Epidermal growth-factor - Induced transcript isoform variation drives mammary cell migration

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Köstler, Wolfgang J ^a,e   Zeisel, Amit ^a   Körner, Cindy ^b   Tsai, Jonathan M ^a,f   Jacob Hirsch, Jasmine ^c   Ben Chetrit, Nir ^a   Sharma, Kirti ^b   Cohen Dvashi, Hadas ^a   Yitzhaky, Assif ^a   Lader, Eric ^d   Tschulena, Ulrich ^b   Rechavi, Gideon ^c   Domany, Eytan ^a   Wiemann, Stefan ^b   Yarden, Yosef ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c TEL AVIV UNIVERSITY   (Israel)

^d QIAGEN   (United States)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; MESSENGER RNA; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; BREAST CELL; CANCER CELL; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; EXON; GENE; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; LAMA3 GENE; PHENOTYPE; PTHLH GENE; UPREGULATION;

ALTERNATIVE SPLICING; CELL LINE; CELL MOVEMENT; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; EXONS; FEMALE; GENETIC VARIATION; HUMANS; MAMMARY GLANDS, HUMAN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYADENYLATION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84891942332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080566     Document Type: Article

References (59)

1. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
2. 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)
3. Castle JC, Zhang C, Shah JK, Kulkarni AV, Kalsotra A, et al. (2008) Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat Genet 40: 1416-1425.
4. Kwan T, Grundberg E, Koka V, Ge B, Lam KC, et al. (2009) Tissue effect on genetic control of transcript isoform variation. PLoS genetics 5: e1000608.
5. Ameur A, Zaghlool A, Halvardson J, Wetterbom A, Gyllensten U, et al. (2011) Total RNA sequencing reveals nascent transcription and widespread cotranscriptional splicing in the human brain. Nature structural & molecular biology 18: 1435-1440.
6. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T (2011) Epigenetics in alternative pre-mRNA splicing. Cell 144: 16-26.
7. Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, et al. (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485: 201-206.
8. Gabut M, Samavarchi-Tehrani P, Wang X, Slobodeniuc V, O'Hanlon D, et al. (2011) An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming. Cell 147: 132-146.
9. Vorlova S, Rocco G, Lefave CV, Jodelka FM, Hess K, et al. (2011) Induction of antagonistic soluble decoy receptor tyrosine kinases by intronic polyA activation. Molecular cell 43: 927-939.
10. Amin EM, Oltean S, Hua J, Gammons MV, Hamdollah-Zadeh M, et al. (2011) WT1 mutants reveal SRPK1 to be a downstream angiogenesis target by altering VEGF splicing. Cancer Cell 20: 768-780.
11. Blaustein M, Pelisch F, Tanos T, Munoz MJ, Wengier D, et al. (2005) Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat Struct Mol Biol 12: 1037-1044. (Pubitemid 41746773)
12. Zhou Z, Qiu J, Liu W, Zhou Y, Plocinik RM, et al. (2012) The Akt-SRPK-SR Axis Constitutes a Major Pathway in Transducing EGF Signaling to Regulate Alternative Splicing in the Nucleus. Molecular cell.
13. Li C, Kato M, Shiue L, Shively JE, Ares M Jr, et al. (2006) Cell type and culture condition-dependent alternative splicing in human breast cancer cells revealed by splicing-sensitive microarrays. Cancer Res 66: 1990-1999.
14. Meng Q, Rayala SK, Gururaj AE, Talukder AH, O'Malley BW, et al. (2007) Signaling-dependent and coordinated regulation of transcription, splicing, and translation resides in a single coregulator, PCBP1. Proc Natl Acad Sci U S A 104: 5866-5871. (Pubitemid 47175625)
15. Nowak DG, Woolard J, Amin EM, Konopatskaya O, Saleem MA, et al. (2008) Expression of pro- and anti-angiogenic isoforms of VEGF is differentially regulated by splicing and growth factors. Journal of cell science 121: 3487-3495.
