nomoto M, Goto M, Kitajima S, Kubota I, Hirotsu Y, Wakimoto J, Hollingsworth MA, Yonezawa S (2007) A micropapillary pattern is predictive of a poor prognosis in lung adenocarcinoma, and reduced surfactant apoprotein A expression in the micropapillary pattern is an excellent indicator of a poor prognosis. Mod Pathol 20:638–647
40. Tyczynski JE, Bray F, Parkin DM (2003) Lung cancer in Europe in 2000: epidemiology, prevention, and early detection. Lancet Oncol 4:45–55
41. Wistuba II, Gazdar AF (2006) Lung cancer preneoplasia. Annu Rev Pathol 1:331–348
42. Yamauchi K, Piao HM, Nakadate T, Shikanai T, Nakamura Y, Ito H, Mouri T, Kobayashi H, Maesawa C, Sawai T, Ohtsu H, Inoue H (2009) Enhanced goblet cell hyperplasia in HDC knockout mice with allergic airway inflammation. Allergol Int 58:125–134
43. Yatabe Y, Koga T, Mitsudomi T, Takahashi T (2004) CK20 expression, CDX2 expression, K-ras mutation, and goblet cell morphology in a subset of lung adenocarcinomas. J Pathol 203:645–652
44. Yoshizawa A, Motoi N, Riely GJ, Sima CS, Gerald WL, Kris MG, Park BJ, Rusch VW, Travis WD (2011) Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases Mod Pathol
45. Yoshizawa A, Sumiyoshi S, Sonobe M, Kobayashi M, Fujimoto M, Kawakami F, Tsuruyama T, Travis WD, Date H, Haga H (2013) Validation of the IASLC/ATS/ERS lung adenocarcinoma classification for prognosis and association with EGFR and KRAS gene mutations: analysis of 440 Japanese patients. J Thorac Oncol 8:52–61
46. Zhang X, Zhang Y, Tao B, Wang D, Cheng H, Wang K, Zhou R, Xie Q, Ke Y (2012) Docking protein Gab2 regulates mucin expression and goblet cell hyperplasia through TYK2/STAT6 pathway. FASEB J 26:4603–4613
47. Zhang Y, Sun Y, Pan Y, Li C, Shen L, Li Y, Luo X, Ye T, Wang R, Hu H, Li H, Wang L, Pao W, Chen H (2012) Frequency of driver mutations in lung adenocarcinoma from female never-smokers varies with histologic subtypes and age at diagnosis. Clin Cancer Res 18:1947–1953