Hierarchical clustering identifies a subgroup of colonic adenocarcinomas expressing crypt-like differentiation markers, associated with MSS status and better prognosis

Virchows Archiv

Volumn 466, Issue 4, 2015, Pages 383-391

  Droy Dupré, Laure ^a   Bossard, Céline ^a   Volteau, Christelle ^a   Bezieau, Stéphane ^a   Laboisse, Christian L ^a   Mosnier, Jean François ^a,b  

^a NANTES UNIVERSITY HOSPITAL   (France)

^b HÔTEL DIEU   (France)

Author keywords

Colonic adenocarcinomas; Hierarchical clustering analysis; Lineage of differentiation

Indexed keywords

CYTOKERATIN 20; CYTOKERATIN 7; MISMATCH REPAIR PROTEIN; MUCIN 2; MUCIN 5AC; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; TRANSCRIPTION FACTOR CDX2; TUMOR MARKER; CDX2 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MUC2 PROTEIN, HUMAN; MUC5AC PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOMA; CELL DIFFERENTIATION; COLON ADENOCARCINOMA; CRYPT LIKE CARCINOMA; DISEASE SEVERITY; EPITHELIUM CELL; FEMALE; GASTROINTESTINAL TRACT; GENOTYPE; HIERARCHICAL CLUSTERING ANALYSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INVESTIGATIVE PROCEDURES; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADENOCARCINOMA; BIOSYNTHESIS; CLUSTER ANALYSIS; COLON TUMOR; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; TISSUE MICROARRAY; VERY ELDERLY; YOUNG ADULT;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; CLUSTER ANALYSIS; COLONIC NEOPLASMS; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; KERATIN-20; KERATIN-7; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MUCIN 5AC; MUCIN-2; PROGNOSIS; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 84930734743     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-015-1724-9     Document Type: Article

References (37)

