Top

International Journal of Colorectal Disease

Published in:

01-07-2005 | Original Article

Common denominator genes that distinguish colorectal carcinoma from normal mucosa

Authors: Roland S. Croner, Thomas Foertsch, Wolfgang M. Brueckl, Klaus Guenther, Renate Siebenhaar, Christian Stremmel, Klaus E. Matzel, Thomas Papadopoulos, Thomas Kirchner, Jürgen Behrens, Ludger Klein-Hitpass, Michael Stuerzl, Werner Hohenberger, Bertram Reingruber

Published in: International Journal of Colorectal Disease | Issue 4/2005

Abstract

Purpose

Microarray technology has been used by a growing number of investigators and several studies have been published that list hundreds of genes differentially expressed by colorectal carcinoma (CRC) and normal mucosa (MC). On the basis of our own and other investigators’ microarray data, our goal was to identify a common denominator gene cluster distinguishing CRC from MC.

Methods

Thirty GeneChips (HG-U133A, Affymetrix) were hybridized, 20 with RNA of CRC stages I–IV (UICC) and 10 with MC. Expression signals showing at least a 4-fold difference between CRC and MC (p<0.01) were identified as differentially expressed. In addition, in our integrative data analysis approach only those genes whose expression was altered simultaneously in at least 2 of 5 recently published studies were subjected to an unsupervised hierarchical cluster analysis.

Results

We detected 168 up- and 283 down-regulated genes in CRC relative to MC. Twenty-three genes were filtered from the five articles reviewed. An unsupervised hierarchical cluster analysis of these 23 genes confirmed the high specificity of these genes to differentiate between CRC and MC in our microarray data.

Conclusions

Colorectal cancer and mucosa could be clearly separated by 23 genes selected for being differentially expressed more than once in a recent literature review. These genes represent a common denominator gene cluster that can be used to distinguish colorectal MC from CRC.

Leslie A, Carey FA, Pratt NR, Steele RJ (2002) The colorectal adenoma–carcinoma sequence. Br J Surg 89:845–860CrossRefPubMed

Cho KR, Vogelstein B (1992) Genetic alterations in the adenoma–carcinoma sequence. Cancer 70 [Suppl]:1727–1731PubMed

Arends JW (2000) Molecular interactions in the Vogelstein model of colorectal carcinoma. J Pathol 190:412–416CrossRefPubMed

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 319:525–532PubMed

Hermanek P, Sobin LH, Wittekind C (1999) How to improve the present TNM staging system. Cancer 86:2189–2191PubMed

Notterman DA, Alon U, Sierk AJ, Levine AJ (2001) Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma, and normal tissue examined by oligonucleotide arrays. Cancer Res 61:3124–3130PubMed

Kitahara O, Furukawa Y, Tanaka T, Kihara C, Ono K, Yanagawa R, Nita ME, Takagi T, Nakamura Y, Tsunoda T (2001) Alterations of gene expression during colorectal carcinogenesis revealed by cDNA microarrays after laser-capture microdissection of tumor tissues and normal epithelia. Cancer Res 61:3544–3549PubMed

Birkenkamp-Demtroder K, Christensen LL, Olesen SH, Frederiksen CM, Laiho P, Aaltonen LA, Laurberg S, Sorensen FB, Hagemann R, Orntoft TF (2002) Gene expression in colorectal cancer. Cancer Res 62:4352–4363PubMed

Takemasa I, Higuchi H, Yamamoto H, Sekimoto M, Tomita N, Nakamori S, Matoba R, Monden M, Matsubara K (2001) Construction of preferential cDNA microarray specialized for human colorectal carcinoma: molecular sketch of colorectal cancer. Biochem Biophys Res Commun 285:1244–1249CrossRefPubMed

10.

Williams NS, Gaynor RB, Scoggin S, Verma U, Gokaslan T, Simmang C, Fleming J, Tavana D, Frenkel E, Becerra C (2003) Identification and validation of genes involved in the pathogenesis of colorectal cancer using cDNA microarrays and RNA interference. Clin Cancer Res 9:931–946PubMed

11.

Croner RS, Guenther K, Foertsch T, Siebenhaar R, Brueckl WM, Stremmel C, Hlubek F, Hohenberger W, Reingruber B (2004) Tissue preparation for gene expression profiling of colorectal carcinoma: three alternatives to laser microdissection with preamplification. J Lab Clin Med 143:344–351CrossRefPubMed

12.

Nachamkin I, Panaro NJ, Li M, Ung H, Yuen PK, Kricka LJ, Wilding P (2001) Agilent 2100 bioanalyzer for restriction fragment length polymorphism analysis of the Campylobacter jejuni flagellin gene. J Clin Microbiol 39:754–757CrossRefPubMed

13.

Hsiao LL, Dangond F, Yoshida T, Hong R, Jensen RV, Misra J, Dillon W, Lee KF, Clark KE, Haverty P, Weng Z, Mutter GL, Frosch MP, Macdonald ME, Milford EL, Crum CP, Bueno R, Pratt RE, Mahadevappa M, Warrington JA, Stephanopoulos G, Stephanopoulos G, Gullans SR (2001) A compendium of gene expression in normal human tissues. Physiol Genomics 7:97–104PubMed

14.

Durig J, Nuckel H, Huttmann A, Kruse E, Holter T, Halfmeyer K, Fuhrer A, Rudolph R, Kalhori N, Nusch A, Deaglio S, Malavasi F, Moroy T, Klein-Hitpass L, Duhrsen U (2003) Expression of ribosomal and translation-associated genes is correlated with a favorable clinical course in chronic lymphocytic leukemia. Blood 101:2748–2755CrossRefPubMed

15.

Guenzi E, Topolt K, Lubeseder-Martellato C, Jorg A, Naschberger E, Benelli R, Albini A, Sturzl M (2003) The guanylate binding protein-1 GTPase controls the invasive and angiogenic capability of endothelial cells through inhibition of MMP-1 expression. EMBO J 22:3772–3782CrossRefPubMed

16.

Lubeseder-Martellato C, Guenzi E, Jorg A, Topolt K, Naschberger E, Kremmer E, Zietz C, Tschachler E, Hutzler P, Schwemmle M, Matzen K, Grimm T, Ensoli B, Sturzl M (2002) Guanylate-binding protein-1 expression is selectively induced by inflammatory cytokines and is an activation marker of endothelial cells during inflammatory diseases. Am J Pathol 161:1749–1759PubMed

17.

Hiki Y, Iyama K, Tsuruta J, Egami H, Kamio T, Suko S, Naito I, Sado Y, Ninomiya Y, Ogawa M (2002) Differential distribution of basement membrane type IV collagen alpha1(IV), alpha2(IV), alpha5(IV) and alpha6(IV) chains in colorectal epithelial tumors. Pathol Int 52:224–233CrossRefPubMed

18.

Shiozawa J, Ito M, Nakayama T, Nakashima M, Kohno S, Sekine I (2000) Expression of matrix metalloproteinase-1 in human colorectal carcinoma. Mod Pathol 13:925–933CrossRefPubMed

19.

Kim PJ, Plescia J, Clevers H, Fearon ER, Altieri DC (2003) Survivin and molecular pathogenesis of colorectal cancer. Lancet 362:205–209CrossRefPubMed

20.

Takemasa I, Yamamoto H, Sekimoto M, Ohue M, Noura S, Miyake Y, Matsumoto T, Aihara T, Tomita N, Tamaki Y, Sakita I, Kikkawa N, Matsuura N, Shiozaki H, Monden M (2000) Overexpression of CDC25B phosphatase as a novel marker of poor prognosis of human colorectal carcinoma. Cancer Res 60:3043–3050PubMed

21.

Miwa N, Furuse M, Tsukita S, Niikawa N, Nakamura Y, Furukawa Y (2000) Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res 12:469–476PubMed

22.

Li A, Varney ML, Singh RK (2001) Expression of interleukin 8 and its receptors in human colon carcinoma cells with different metastatic potentials. Clin Cancer Res 7:3298–3304PubMed

23.

