Epithelial splicing regulatory protein 1 and 2 paralogues correlate with splice signatures and favorable outcome in human colorectal cancer

Oncotarget

Volumn 7, Issue 45, 2016, Pages 73800-73816

  Deloria, Abigail J ^a   Höflmayer, Doris ^b,e   Kienzl, Philip ^a   Lopatecka, Justyna ^a   Sampl, Sandra ^a   Klimpfinger, Martin ^b   Braunschmid, Tamara ^b   Bastian, Fabienne ^b   Lu, Lingeng ^c   Marian, Brigitte ^a   Stättner, Stefan ^b,d   Holzmann, Klaus ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b KAISER FRANZ JOSEF HOSPITAL   (Austria)

^c YALE CANCER CENTER   (United States)

^d Transplantation and Thoracic Surgery ^*  (Austria)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Colorectal cancer; Epithelial splicing regulatory protein; Microsatellite instability; Overall survival; Prognostic marker

Indexed keywords

EPITHELIAL SPLICING REGULATORY PROTEIN 1; EPITHELIAL SPLICING REGULATORY PROTEIN 2; FIBROBLAST GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; MEMBRANE PROTEIN; PROTEIN CTNND1; PROTEIN ENAH; UNCLASSIFIED DRUG; ESRP1 PROTEIN, HUMAN; ESRP2 PROTEIN, HUMAN; RNA BINDING PROTEIN;

ADULT; AGED; ARTICLE; CANCER INHIBITION; CANCER PATIENT; CANCER PROGNOSIS; CANCER STAGING; CANCER TISSUE; CARCINOGENESIS; COHORT ANALYSIS; COLORECTAL CANCER; CONTROLLED STUDY; EARLY DIAGNOSIS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; OVERALL SURVIVAL; PARALOGY; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING; CANCER GRADING; COLORECTAL TUMOR; GENE EXPRESSION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FEMALE; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; RNA SPLICING; RNA-BINDING PROTEINS;

EID: 84995769150     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12070     Document Type: Article

