A gene expression and pre-mRNA splicing signature that marks the adenoma-adenocarcinoma progression in colorectal cancer

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Pesson, Marine ^a   Volant, Alain ^a,b   Uguen, Arnaud ^a,b   Trillet, Kilian ^a   De La Grange, Pierre ^c   Aubry, Marc ^d   Daoulas, Mélanie ^b   Robaszkiewicz, Michel ^b   Le Gac, Gérald ^a,b   Morel, Alain ^e   Simon, Brigitte ^a   Corcos, Laurent ^a,b  

^a FACULTÉ DE MÉDECINE ET DES SCIENCES DE LA SANTÉ   (France)

^b UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

^e INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FBLN1 PROTEIN; INHBA PROTEIN; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG; RNA PRECURSOR;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER GROWTH; CANCER RISK; CFH GENE; COLORECTAL ADENOMA; COLORECTAL CARCINOMA; CRYAB GENE; DPT GENE; FBLN1 GENE; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; ITIH5 GENE; MICROARRAY ANALYSIS; NR3C2 GENE; RNA SPLICING; SLIT3 GENE; TIMP1 GENE; ADENOCARCINOMA; ADENOMA; BIOPSY; CLUSTER ANALYSIS; COLORECTAL TUMOR; DISEASE COURSE; DOWN REGULATION; EXON; GENE EXPRESSION REGULATION; GENETICS; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; UPREGULATION;

ADENOCARCINOMA; ADENOMA; BIOPSY; CLUSTER ANALYSIS; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; DOWN-REGULATION; EXONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTESTINAL MUCOSA; RNA PRECURSORS; RNA SPLICING; UP-REGULATION;

EID: 84895551622     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087761     Document Type: Article

References (53)