Mason IJ, Taylor A, Williams JG, Sage H, Hogan BL (1986) Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell ‘culture shock’ glycoprotein of Mr 43,000. EMBO J 5:1465–1472PubMed

24.

Lewin AR, Reid LE, McMahon M, Stark GR, Kerr IM (1991) Molecular analysis of a human interferon-inducible gene family. Eur J Biochem 199:417–423PubMed

25.

Lincoln AJ, Wickramasinghe D, Stein P, Schultz RM, Palko ME, De Miguel MP, Tessarollo L, Donovan PJ (2002) Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 30:446–449

26.

Dhanesuan N, Sharp JA, Blick T, Price JT, Thompson EW (2002) Doxycycline-inducible expression of SPARC/osteonectin/BM40 in MDA-MB-231 human breast cancer cells results in growth inhibition. Breast Cancer Res Treat 75:73–85CrossRefPubMed

27.

Behrens P, Brinkmann U, Wellmann A (2003) CSE1L/CAS: its role in proliferation and apoptosis. Apoptosis 8:39–44CrossRefPubMed

28.

Payne AM, Downes SM, Bessant DA, Plant C, Moore T, Bird AC, Bhattacharya SS (1999) Genetic analysis of the guanylate cyclase activator 1B (GUCA1B) gene in patients with autosomal dominant retinal dystrophies. J Med Genet 36:691–693PubMed

29.

Puscas I, Coltau M, Baican M, Domuta G, Hecht A (2001) Calcium, carbonic anhydrase and gastric acid secretion. Physiol Res 50:359–364PubMed

30.

Makela S, Kere J, Holmberg C, Hoglund P (2002) SLC26A3 mutations in congenital chloride diarrhea. Human Mutat 20:425–438CrossRef

31.

Sweadner KJ, Rael E (2000) The FXYD gene family of small ion transport regulators or channels: cDNA sequence, protein signature sequence, and expression. Genomics 68:41–56CrossRefPubMed

32.

Sly WS, Whyte MP, Sundaram V, Tashian RE, Hewett-Emmett D, Guibaud P, Vainsel M, Baluarte HJ, Gruskin A, Al-Mosawi Met al (1985) Carbonic anhydrase II deficiency in 12 families with the autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification. N Engl J Med 313:139–145

33.

Schweinfest CW, Henderson KW, Suster S, Kondoh N, Papas TS (1993) Identification of a colon mucosa gene that is down-regulated in colon adenomas and adenocarcinomas. Proc Natl Acad Sci USA 90:4166–4170

34.

Stoehlmacher J, Lenz HJ (2003) Implications of genetic testing in the management of colorectal cancer. Am J Pharmacogenomics 3:73–88PubMed

Title: Common denominator genes that distinguish colorectal carcinoma from normal mucosa
Authors: Roland S. Croner
Thomas Foertsch
Wolfgang M. Brueckl
Klaus Guenther
Renate Siebenhaar
Christian Stremmel
Klaus E. Matzel
Thomas Papadopoulos
Thomas Kirchner
Jürgen Behrens
Ludger Klein-Hitpass
Michael Stuerzl
Werner Hohenberger
Bertram Reingruber
Publication date: 01-07-2005
Publisher: Springer-Verlag
Published in: International Journal of Colorectal Disease / Issue 4/2005
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI: https://doi.org/10.1007/s00384-004-0664-7

At a glance: The STEP trials

Springer Medicine

Common denominator genes that distinguish colorectal carcinoma from normal mucosa

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 4/2005

Perforated right colonic diverticulitis complicating pregnancy at 37 weeks’ gestation

Can three-dimensional endoanal ultrasonography detect external anal sphincter atrophy? A comparison with endoanal magnetic resonance imaging

Epithelioid hemangiosarcoma of the rectum

Electrodynamic smooth muscle sphincter

Expression of c-kit messenger ribonucleic acid and c-kit protein in sigmoid colon of patients with slow transit constipation

Comparison of inpatient and outpatient upper gastrointestinal haemorrhage