1. Jass JR (2007) Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 50:113–130
2. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM, Bos JL (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319:525–532
3. Tomlinson I, Bodmer W (1999) Selection, the mutation rate and cancer: ensuring that the tail does not wag the dog. Nat Med 5:11–12
4. Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C, van Es JH, Breukel C, Wiegant J, Giles RH, Clevers H (2001) Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 3:433–438
5. Aaltonen LA, Peltomäki P, Leach FS, Sistonen P, Pylkkänen L, Mecklin JP, Järvinen H, Powell SM, Jen J, Hamilton SR et al (1993) Clues to the pathogenesis of familial colorectal cancer. Science 260:812–816
6. Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M (1993) Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 363:558–561
7. Thibodeau SN, Bren G, Schaid D (1993) Microsatellite instability in cancer of the proximal colon. Science 260:816–819
8. Cunningham JM, Christensen ER, Tester DJ, Kim CY, Roche PC, Burgart LJ, Thibodeau SN (1998) Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. Cancer Res 58:3455–3460
9. Gafà R, Maestri I, Matteuzzi M, Santini A, Ferretti S, Cavazzini L, Lanza G (2000) Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability. Cancer 89:2025–2037
10. Alexander J, Watanabe T, Wu TT, Rashid A, Li S, Hamilton SR (2001) Histopathological identification of colon cancer with microsatellite instability. Am J Pathol 158:527–535
11. Greenson JK, Huang SC, Herron C, Moreno V, Bonner JD, Tomsho LP, Ben-Izhak O, Cohen HI, Trougouboff P, Bejhar J, Sova Y, Pinchev M, Rennert G, Gruber SB (2009) Pathologic predictors of microsatellite instability in colorectal cancer. Am J Surg Pathol 33:126–133
12. Hamilton SR, Bosman FT, Boffetta P, Ilyas M, Morreau H, Nakamura S-I, Quirke P, Riboli E, Sobin LH (2010) Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds) WHO classification of tumours of the digestive system. IARC Press, Lyon, pp 134–146
13. Sobin LH, Brierley J (2009) Colon and rectum. In: Sobin LH, Gospodarowicz MK, Wittekind C (eds) TNM classification of malignant tumours, 7th edn. Wiley-Blackwell, Oxford, pp 100–105
14. Liu CL, Prapong W, Natkunam Y, Alizadeh A, Montgomery K, Gilks CB, van de Rijn M (2002) Software tools for high-throughput analysis and archiving of immunohistochemistry staining data obtained with tissue microarrays. Am J Pathol 161:1557–1565
15. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868
16. Suraweera N, Duval A, Reperant M, Vaury C, Furlan D, Leroy K, Seruca R, Iacopetta B, Hamelin R (2002) Evaluation of tumor microsatellite instability using five quasimonomorphic mononucleotide repeats and pentaplex PCR. Gastroenterology 123:1804–1811
17. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, Moore T, Hudson J Jr, Lu L, Lewis DB, Tibshirani R, Sherlock G, Chan WC, Greiner TC, Weisenburger DD, Armitage JO, Warnke R, Levy R, Wilson W, Grever MR, Byrd JC, Botstein D, Brown PO, Staudt LM (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:503–511
18. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lønning PE, Børresen-Dale AL (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98:10869–10874
19. Makretsov NA, Huntsman DG, Nielsen TO, Yorida E, Peacock M, Cheang MC, Dunn SE, Hayes M, van de Rijn M, Bajdik C, Gilks CB (2004) Hierarchical clustering analysis of tissue microarray immunostaining data identifies prognostically significant groups of breast carcinoma. Clin Cancer Res 10:6143–6151
20. Jacquemier J, Ginestier C, Rougemont J, Bardou VJ, Charafe-Jauffret E, Geneix J, Adélaïde J, Koki A, Houvenaeghel G, Hassoun J, Maraninchi D, Viens P, Birnbaum D, Bertucci F (2005) Protein expression profiling identifies subclasses of breast cancer and predicts prognosis. Cancer Res 65:767–779
21. Alkushi A, Clarke BA, Akbari M, Makretsov N, Lim P, Miller D, Magliocco A, Coldman A, van de Rijn M, Huntsman D, Parker R, Gilks CB (2007) Identification of prognostically relevant and reproducible subsets of endometrial adenocarcinoma based on clustering analysis of immunostaining data. Mod Pathol 20:1156–1165
22. Lorentz O, Duluc I, Arcangelis AD, Simon-Assmann P, Kedinger M, Freund JN (1997) Key role of the Cdx2 homeobox gene in extracellular matrix-mediated intestinal cell differentiation. J Cell Biol 139:1553–1565
23. Silberg DG, Swain GP, Suh ER, Traber PG (2000) Cdx1 and cdx2 expression during intestinal development. Gastroenterology 119:961–971
24. Moll R, Löwe A, Laufer J, Franke WW (1992) Cytokeratin 20 in human carcinomas. A new histodiagnostic marker detected by monoclonal antibodies. Am J Pathol 140:427–447
25. Chang SK, Dohrman AF, Basbaum CB, Ho SB, Tsuda T, Toribara NW, Gum JR, Kim YS (1994) Localization of mucin (MUC2 and MUC3) messenger RNA and peptide expression in human normal intestine and colon cancer. Gastroenterology 107:28–36
26. Uesaka T, Kageyama N, Watanabe H (2004) Identifying target genes regulated downstream of Cdx2 by microarray analysis. J Mol Biol 337:647–660
27. Stosiek P, Bräutigam E, Kasper M (1991) Expression of cytokeratin 7 in human glandular epithelium of fetal stomach. Acta Histochem 91:21–23
28. Tatsumi N, Kushima R, Vieth M, Mukaisho K, Kakinoki R, Okabe H, Borchard F, Stolte M, Okanoue T, Hattori T (2006) Cytokeratin 7/20 and mucin core protein expression in ulcerative colitis-associated colorectal neoplasms. Virchows Arch 448:756–762
29. Forgue-Lafitte ME, Fabiani B, Levy PP, Maurin N, Fléjou JF, Bara J (2007) Abnormal expression of M1/MUC5AC mucin in distal colon of patients with diverticulitis, ulcerative colitis and cancer. Int J Cancer 121:1543–1549
30. Hinoi T, Tani M, Lucas PC, Caca K, Dunn RL, Macri E, Loda M, Appelman HD, Cho KR, Fearon ER (2001) Loss of CDX2 expression and microsatellite instability are prominent features of large cell minimally differentiated carcinomas of the colon. Am J Pathol 159:2239–2248
31. McGregor DK, Wu TT, Rashid A, Luthra R, Hamilton SR (2004) Reduced expression of cytokeratin 20 in colorectal carcinomas with high levels of microsatellite instability. Am J Surg Pathol 28:712–718
32. Biemer-Hüttmann AE, Walsh MD, McGuckin MA, Simms LA, Young J, Leggett BA, Jass JR (2000) Mucin core protein expression in colorectal cancers with high levels of microsatellite instability indicates a novel pathway of morphogenesis. Clin Cancer Res 6:1909–1916
33. Yao T, Nishiyama KI, Oya M, Kouzuki T, Kajiwara M, Tsuneyoshi M (2000) Multiple ‘serrated adenocarcinomas’ of the colon with a cell lineage common to metaplastic polyp and serrated adenoma. Case report of a new subtype of colonic adenocarcinoma with gastric differentiation. J Pathol 190:444–449
34. Buisine MP, Janin A, Maunoury V, Audié JP, Delescaut MP, Copin MC, Colombel JF, Degand P, Aubert JP, Porchet N (1996) Aberrant expression of a human mucin gene (MUC5AC) in rectosigmoid villous adenoma. Gastroenterology 110:84–91
35. Iacopetta B, Kawakami K, Watanabe T (2008) Predicting clinical outcome of 5-fluorouracil-based chemotherapy for colon cancer patients: is the CpG island methylator phenotype the 5-fluorouracil-responsive subgroup? Int J Clin Oncol 13:498–503
36. Boland CR, Goel A (2010) Microsatellite instability in colorectal cancer. Gastroenterology 138:2073–2087
37. Varadhachary GR, Raber MN, Matamoros A, Abbruzzese JL (2008) Carcinoma of unknown primary with a colon-cancer profile-changing paradigm and emerging definitions. Lancet Oncol 9:596–599