16. Goncalves V, Matos P, Jordan P (2008) The beta-catenin/TCF4 pathway modifies alternative splicing through modulation of SRp20 expression. RNA 14: 2538-2549.
17. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB (2008) Proliferating cells express mRNAs with shortened 39 untranslated regions and fewer microRNA target sites. Science 320: 1643-1647. (Pubitemid 351931255)
18. Oberdoerffer S, Moita LF, Neems D, Freitas RP, Hacohen N, et al. (2008) Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNPLL. Science 321: 686-691.
19. Grigoryev YA, Kurian SM, Nakorchevskiy AA, Burke JP, Campbell D, et al. (2009) Genome-wide analysis of immune activation in human T and B cells reveals distinct classes of alternatively spliced genes. PLoS ONE 4: e7906.
20. Yoon OK, Hsu TY, Im JH, Brem RB (2012) Genetics and regulatory impact of alternative polyadenylation in human B-lymphoblastoid cells. PLoS genetics 8: e1002882.
21. Hang X, Li P, Li Z, Qu W, Yu Y, et al. (2009) Transcription and splicing regulation in human umbilical vein endothelial cells under hypoxic stress conditions by exon array. BMC Genomics 10: 126.
22. Rajan P, Dalgliesh C, Carling PJ, Buist T, Zhang C, et al. (2011) Identification of novel androgen-regulated pathways and mRNA isoforms through genomewide exon-specific profiling of the LNCaP transcriptome. PLoS ONE 6: e29088.
23. Zhang LQ, Cheranova D, Gibson M, Ding S, Heruth DP, et al. (2012) RNA-seq reveals novel transcriptome of genes and their isoforms in human pulmonary microvascular endothelial cells treated with thrombin. PLoS ONE 7: e31229.
24. Hartmann B, Castelo R, Blanchette M, Boue S, Rio DC, et al. (2009) Global analysis of alternative splicing regulation by insulin and wingless signaling in Drosophila cells. Genome biology 10: R11.
25. Singer GA, Wu J, Yan P, Plass C, Huang TH, et al. (2008) Genome-wide analysis of alternative promoters of human genes using a custom promoter tiling array. BMC Genomics 9: 349.
26. McKee AE, Neretti N, Carvalho LE, Meyer CA, Fox EA, et al. (2007) Exon expression profiling reveals stimulus-mediated exon use in neural cells. Genome biology 8: R159.
27. Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, et al. (2007) A posttranscriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21: 1636-1652. (Pubitemid 47026368)
28. Amit I, Citri A, Shay T, Lu Y, Katz M, et al. (2007) A module of negative feedback regulators defines growth factor signaling. Nat Genet 39: 503-512. (Pubitemid 46514770)
29. Yarden Y, Sliwkowski MX (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2: 127-137. (Pubitemid 33674041)
30. Katz M, Amit I, Citri A, Shay T, Carvalho S, et al. (2007) A reciprocal tensin-3- cten switch mediates EGF-driven mammary cell migration. Nat Cell Biol 9: 961-969. (Pubitemid 47190451)
31. Simpson KJ, Selfors LM, Bui J, Reynolds A, Leake D, et al. (2008) Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 10: 1027-1038.
32. Tarcic G, Avraham R, Pines G, Amit I, Shay T, et al. (2012) EGR1 and the ERK-ERF axis drive mammary cell migration in response to EGF. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 26: 1582-1592.
33. Zeisel A, Kostler WJ, Molotski N, Tsai JM, Krauthgamer R, et al. (2011) Coupled pre-mRNA and mRNA dynamics unveil operational strategies underlying transcriptional responses to stimuli. Molecular systems biology 7: 529.
34. Welcker M, Orian A, Grim JE, Eisenman RN, Clurman BE (2004) A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Current biology: CB 14: 1852-1857. (Pubitemid 39412248)
35. Lin KT, Gong J, Li CF, Jang TH, Chen WL, et al. (2012) Vav3-Rac1 Signaling Regulates Prostate Cancer Metastasis with Elevated Vav3 Expression Correlating with Prostate Cancer Progression and Posttreatment Recurrence. Cancer research.
