A subset of high-grade pulmonary neuroendocrine carcinomas shows up-regulation of matrix metalloproteinase-7 associated with nuclear β-catenin immunoreactivity, independent of EGFR and HER-2 gene amplification or expression

Virchows Archiv

Volumn 447, Issue 6, 2005, Pages 969-977

  Pelosi, Giuseppe ^a,c   Scarpa, Aldo ^b   Veronesi, Giulia ^c   Spaggiari, Lorenzo ^c   Del Curto, Barbara ^a   Moore, Patrick S ^b   Maisonneuve, Patrick ^c   Sonzogni, Angelica ^a   Masullo, Michele ^a   Viale, Giuseppe ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

catenin; EGFR; Lung; MMP 7; Neuroendocrine carcinoma

Indexed keywords

BETA CATENIN; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR; MATRILYSIN;

ADULT; AGED; ARTICLE; CONTROLLED STUDY; EXON; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; LARGE CELL CARCINOMA; LUNG CARCINOMA; LUNG SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; NEUROENDOCRINE TUMOR; NUCLEOTIDE SEQUENCE; ONCOGENE NEU; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING; SURVIVAL; UPREGULATION;

ADULT; AGED; BASE SEQUENCE; BETA CATENIN; CARCINOMA, NEUROENDOCRINE; CELL NUCLEUS; DNA MUTATIONAL ANALYSIS; FEMALE; GENE AMPLIFICATION; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LUNG NEOPLASMS; MALE; MATRIX METALLOPROTEINASE 7; MIDDLE AGED; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-3; UP-REGULATION;

EID: 28344444144     PISSN: 09456317     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00428-005-0044-x     Document Type: Article