References (44)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J and Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015; 65:87-108.
2. Heinzle C, Sutterluty H, Grusch M, Grasl-Kraupp B, Berger W and Marian B. Targeting fibroblast-growth-factorreceptor-dependent signaling for cancer therapy. Expert opinion on therapeutic targets. 2011; 15:829-846.
3. Carter EP, Fearon AE and Grose RP. Careless talk costs lives: fibroblast growth factor receptor signalling and the consequences of pathway malfunction. Trends in cell biology. 2015; 25:221-233.
4. Goke F, Goke A, von Massenhausen A, Franzen A, Sharma R, Kirsten R, Bohm D, Kristiansen G, Stenzinger A, Wynes M, Hirsch FR, Weichert W, Heasley L, Buettner R and Perner S. Fibroblast growth factor receptor 1 as a putative therapy target in colorectal cancer. Digestion. 2013; 88:172-181.
5. Touat M, Ileana E, Postel-Vinay S, Andre F and Soria JC. Targeting FGFR Signaling in Cancer. Clinical cancer research. 2015; 21:2684-2694.
6. Holzmann K, Grunt T, Heinzle C, Sampl S, Steinhoff H, Reichmann N, Kleiter M, Hauck M and Marian B. Alternative Splicing of Fibroblast Growth Factor Receptor IgIII Loops in Cancer. Journal of nucleic acids. 2012; 2012:950508.
7. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M and Ornitz DM. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. The Journal of biological chemistry. 2006; 281:15694-15700.
8. Sonvilla G, Allerstorfer S, Heinzle C, Stattner S, Karner J, Klimpfinger M, Wrba F, Fischer H, Gauglhofer C, Spiegl-Kreinecker S, Grasl-Kraupp B, Holzmann K, Grusch M, Berger W and Marian B. Fibroblast growth factor receptor 3-IIIc mediates colorectal cancer growth and migration. British journal of cancer. 2010; 102:1145-1156.
9. Ranieri D, Rosato B, Nanni M, Magenta A, Belleudi F and Torrisi MR. Expression of the FGFR2 mesenchymal splicing variant in epithelial cells drives epithelialmesenchymal transition. Oncotarget. 2016; 7:5440-5460. doi: 10.18632/oncotarget.6706.
10. Warzecha CC, Sato TK, Nabet B, Hogenesch JB and Carstens RP. ESRP1 and ESRP2 are epithelial cell-typespecific regulators of FGFR2 splicing. Molecular cell. 2009; 33:591-601.
11. Warzecha CC, Jiang P, Amirikian K, Dittmar KA, Lu H, Shen S, Guo W, Xing Y and Carstens RP. An ESRPregulated splicing programme is abrogated during the epithelial-mesenchymal transition. Embo J. 2010; 29:3286-3300.
12. Warzecha CC, Shen S, Xing Y and Carstens RP. The epithelial splicing factors ESRP1 and ESRP2 positively and negatively regulate diverse types of alternative splicing events. RNA biology. 2009; 6:546-562.
13. Shirakihara T, Horiguchi K, Miyazawa K, Ehata S, Shibata T, Morita I, Miyazono K and Saitoh M. TGF-beta regulates isoform switching of FGF receptors and epithelialmesenchymal transition. Embo J. 2011; 30:783-795.
14. Horiguchi K, Sakamoto K, Koinuma D, Semba K, Inoue A, Inoue S, Fujii H, Yamaguchi A, Miyazawa K, Miyazono K and Saitoh M. TGF-beta drives epithelial-mesenchymal transition through deltaEF1-mediated downregulation of ESRP. Oncogene. 2012; 31:3190-3201.
15. Lin SH, Wang J, Saintigny P, Wu CC, Giri U, Zhang J, Menju T, Diao L, Byers L, Weinstein JN, Coombes KR, Girard L, Komaki R, Wistuba, II, Date H, Minna JD, et al. Genes suppressed by DNA methylation in non-small cell lung cancer reveal the epigenetics of epithelialmesenchymal transition. BMC genomics. 2014; 15:1079.
16. Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ, Wada T, Masuko T, Mogushi K, Tanaka H, Osawa T, Kanki Y, Minami T, Aburatani H, Ohmura M, Kubo A, et al. Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nature communications. 2012; 3:883.
17. Ivanov I, Lo KC, Hawthorn L, Cowell JK and Ionov Y. Identifying candidate colon cancer tumor suppressor genes using inhibition of nonsense-mediated mRNA decay in colon cancer cells. Oncogene. 2007; 26:2873-2884.
18. Ueda J, Matsuda Y, Yamahatsu K, Uchida E, Naito Z, Korc M and Ishiwata T. Epithelial splicing regulatory protein 1 is a favorable prognostic factor in pancreatic cancer that attenuates pancreatic metastases. Oncogene. 2014; 33:4485-4495.
19. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W and Zimmermann P. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Advances in bioinformatics. 2008; 2008:420747.
20. Ishii H, Saitoh M, Sakamoto K, Kondo T, Katoh R, Tanaka S, Motizuki M, Masuyama K and Miyazawa K. Epithelial splicing regulatory proteins 1 (ESRP1) and 2 (ESRP2) suppress cancer cell motility via different mechanisms. The Journal of biological chemistry. 2014; 289:27386-27399.
21. Matsuda Y, Hagio M, Seya T and Ishiwata T. Fibroblast growth factor receptor 2 IIIc as a therapeutic target for colorectal cancer cells. Molecular cancer therapeutics. 2012; 11:2010-2020.
22. Matsuda Y, Ueda J and Ishiwata T. Fibroblast growth factor receptor 2: expression, roles, and potential as a novel molecular target for colorectal cancer. Pathology research international. 2012; 2012:574768.