36. Huser CA, Pringle MA, Heath VJ, Bell AK, Kendrick H, et al. (2010) TSC- 22D1 isoforms have opposing roles in mammary epithelial cell survival. Cell death and differentiation 17: 304-315.
37. Liu Y, Ren S, Castellanos-Martin A, Perez-Losada J, Kwon YW, et al. (2012) Multiple novel alternative splicing forms of FBXW7alpha have a translational modulatory function and show specific alteration in human cancer. PLoS ONE 7: e49453.
38. Vitorino P, Meyer T (2008) Modular control of endothelial sheet migration. Genes Dev 22: 3268-3281.
39. Prinos P, Garneau D, Lucier JF, Gendron D, Couture S, et al. (2011) Alternative splicing of SYK regulates mitosis and cell survival. Nature structural & molecular biology 18: 673-679.
40. Zeisel A, Yitzhaky A, Koerner C, Lauriola M, Cohen-Dvashi H, et al. (2012) qCMA: A Desktop Application for Quantitative Collective Cell Migration Analysis. Journal of Biomolecular Screening: [Epub ahead of print].
41. Goldberg MS, Sharp PA (2012) Pyruvate kinase M2-specific siRNA induces apoptosis and tumor regression. The Journal of experimental medicine 209: 217-224.
42. Bar-Joseph Z, Gitter A, Simon I (2012) Studying and modelling dynamic biological processes using time-series gene expression data. Nature reviews Genetics 13: 552-564.
43. Hamill KJ, Paller AS, Jones JC (2010) Adhesion and migration, the diverse functions of the laminin alpha3 subunit. Dermatologic clinics 28: 79-87.
44. Ryan MC, Tizard R, VanDevanter DR, Carter WG (1994) Cloning of the LamA3 gene encoding the alpha 3 chain of the adhesive ligand epiligrin. Expression in wound repair. The Journal of biological chemistry 269: 22779-22787.
45. Hamill KJ, Langbein L, Jones JC, McLean WH (2009) Identification of a novel family of laminin N-terminal alternate splice isoforms: structural and functional characterization. The Journal of biological chemistry 284: 35588-35596.
46. Miller KA, Chung J, Lo D, Jones JC, Thimmapaya B, et al. (2000) Inhibition of laminin-5 production in breast epithelial cells by overexpression of p300. The Journal of biological chemistry 275: 8176-8182. (Pubitemid 30159733)
47. Virolle T, Djabari Z, Ortonne JP, Aberdam D (2000) DNA conformation driven by AP-1 triggers cell-specific expression via a strong epithelial enhancer. EMBO reports 1: 328-333.
48. Dietze EC, Bowie ML, Mrozek K, Caldwell LE, Neal C, et al. (2005) CREBbinding protein regulates apoptosis and growth of HMECs grown in reconstituted ECM via laminin-5. Journal of cell science 118: 5005-5022. (Pubitemid 41672432)
49. Virolle T, Coraux C, Ferrigno O, Cailleteau L, Ortonne JP, et al. (2002) Binding of USF to a non-canonical E-box following stress results in a cell-specific derepression of the lama3 gene. Nucleic acids research 30: 1789-1798. (Pubitemid 34679757)
50. Moller-Levet CS, Betts GN, Harris AL, Homer JJ, West CM, et al. (2009) Exon array analysis of head and neck cancers identifies a hypoxia related splice variant of LAMA3 associated with a poor prognosis. PLoS computational biology 5: e1000571.
51. Li J, Karaplis AC, Huang DC, Siegel PM, Camirand A, et al. (2011) PTHrP drives breast tumor initiation, progression, and metastasis in mice and is a potential therapy target. The Journal of clinical investigation 121: 4655-4669.
52. Nakamura M, Hashimoto T, Furuyama J, Kakudo K (1995) Multiple alternative splice isoforms of parathyroid hormone-related peptide mRNA in human cell lines. Journal of molecular endocrinology 15: 245-249.
53. Wu G, Iwamura M, di Sant'Agnese PA, Deftos LJ, Cockett AT, et al. (1998) Characterization of the cell-specific expression of parathyroid hormone-related protein in normal and neoplastic prostate tissue. Urology 51: 110-120. (Pubitemid 28267886)
54. