Alternative splicing of VEGFA, APP and NUMB genes in colorectal cancer

World Journal of Gastroenterology

Volumn 21, Issue 21, 2015, Pages 6550-6560

  Zhao, Yi Jun ^a   Han, Hua Zhong ^a   Liang, Yong ^b   Shi, Chen Zhang ^a   Zhu, Qing Chao ^a   Yang, Jun ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Alternative splicing; Amyloid beta precursor protein; Colorectal cancer; Numb homolog; Vascular endothelial growth factor A

Indexed keywords

AMYLOID BETA PRECURSOR PROTEIN GENE; ARTICLE; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; MALE; NUMB HOMOLOG GENE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; VASCULOTROPIN A GENE; ADENOCARCINOMA; ALTERNATIVE RNA SPLICING; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY;

AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; MEMBRANE PROTEIN; MESSENGER RNA; NERVE PROTEIN; NUMB PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ADENOCARCINOMA; ALTERNATIVE SPLICING; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; AMYLOID BETA-PROTEIN PRECURSOR; COLORECTAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84930811619     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i21.6550     Document Type: Article

References (53)

1. Kornblihtt AR, Schor IE, Alló M, Dujardin G, Petrillo E, Muñoz MJ. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 2013; 14: 153-165 [PMID: 23385723 DOI: 10.1038/nrm3525]
2. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008; 40: 1413-1415 [PMID: 18978789 DOI: 10.1038/ng.259]
3. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008; 456: 470-476 [PMID: 18978772 DOI: 10.1038/nature07509]
4. Cowper AE, Cáceres JF, Mayeda A, Screaton GR. Serine-arginine (SR) protein-like factors that antagonize authentic SR proteins and regulate alternative splicing. J Biol Chem 2001; 276: 48908-48914 [PMID: 11684676 DOI: 10.1074/jbc.M103967200]
5. Martinez-Contreras R, Fisette JF, Nasim FU, Madden R, Cordeau M, Chabot B. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol 2006; 4: e21 [PMID: 16396608 DOI: 10.1371/journal.pbio.0040021]
6. Tazi J, Bakkour N, Stamm S. Alternative splicing and disease. Biochim Biophys Acta 2009; 1792: 14-26 [PMID: 18992329 DOI: 10.1016/j.bbadis.2008.09.017]
7. Klinck R, Bramard A, Inkel L, Dufresne-Martin G, Gervais-Bird J, Madden R, Paquet ER, Koh C, Venables JP, Prinos P, Jilaveanu-Pelmus M, Wellinger R, Rancourt C, Chabot B, Abou Elela S. Multiple alternative splicing markers for ovarian cancer. Cancer Res 2008; 68: 657-663 [PMID: 18245464 DOI: 10.1158/0008-5472.can-07-2580]
8. Kim E, Goren A, Ast G. Alternative splicing and disease. RNA Biol 2008; 5: 17-19 [PMID: 18388487 DOI: 10.4161/rna.5.1.5944]
9. Thorsen K, Sørensen KD, Brems-Eskildsen AS, Modin C, Gaustadnes M, Hein AM, Kruhøffer M, Laurberg S, Borre M, Wang K, Brunak S, Krainer AR, Tørring N, Dyrskjøt L, Andersen CL, Orntoft TF. Alternative splicing in colon, bladder, and prostate cancer identified by exon array analysis. Mol Cell Proteomics 2008; 7: 1214-1224 [PMID: 18353764 DOI: 10.1074/mcp.M700590-MCP200]
10. Misquitta-Ali CM, Cheng E, O'Hanlon D, Liu N, McGlade CJ, Tsao MS, Blencowe BJ. Global profiling and molecular characterization of alternative splicing events misregulated in lung cancer. Mol Cell Biol 2011; 31: 138-150 [PMID: 21041478 DOI: 10.1128/mcb.00709-10]
11. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell 2009; 136: 777-793 [PMID: 19239895 DOI: 10.1016/j.cell.2009.02.011]
12. Dutertre M, Vagner S, Auboeuf D. Alternative splicing and breast cancer. RNA Biol 2010; 7: 403-411 [PMID: 20622514 DOI: 10.4161/rna.7.4.12152]
13. Venables JP, Klinck R, Koh C, Gervais-Bird J, Bramard A, Inkel L, Durand M, Couture S, Froehlich U, Lapointe E, Lucier JF, Thibault P, Rancourt C, Tremblay K, Prinos P, Chabot B, Elela SA. Cancer-associated regulation of alternative splicing. Nat Struct Mol Biol 2009; 16: 670-676 [PMID: 19448617 DOI: 10.1038/nsmb.1608]
14. Kelemen O, Convertini P, Zhang Z, Wen Y, Shen M, Falaleeva M, Stamm S. Function of alternative splicing. Gene 2013; 514: 1-30 [PMID: 22909801 DOI: 10.1016/j.gene.2012.07.083]
15. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246: 1306-1309 [PMID: 2479986 DOI: 10.1126/science.2479986]
16. Karathanasis E, Chan L, Karumbaiah L, McNeeley K, D'Orsi CJ, Annapragada AV, Sechopoulos I, Bellamkonda RV. Tumor vascular permeability to a nanoprobe correlates to tumor-specific expression levels of angiogenic markers. PLoS One 2009; 4: e5843 [PMID: 19513111 DOI: 10.1371/journal.pone.0005843]
17. Siegel R, Desantis C, Jemal A. Colorectal cancer statistics, 2014. CA Cancer J Clin 2014; 64: 104-117 [PMID: 24639052 DOI: 10.3322/caac.21220]
18. Key TJ, Allen NE, Spencer EA, Travis RC. The effect of diet on risk of cancer. Lancet 2002; 360: 861-868 [PMID: 12243933 DOI: 10.1016/s0140-6736(02)09958-0]
19. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res 1995; 55: 3964-3968 [PMID: 7664263]
20. Harper SJ, Bates DO. VEGF-A splicing: the key to antiangiogenic therapeutics? Nat Rev Cancer 2008; 8: 880-887 [PMID: 18923433 DOI: 10.1038/nrc2505]
21. Cheung N, Wong MP, Yuen ST, Leung SY, Chung LP. Tissue-specific expression pattern of vascular endothelial growth factor isoforms in the malignant transformation of lung and colon. Hum Pathol 1998; 29: 910-914 [PMID: 9744306 DOI: 10.1016/S0046-8177(98)90195-2]
22. Ferrara N. The role of vascular endothelial growth factor in pathological angiogenesis. Breast Cancer Res Treat 1995; 36: 127-137 [PMID: 8534862 DOI: 10.1007/BF00666035]
23. Zhang HT, Scott PA, Morbidelli L, Peak S, Moore J, Turley H, Harris AL, Ziche M, Bicknell R. The 121 amino acid isoform of vascular endothelial growth factor is more strongly tumorigenic than other splice variants in vivo. Br J Cancer 2000; 83: 63-68 [PMID: 10883669 DOI: 10.1054/bjoc.2000.1279]
24. Yu JL, Rak JW, Klement G, Kerbel RS. Vascular endothelial growth factor isoform expression as a determinant of blood vessel patterning in human melanoma xenografts. Cancer Res 2002; 62: 1838-1846 [PMID: 11912163]
25. Pritchard-Jones RO, Dunn DB, Qiu Y, Varey AH, Orlando A, Rigby H, Harper SJ, Bates DO. Expression of VEGF(xxx)b, the inhibitory isoforms of VEGF, in malignant melanoma. Br J Cancer 2007; 97: 223-230 [PMID: 17595666 DOI: 10.1038/sj.bjc.6603839]
26. Zygalaki E, Tsaroucha EG, Kaklamanis L, Lianidou ES. Quantitative real-time reverse transcription PCR study of the expression of vascular endothelial growth factor (VEGF) splice variants and VEGF receptors (VEGFR-1 and VEGFR-2) in non small cell lung cancer. Clin Chem 2007; 53: 1433-1439 [PMID: 17599955 DOI: 10.1373/clinchem.2007.086819]
27. Matsuyama M, Chijiwa T, Inoue Y, Abe Y, Nishi M, Miyazaki N, Furukawa D, Mukai M, Suemizu H, Sekido Y, Ueyama Y, Nakamura M. Alternative splicing variant of vascular endothelial growth factor-A is a critical prognostic factor in non-small cell lung cancer. Oncol Rep 2009; 22: 1407-1413 [PMID: 19885594]
28. Hyder SM, Chiappetta C, Stancel GM. Pharmacological and endogenous progestins induce vascular endothelial growth factor expression in human breast cancer cells. Int J Cancer 2001; 92: 469-473 [PMID: 11304678 DOI: 10.1002/ijc.1236]
29. Stimpfl M, Tong D, Fasching B, Schuster E, Obermair A, Leodolter S, Zeillinger R. Vascular endothelial growth factor splice variants and their prognostic value in breast and ovarian cancer. Clin Cancer Res 2002; 8: 2253-2259 [PMID: 12114428]
30. Catena R, Muniz-Medina V, Moralejo B, Javierre B, Best CJ, Emmert-Buck MR, Green JE, Baker CC, Calvo A. Increased expression of VEGF121/VEGF165-189 ratio results in a significant enhancement of human prostate tumor angiogenesis. Int J Cancer 2007; 120: 2096-2109 [PMID: 17278099 DOI: 10.1002/ijc.22461]
31. Fauconnet S, Bernardini S, Lascombe I, Boiteux G, Clairotte A, Monnien F, Chabannes E, Bittard H. Expression analysis of VEGF-A and VEGF-B: relationship with clinicopathological parameters in bladder cancer. Oncol Rep 2009; 21: 1495-1504 [PMID: 19424629]
32. Woolard J, Wang WY, Bevan HS, Qiu Y, Morbidelli L, Pritchard-Jones RO, Cui TG, Sugiono M, Waine E, Perrin R, Foster R, Digby-Bell J, Shields JD, Whittles CE, Mushens RE, Gillatt DA, Ziche M, Harper SJ, Bates DO. VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res 2004; 64: 7822-7835 [PMID: 15520188 DOI: 10.1158/0008-5472.can-04-0934]
33. Perrin RM, Konopatskaya O, Qiu Y, Harper S, Bates DO, Churchill AJ. Diabetic retinopathy is associated with a switch in splicing from anti- to pro-angiogenic isoforms of vascular endothelial growth factor. Diabetologia 2005; 48: 2422-2427 [PMID: 16193288 DOI: 10.1007/s00125-005-1951-8]
34. Díaz R, Peña C, Silva J, Lorenzo Y, García V, García JM, Sánchez A, Espinosa P, Yuste R, Bonilla F, Domínguez G. p73 Isoforms affect VEGF, VEGF165b and PEDF expression in human colorectal tumors: VEGF165b downregulation as a marker of poor prognosis. Int J Cancer 2008; 123: 1060-1067 [PMID: 18546269 DOI: 10.1002/ijc.23619]
35. Varey AH, Rennel ES, Qiu Y, Bevan HS, Perrin RM, Raffy S, Dixon AR, Paraskeva C, Zaccheo O, Hassan AB, Harper SJ, Bates DO. VEGF 165 b, an antiangiogenic VEGF-A isoform, binds and inhibits bevacizumab treatment in experimental colorectal carcinoma: balance of pro- and antiangiogenic VEGF-A isoforms has implications for therapy. Br J Cancer 2008; 98: 1366-1379 [PMID: 18349829 DOI: 10.1038/sj.bjc.6604308]
36. Rennel E, Waine E, Guan H, Schüler Y, Leenders W, Woolard J, Sugiono M, Gillatt D, Kleinerman E, Bates D, Harper S. The endogenous anti-angiogenic VEGF isoform, VEGF165b inhibits human tumour growth in mice. Br J Cancer 2008; 98: 1250-1257 [PMID: 18349828 DOI: 10.1038/sj.bjc.6604309]
37. Rennel ES, Hamdollah-Zadeh MA, Wheatley ER, Magnussen A, Schüler Y, Kelly SP, Finucane C, Ellison D, Cebe-Suarez S, Ballmer-Hofer K, Mather S, Stewart L, Bates DO, Harper SJ. Recombinant human VEGF165b protein is an effective anticancer agent in mice. Eur J Cancer 2008; 44: 1883-1894 [PMID: 18657413 DOI: 10.1016/j.ejca.2008.05.027]
38. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski BL, Lieberburg I, Koo EH, Schenk D, Teplow DB. Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 1992; 359: 322-325 [PMID: 1383826 DOI: 10.1038/359322a0]