23. Zhao Q, Caballero OL, Davis ID, Jonasch E, Tamboli P, Yung WK, Weinstein JN, Kenna Shaw for Trn, Strausberg RL and Yao J. Tumor-specific isoform switch of the fibroblast growth factor receptor 2 underlies the mesenchymal and malignant phenotypes of clear cell renal cell carcinomas. Clinical cancer research. 2013; 19:2460-2472.
24. Ponta H, Sherman L and Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nature reviews Molecular cell biology. 2003; 4:33-45.
25. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA and Allan AL. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. Journal of cellular and molecular medicine. 2009; 13:2236-2252.
26. Koneczny I, Schulenburg A, Hudec X, Knofler M, Holzmann K, Piazza G, Reynolds R, Valent P and Marian B. Autocrine fibroblast growth factor 18 signaling mediates Wnt-dependent stimulation of CD44-positive human colorectal adenoma cells. Molecular carcinogenesis. 2015; 54:789-799.
27. Marzese DM, Liu M, Huynh JL, Hirose H, Donovan NC, Huynh KT, Kiyohara E, Chong K, Cheng D, Tanaka R, Wang J, Morton DL, Barkhoudarian G, Kelly DF and Hoon DS. Brain metastasis is predetermined in early stages of cutaneous melanoma by CD44v6 expression through epigenetic regulation of the spliceosome. Pigment cell & melanoma research. 2015; 28:82-93.
28. Toyoda A, Kawana H, Azuhata K, Yu J, Omata A, Kishi H, Higashi M and Harigaya K. Aberrant expression of human ortholog of mammalian enabled (hMena) in human colorectal carcinomas: implications for its role in tumor progression. International journal of oncology. 2009; 34:53-60.
29. Yao J, Caballero OL, Huang Y, Lin C, Rimoldi D, Behren A, Cebon JS, Hung MC, Weinstein JN, Strausberg RL and Zhao Q. Altered expression and splicing of ESRP1 in malignant melanoma correlates with epithelialmesenchymal status and tumor-associated immune cytolytic activity. Cancer immunology research. 2016.
30. Zhang J and Manley JL. Misregulation of pre-mRNA alternative splicing in cancer. Cancer discovery. 2013; 3:1228-1237.
31. de la Chapelle A and Hampel H. Clinical relevance of microsatellite instability in colorectal cancer. J Clin Oncol. 2010; 28:3380-3387.
32. Leontieva OV and Ionov Y. RNA-binding motif protein 35A is a novel tumor suppressor for colorectal cancer. Cell Cycle. 2009; 8:490-497.
33. Bertorelle R, Briarava M, Rampazzo E, Biasini L, Agostini M, Maretto I, Lonardi S, Friso ML, Mescoli C, Zagonel V, Nitti D, De Rossi A and Pucciarelli S. Telomerase is an independent prognostic marker of overall survival in patients with colorectal cancer. British journal of cancer. 2013; 108:278-284.
34. Drescher KM, Sharma P and Lynch HT. Current hypotheses on how microsatellite instability leads to enhanced survival of Lynch Syndrome patients. Clinical & developmental immunology. 2010; 2010:170432.
35. Tan TZ, Miow QH, Miki Y, Noda T, Mori S, Huang RY and Thiery JP. Epithelial-mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer patients. EMBO molecular medicine. 2014; 6:1279-1293.
36. Shia J. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part I. The utility of immunohistochemistry. The Journal of molecular diagnostics. 2008; 10:293-300.
37. Umar A, Boland CR, Terdiman JP, Syngal S, de la Chapelle A, Ruschoff J, Fishel R, Lindor NM, Burgart LJ, Hamelin R, Hamilton SR, Hiatt RA, Jass J, Lindblom A, Lynch HT, Peltomaki P, et al. Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. Journal of the National Cancer Institute. 2004; 96:261-268.
38. Sampl S, Pramhas S, Stern C, Preusser M, Marosi C and Holzmann K. Expression of telomeres in astrocytoma WHO grade 2 to 4: TERRA level correlates with telomere length, telomerase activity, and advanced clinical grade. Translational oncology. 2012; 5:56-65.
39. Schweiger N, Hauck M, Steinhoff H, Sampl S, Reifinger M, Walter I, Kreilmeier T, Marian B, Grusch M, Berger W, Holzmann K and Kleiter M. Canine and human sarcomas exhibit predominant FGFR1 expression and impaired viability after inhibition of signaling. Molecular carcinogenesis. 2015; 54:841-852.
40. Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012; 487:330-337.
41. Li B and Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics. 2011; 12:323.
42. Contal C and O'Quigley J. An application of changepoint methods in studying the effect of age on survival in breast cancer. Computational Statistics & Data Analysis. 1999; 30:253-270.
43. Lu L, Katsaros D, Canuto EM, Biglia N, Risch HA and Yu H. LIN-28B/let-7a/IGF-II axis molecular subtypes are associated with epithelial ovarian cancer prognosis. Gynecologic oncology. 2016.
44. Keirsebilck A, Bonne S, Staes K, van Hengel J, Nollet F, Reynolds A and van Roy F. Molecular cloning of the human p120ctn catenin gene (CTNND1): expression of multiple alternatively spliced isoforms. Genomics. 1998; 50:129-146.