References (60)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R (1997) b-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804
2. Barshack I, Goldberg I, Chowers Y, Horowitz A, Kopolovic J (2002) Different beta-catenin immunoexpression in carcinoid tumors of the appendix in comparison to other gastrointestinal carcinoid tumors. Pathol Res Pract 198:531-536
3. Beasley MB, Lantuejoul S, Abbondanzo S, Chu WS, Hasleton PS, Travis WD, Brambilla E (2003) The P16/cyclin D1/Rb pathway in neuroendocrine tumors of the lung. Human Pathol 34:136-142
4. Bolon I, Devouassoux M, Roberft C, Moro D, Brambilla C, Brambilla E (1997) Expression of urokinase-type plasminogen activator, stromelysin 1, stromelysin 3, and matrilysin genes in lung carcinomas. Am J Pathol 150:1619-1629
5. Borchers AH, Sanders LA, Bowden GT (1997) Regulation of matrilysin expression in cells of squamous cell carcinoma by E-cadherin-mediated cell-cell contact. J Cancer Res Clin Oncol 123:13-20
6. Brabletz T, Jung A, Dag S, Hlubek F, Kirchner T (1999) b-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 155:1033-1038
7. Brambilla E, Negoescu A, Gazzeri S, Lantuejoul S, Moro D, Brambilla C, Coll JL (1996) Apoptosis-related factors p53, Bcl2, and Bax in neuroendocrine lung tumors. Am J Pathol 149:1941-1452
8. Chan AO, Kim SG, Bedeir A, Issak JP, Hamilton SR, Rashid A (2003) CpG island methylation in carcinoid and pancreatic endocrine tumors. Oncogene 22:924-934
9. Clavel CE, Nollet F, Berx G, Tejpar S, Nawrocki-Raby B, Kaplan HH, van Roy FM, Birembaut PL (2001) Expression of the E-cadherin-catenin complex in lung neuroendocrine tumours. J Pathol 194:20-26
10. Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P, Matrisian LM (1999) The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18:2883-2891
11. Davies G, Jiang WG, Mason MD (2001) Matrilysin mediates extracellular cleavage of E-cadherin from prostate cancer cells: a key mechanism in hepatocyte growth factor/scatter factor-induced cell-cell dissociation and in vitro invasion. Clin Cancer Res 7:3289-3297
12. De Pas T, Pelosi G, de Braud F, Veronesi G, Curigliano G, Leon ME, Danesi R, Noberasco C, d'Aiuto M, Catalano G, Viale G, Spaggiari L (2004) Modulation of epidermal growth factor receptor status by chemotherapy in patients with locally advanced non-small-cell lung cancer is rare. J Clin Oncol 22:4966-4970
13. Dorudi S, Hanby AM, Poulsom R, Northover J, Hart IR (1995) Level of expression of E-cadherin mRNA in colorectal cancer correlates with clinical outcome. Br J Cancer 71:614-616
14. Dosaka-Akita H, Cagle PT, Hiroumi H, Fujita M, Yamashita M, Sharma A, Kawakami Y, Benedict WF (2000) Differential retinoblastoma and p16(INK4A) protein expression in neuroendocrine tumors of the lung. Cancer 88:550-556
15. Fujimori M, Ikeda S, Shimizu Y, Okajima M, Asahara T (2001) Accumulation of beta-catenin protein and mutations in exon 3 of beta-catenin gene in gastrointestinal carcinoid tumor. Cancer Res 61:6656-6659
16. Gumbinber BM (2000) Regulation of cadherin adhesive activity. J Cell Biol 148:399-404
17. Huber AH, Weis WI (2001) The structure of the b-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by b-catenin. Cell 105:391-402
18. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A (1998) Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3b and b-catenin and promotes GSK-3b-dependent phospholylation of b-catenin. EMBO J 17:1371-1384
19. Jones MH, Virtanen C, Honjoh D, Miyoshi T, Satoh Y, Okumura S, Nakagawa K, Nomura H, Ishikawa Y (2004) 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
20. Kawahara M, Kammori M, Kanauchi H, Noguchi C, Kuramoto S, Kaminishi M, Endo H, Takubo K (2002) Immunohistochemical prognostic indicators of gastrointestinal carcinoid tumours. Eur J Surg Oncol 28:140-146
21. Kioi M, Yamamoto K, Higashi S, Koshikawa N, Fujita K, Miyazaki K (2003) Matrilysin (MMP-7) induces homotypic adhesion of human colon cancer cells and enhances their metastatic potential in nude mouse model. Oncogene 22:8662-8670
22. Kotsinas A, Evangelou K, Zacharatos P, Kittas C, Gorgoulis VG (2002) Proliferation, but not apoptosis, is associated with distinct beta-catenin expression patterns in non-small-cell lung carcinomas: relationship with adenomatous polyposis coli and G(1)-to S-phase cell-cycle regulators. Am J Pathol 161:1619-1634
23. Kuroda N, Mizushima S, Guo L, Jin Y, Tao L, Miyazaki E, Toi M, Naruse K, Hiroi M, Enzan H (2001) Goblet cell carcinoid of the appendix: investigation of the expression of beta-catenin and E-cadherin. Pathol Int 51:283-287
24. Leotlela PD, Jauch A, Holtgreve-Grez H, Thakker RV (2003) Genetics of neuroendocrine and carcinoid tumours. Endocr Relat Cancer 10:437-450
25. Li CC, Hirowaka M, Qian ZR, Xu B, Sano T (2002) Expression of E-cadherin, b-catenin, and Ki-67 in goblet cell carcinoids of the appendix: an immunohistochemical study with clinical correlation. Endocr Pathol 13:47-58
26. Li YJ, Wei ZM, Meng YX, Ji XR (2005) Beta-catenin up-regulates the expression of cyclinD1, c-myc and MMP-7 in human pancreatic cancer: relationships with carcinogenesis and metastasis. World J Gastroenterol 11:2117-2123
27. Lu Z, Ghosh S, Wang Z, Hunter T (2003) Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 4:499-515
28. Lu Z, Hunter T (2004) Wnt-independent β-catenin transactivation in tumor development. Cell Cycle 3:571-573
29. Machin P, Catasus L, Pons C, Munoz J, Matias-Guiu X, Prat J (2002) CTNNB1 mutations and beta-catenin expression in endometrial carcinomas. Human Pathol 33:206-212
30. Marchevsky AM, Gal AA, Shah S, Koss MN (2001) 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
31. McGuire JK, Li Q, Parks WC (2003) Matrilysin (matrix metalloproteinase-7) mediates E-cadherin ectodomain shedding in injured lung epithelium. Am J Pathol 162:1831-1843