1. Citarda F, Tomaselli G, Capocaccia R, Barcherini S, Crespi M (2001) Efficacy in standard clinical practice of colonoscopic polypectomy in reducing colorectal cancer incidence. Gut 48: 812-815. (Pubitemid 32476984)
2. Shinya H, Wolff WI (1979) Morphology, anatomic distribution and cancer potential of colonic polyps. Annals of Surgery 190: 679-683.
3. Fornasarig M, Valentini M, Poletti M, Carbone A, Bidoli E, et al. (1998) Evaluation of the risk for metachronous colorectal neoplasms following intestinal polypectomy: a clinical, endoscopic and pathological study. Hepato-gastroenterology 45: 1565-1572. (Pubitemid 28515160)
4. Jones S, Chen Wd, Parmigiani G, Diehl F, Beerenwinkel N, et al. (2008) Comparative lesion sequencing provides insights into tumor evolution. Proceedings of the National Academy of Sciences 105: 4283-4288.
5. Ma Y, Zhang P, Yang J, Liu Z, Yang Z, et al. (2012) Candidate microRNA biomarkers in human colorectal cancer: Systematic review profiling studies and experimental validation. International Journal of Cancer 130: 2077-2087.
6. Gardina PJ, Clark TA, Shimada B, Staples MK, Yang Q, et al. (2006) Alternative splicing and differential gene expression in colon cancer detected by a whole genome exon array. BMC Genomics 7: 325.
7. Bianchini M, Levy E, Zucchini C, Pinski V, Macagno C, et al. (2006) Comparative study of gene expression by cDNA microarray in human colorectal cancer tissues and normal mucosa. International Journal of Oncology 29: 83-94.
8. Bertucci F, Salas S, Eysteries S, Nasser V, Finetti P, et al. (2004) Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters. Oncogene 23: 1377-1391. (Pubitemid 38406833)
9. Skrzypczak M, Goryca K, Rubel T, Paziewska A, Mikula M, et al. (2010) Modeling oncogenic signaling in colon tumors by multidirectional analyses of microarray data directed for maximization of analytical reliability. PLoS ONE 5.
10. Cattaneo E, Laczko E, Buffoli F, Zorzi F, Bianco MA, et al. (2011) Preinvasive colorectal lesion transcriptomes correlate with endoscopic morphology (polypoid vs. nonpolypoid). EMBO Molecular Medicine 3: 334-347.
11. Carvalho B, Sillars-Hardebol AH, Postma C, Mongera S, Droste JTS, et al. (2012) Colorectal adenoma to carcinoma progression is accompanied by changes in gene expression associated with ageing, chromosomal instability, and fatty acid metabolism. Cellular Oncology 35: 53-63.
12. Sillars-Hardebol AH, Carvalho B, Wit M, Postma C, Delis-van Diemen PM, et al. (2010) Identification of key genes for carcinogenic pathways associated with colorectal adenoma-to-carcinoma progression. Tumor Biology 31: 89-96.
13. Tang H, Guo Q, Zhang C, Zhu J, Yang H, et al. (2010) Identification of an intermediate signature that marks the initial phases of the colorectal adenoma-carcinoma transition. International Journal of Molecular Medicine 26: 631-641.
14. Heijink DM, Fehrmann RSN, de Vries EGE, Koornstra JJ, Oosterhuis D, et al. (2011) A bioinformatical and functional approach to identify novel strategies for chemoprevention of colorectal cancer. Oncogene 30: 2026-2036.
15. Thorsen K, Mansilla F, Schepeler T, Øster B, Rasmussen MH, et al. (2011) Alternative splicing of SLC39A14 in colorectal cancer is regulated by the Wnt pathway. Molecular & Cellular Proteomics 10.
16. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. (Pubitemid 352759009)
17. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37: 1-13.
18. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Research 38: D355-D360.
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22deltadeltaCT method. Methods 25: 402-408. (Pubitemid 34164012)
20. Arber N, Shapira I, Ratan J, Stern B, Hibshoosh H, et al. (2000) Activation of c-K-ras mutations in human gastrointestinal tumors. Gastroenterology 118: 1045-1050. (Pubitemid 30346981)
21. Lascorz J, Chen B, Hemminki K, Försti A (2011) Consensus pathways implicated in prognosis of colorectal cancer identified through systematic enrichment analysis of gene expression profiling studies. PLoS ONE 6.
22. Sabates-Bellver J, Van der Flier LG, de Palo M, Cattaneo E, Maake C, et al. (2007) Transcriptome profile of human colorectal adenomas. Molecular Cancer Research 5: 1263-1275.
23. Heslin MJ, Yan J, Johnson MR, Weiss H, Diasio RB, et al. (2001) Role of matrix metalloproteinases in colorectal carcinogenesis. Annals of Surgery 233: 786-792. (Pubitemid 32494559)
24. Van den Berg YW, Osanto S, Reitsma PH, Versteeg HH (2012) The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood 119: 924-932.
25. Lin Y-M, Furukawa Y, Tsunoda T, Yue C-T, Yang K-C, et al. (2002) Molecular diagnosis of colorectal tumors by expression profiles of 50 genes expressed differentially in adenomas and carcinomas. Oncogene 21: 4120-4128. (Pubitemid 34712879)
26. Galamb O, Sipos F, Spisák S, Galamb B, Krenács T, et al. (2009) Potential biomarkers of colorectal adenoma-dysplasia-carcinoma progression: mRNA expression profiling and in situ protein detection on TMAs reveal 15 sequentially upregulated and 2 downregulated genes. Cellular Oncology 31: 19-29.
27. Galamb O, Wichmann B, Sipos F, Spisák S, Krenács T, et al. (2012) Dysplasia-carcinoma transition specific transcripts in colonic biopsy samples. PLoS ONE 7: e48547.