39. Yankner BA. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 1996; 16: 921-932 [PMID: 8630250]
40. Hansel DE, Rahman A, Wehner S, Herzog V, Yeo CJ, Maitra A. Increased expression and processing of the Alzheimer amyloid precursor protein in pancreatic cancer may influence cellular proliferation. Cancer Res 2003; 63: 7032-7037 [PMID: 14612490]
41. Ko SY, Lin SC, Chang KW, Wong YK, Liu CJ, Chi CW, Liu TY. Increased expression of amyloid precursor protein in oral squamous cell carcinoma. Int J Cancer 2004; 111: 727-732 [PMID: 15252842 DOI: 10.1002/ijc.20328]
42. Krause K, Karger S, Sheu SY, Aigner T, Kursawe R, Gimm O, Schmid KW, Dralle H, Fuhrer D. Evidence for a role of the amyloid precursor protein in thyroid carcinogenesis. J Endocrinol 2008; 198: 291-299 [PMID: 18480379 DOI: 10.1677/joe-08-0005]
43. Takayama K, Tsutsumi S, Suzuki T, Horie-Inoue K, Ikeda K, Kaneshiro K, Fujimura T, Kumagai J, Urano T, Sakaki Y, Shirahige K, Sasano H, Takahashi S, Kitamura T, Ouchi Y, Aburatani H, Inoue S. Amyloid precursor protein is a primary androgen target gene that promotes prostate cancer growth. Cancer Res 2009; 69: 137-142 [PMID: 19117996 DOI: 10.1158/0008-5472.can-08-3633]
44. Cáceres J, Brandan E. Interaction between Alzheimer's disease beta A4 precursor protein (APP) and the extracellular matrix: evidence for the participation of heparan sulfate proteoglycans. J Cell Biochem 1997; 65: 145-158 [PMID: 9136074]
45. Sandhu FA, Kim Y, Lapan KA, Salim M, Aliuddin V, Zain SB. Expression of the C terminus of the amyloid precursor protein alters growth factor responsiveness in stably transfected PC12 cells. Proc Natl Acad Sci USA 1996; 93: 2180-2185 [PMID: 8700905]
46. Ponte P, Gonzalez-DeWhitt P, Schilling J, Miller J, Hsu D, Greenberg B, Davis K, Wallace W, Lieberburg I, Fuller F. A new A4 amyloid mRNA contains a domain homologous to serine proteinase inhibitors. Nature 1988; 331: 525-527 [PMID: 2893289 DOI: 10.1038/331525a0]
47. Wang Z, Sandiford S, Wu C, Li SS. Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling. EMBO J 2009; 28: 2360-2373 [PMID: 19609305 DOI: 10.1038/emboj.2009.190]
48. Cheng X, Huber TL, Chen VC, Gadue P, Keller GM. Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development 2008; 135: 3447-3458 [PMID: 18799543 DOI: 10.1242/dev.025916]
49. Ho L, Alman B. Protecting the hedgerow: p53 and hedgehog pathway interactions. Cell Cycle 2010; 9: 506-511 [PMID: 20081367]
50. Colaluca IN, Tosoni D, Nuciforo P, Senic-Matuglia F, Galimberti V, Viale G, Pece S, Di Fiore PP. NUMB controls p53 tumour suppressor activity. Nature 2008; 451: 76-80 [PMID: 18172499 DOI: 10.1038/nature06412]
51. Bani-Yaghoub M, Kubu CJ, Cowling R, Rochira J, Nikopoulos GN, Bellum S, Verdi JM. A switch in numb isoforms is a critical step in cortical development. Dev Dyn 2007; 236: 696-705 [PMID: 17253625 DOI: 10.1002/dvdy.21072]
52. Verdi JM, Bashirullah A, Goldhawk DE, Kubu CJ, Jamali M, Meakin SO, Lipshitz HD. Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc Natl Acad Sci USA 1999; 96: 10472-10476 [PMID: 10468633]
53. Zhang C, Frias MA, Mele A, Ruggiu M, Eom T, Marney CB, Wang H, Licatalosi DD, Fak JJ, Darnell RB. Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls. Science 2010; 329: 439-443 [PMID: 20558669 DOI: 10.1126/science.1191150]