32. Mylona E, Kapranou A, Mavrommatis J, Markaki S, Keramopoulos A, Nakopoulou L (2005) The multifunctional role of the immunohistochemical expression of MMP-7 in invasive breast cancer. Acta Pathol Microbiol Immunol Scand 113:246-255
33. Nagafuchi A (2001) Molecular architecture of the adherens junctions. Curr Opin Cell Biol 13:600-603
34. Noe V, Fingleton B, Jacobs K, Crawford HC, Vermeulen S, Steelant W, Bruyneel E, Matrisian LM, Mareel M (2001) Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 114:111-118
35. Ougolkov AV, Yamashita K, Mai M, Minamoto T (2002) Oncogenic beta-catenin and MMP-7 (matrilysin) cosegregate in late-stage clinical colon cancer. Gastroenterology 122:60-71
36. 3 promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of b-catenin signaling. J Cell Biol 154:369-387
37. Pelosi G, Del Curto B, Dell'Orto P, Pasini F, Veronesi G, Spaggiari L, Maisonneuve P, Iannucci A, Terzi A, Lonardoni A, Viale G (2005) Lack of prognostic implications of HER-2/neu abnormalities in 345 stage I non-small cell carcinomas (NSCLC) and 207 stage I-III neuroendocrine tumours (NET) of the lung. Int J Cancer 113:101-108
38. Pelosi G, Pasini F, Fraggetta F, Pastorino U, Iannucci A, Maisonneuve P, Arrigoni G, De Manzoni G, Bresaola E, Viale G (2003) Independent value of fascin immunoreactivity for predicting lymph node metastases in typical and atypical pulmonary carcinoids. Lung Cancer J IASLC 42:203-213
39. Pelosi G, Pasini F, Olsen Stenholm C, Pastorino U, Maisonneuve P, Sonzogni A, Maffini F, Pruneri G, Fraggetta F, Cavallon A, Roz E, Iannucci A, Bresaola E, Viale G (2002) p63 immunoreactivity in lung cancer: yet another player in the development of squamous cell carcinomas? J Pathol 198:100-109
40. Pelosi G, Rodriguez J, Viale G, Rosai J (2005) Pulmonary carcinoid tumor overdiagnosed as small-cell carcinoma on biopsy specimens: a major pitfall in the management of lung cancer patients. Am J Surg Pathol 29:179-187
41. Pelosi G, Scarpa A, Puppa G, Veronesi G, Spaggiari L, Pasini F, Maisonneuve P, Iannucci A, Arrigoni GL, Viale G (2005) Alteration of the E-cadherin/b-catenin cell adhesion system is common in pulmonary neuroendocrine tumors and is an independent predictor of lymph node metastasis in atypical carcinoid. Cancer 103:1154-1164
42. Pirinen RT, Hirvikoski P, Johansson RT, Hollmen S, Kosma VM (2001) Reduced expression of alpha-catenin, beta-catenin, and gamma-catenin is associated with high cell proliferative activity and poor differentiation in non-small cell lung cancer. J Clin Pathol 54:391-395
43. Polakis P (2000) Wnt signaling and cancer. Genes Dev 14:1837-1851
44. Prange W, Breuhahn K, Fischer F, Zilkens C, Pietsch T, Petmecky K, Eilers R, Dienes HP, Schirmacher P (2003) Beta-catenin accumulation in the progression of human hepatocarcinogenesis correlates with loss of E-cadherin and accumulation of p53, but not with expression of conventional WNT-1 target genes. J Pathol 201:250-259
45. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P (1996) Binding of GSK3b to the APC-b-catenin complex and regulation of complex assembly. Science 272:1023-1026
46. Saeki H, Tanaka S, Sugimachi K, Kimura Y, Miyazaki M, Ohga T, Sugimachi K (2002) Interrelation between expression of matrix metalloproteinase 7 and beta-catenin in esophageal cancer. Dig Dis Sci 47:2738-2742
47. Salon C, Moro D, Lantuejoul S, Brichon PY, Drabkin H, Brambilla C, Brambilla E (2004) E-cadherin-b-catenin adhesion complex in neuroendocrine tumors of the lung: a suggested role upon local invasion and metastasis. Human Pathol 35:1148-1155
48. Semba S, Han S-Y, Ikeda H, Akira H (2001) Frequent nuclear accumulation of b-catenin in pituitary adenoma. Cancer 91:42-48
49. Semba S, Kusumi R, Moriya T, Sasano H (2000) Nuclear accumulation of B-Catenin in human endocrine tumors: association with Ki-67 (MIB-1) proliferative activity. Endocr Pathol 11:243-250
50. Stancu M, Wu TT, Wallace C, Houlihan PS, Hamilton SR, Rashid A (2003) Genetic alterations in goblet cell carcinoids of the vermiform appendix and comparison with gastrointestinal carcinoid tumors. Mod Pathol 16:1189-1198
51. Su LK, Vogelstein B, Kinzler KW (1993) Association of APC tumor suppressor protein with catenins. Science 262:1734-1737
52. Sun X, Gong Y, Talamont MS, Rao MS (2002) Expression of cell adhesion molecules, CD44s and E-cadherin, and microvessel density in carcinoid tumors. Mod Pathol 15:1333-1338
53. Takeichi M (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251:1451-1455
54. Tetsu O, McCormick F (1999) b-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422-426
55. Toyooka S, Toyooka KO, Maruyama R, Virmani AK, Girard L, Miyajima K, Harada K, Ariyoshi Y, Takahashi T, Sugio K, Brambilla E, Gilcrease M, Minna JD, Gazdar AF (2001) DNA methylation profiles of lung tumors. Mol Cancer Ther 1:61-67
56. Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC (2004) Tumours of the lung, pleura, thymus and heart. IARC Press, Lyon
57. Ullmann R, Petzmann S, Sharma A, Cagle PT, Popper HH (2001) Chromosomal aberrations in a series of large-cell neuroendocrine carcinomas: unexpected divergence from small-cell carcinoma of the lung. Human Pathol 32:1059-1063
58. Watabe M, Nagafuchi A, Tsukita S, Takeichi M (1994) Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line. J Cell Biol 127:247-256
59. Xu H, Tanimoto A, Murata Y, Kimura S, Wang KY, Sasaguri Y (2003) Difference in responsiveness of human esophageal squamous cell carcinoma lines to epidermal growth factor for MMP-7 expression. Int J Oncol 23:469-476
60. Yang F, Li X, Sharma M, Sasaki CY, Longo DL, Lim B, Sun Z (2002) Linking b-catenin to androgen-signaling pathway. J Biol Chem 277:11336-11344