28. Lam AK-Y, Ong K, Ho Y-H (2008) Aurora kinase expression in colorectal adenocarcinoma: correlations with clinicopathological features, p16 expression, and telomerase activity. Human Pathology 39: 599-604.
29. Romanuik TL, Ueda T, Le N, Haile S, Yong TMK, et al. (2009) Novel biomarkers for prostate cancer including noncoding transcripts. The American Journal of Pathology 175: 2264-2276.
30. Miyoshi N, Ishii H, Sekimoto M, Doki Y, Mori M (2009) RGS16 is a marker for prognosis in colorectal cancer. Annals of Surgical Oncology 16: 3507-3514.
31. Hubner RA, Muir KR, Liu JF, Logan RFA, Grainge M, et al. (2006) Genetic variants of UGT1A6 influence risk of colorectal adenoma recurrence. Clinical Cancer Research 12: 6585-6589. (Pubitemid 44799734)
32. Jovov B, Araujo-Perez F, Sigel CS, Stratford JK, McCoy AN, et al. (2012) Differential gene expression between African American and European American colorectal cancer patients. PLoS ONE 7.
33. Wang Q, Wen Y-G, Li D-P, Xia J, Zhou C-Z, et al. (2012) Upregulated INHBA expression is associated with poor survival in gastric cancer. Medical Oncology 29: 77-83.
34. Vié N, Copois V, Bascoul-Mollevi C, Denis V, Bec N, et al. (2008) Overexpression of phosphoserine aminotransferase PSAT1 stimulates cell growth and increases chemoresistance of colon cancer cells. Molecular Cancer 7: 14.
35. Kim YS, Ahn YH, Song KJ, Kang JG, Lee JH, et al. (2012) Overexpression and β-1,6-N-acetylglucosaminylation-initiated aberrant glycosylation of TIMP-1: a "double whammy" strategy in colon cancer progression. Journal of Biological Chemistry 287: 32467-32478.
36. Ahn YH, Kim KH, Shin PM, Ji ES, Kim H, et al. (2012) Identification of low-abundance cancer biomarker candidate TIMP1 from serum with lectin fractionation and peptide affinity enrichment by ultrahigh-resolution mass spectrometry. Analytical Chemistry 84: 1425-1431.
37. Jeffery N, McLean MH, El-Omar EM, Murray GI (2009) The matrix metalloproteinase/tissue inhibitor of matrix metalloproteinase profile in colorectal polyp cancers. Histopathology 54: 820-828.
38. Daum JR, Wren JD, Daniel JJ, Sivakumar S, McAvoy JN, et al. (2009) Ska3 is required for spindle checkpoint silencing and the maintenance of chromosome cohesion in mitosis. Current Biology 19: 1467-1472.
39. Garnett MJ, Mansfeld J, Godwin C, Matsusaka T, Wu J, et al. (2009) UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nature Cell Biology 11: 1363-1369.
40. Hirota T, Kunitoku N, Sasayama T, Marumoto T, Zhang D, et al. (2003) Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114: 585-598. (Pubitemid 37159255)
41. Huang J, Zheng D-L, Qin F-S, Cheng N, Chen H, et al. (2010) Genetic and epigenetic silencing of SCARA5 may contribute to human hepatocellular carcinoma by activating FAK signaling. Journal of Clinical Investigation 120: 223-241.
42. Yan N, Zhang S, Yang Y, Cheng L, Li C, et al. (2012) Therapeutic upregulation of Class A scavenger receptor member 5 inhibits tumor growth and metastasis. Cancer Science 103: 1631-1639.
43. Khamas A, Ishikawa T, Shimokawa K, Mogushi K, Iida S, et al. (2012) Screening for epigenetically masked genes in colorectal cancer using 5-Aza-2′-deoxycytidine, microarray and gene expression profile. Cancer Genomics-Proteomics 9: 67-75.
44. Di Fabio F, Alvarado C, Majdan A, Gologan A, Voda L, et al. (2007) Underexpression of mineralocorticoid receptor in colorectal carcinomas and association with VEGFR-2 overexpression. Journal of Gastrointestinal Surgery 11: 1521-1528.
45. Bommer GT (2004) DRO1, a gene down-regulated by oncogenes, mediates growth inhibition in colon and pancreatic cancer cells. Journal of Biological Chemistry 280: 7962-7975.
46. Kanda M, Nomoto S, Okamura Y, Hayashi M, Hishida M, et al. (2011) Promoter hypermethylation of fibulin 1 gene is associated with tumor progression in hepatocellular carcinoma. Molecular Carcinogenesis 50: 571-579.
47. Cui T, Chen Y, Knösel T, Yang L, Zöller K, et al. (2011) Human complement factor H is a novel diagnostic marker for lung adenocarcinoma. International Journal of Oncology.
48. Jiang X, Tan J, Li J, Kivimäe S, Yang X, et al. (2008) DACT3 is an epigenetic regulator of Wnt/ β-catenin signaling in colorectal cancer and is a therapeutic target of histone modifications. Cancer Cell 13: 529-541. (Pubitemid 351766796)
49. Hamm A, Veeck J, Bektas N, Wild PJ, Hartmann A, et al. (2008) Frequent expression loss of Inter-alpha-trypsin inhibitor heavy chain (ITIH) genes in multiple human solid tumors: A systematic expression analysis. BMC Cancer 8: 25.
50. Zhang H, Widegren E, Wang D-W, Sun X-F (2011) SPARCL1: a potential molecule associated with tumor diagnosis, progression and prognosis of colorectal cancer. Tumor Biology 32: 1225-1231.
51. Miyoshi N, Ishii H, Mimori K, Takatsuno Y, Kim H, et al. (2009) Abnormal expression of TRIB3 in colorectal cancer: a novel marker for prognosis. British Journal of Cancer 101: 1664-1670.
52. André F, Michiels S, Dessen P, Scott V, Suciu V, et al. (2009) Exonic expression profiling of breast cancer and benign lesions: a retrospective analysis. The Lancet Oncology 10: 381-390.
53. Pal S, Gupta R, Davuluri RV (2012) Alternative transcription and alternative splicing in cancer. Pharmacology & Therapeutics.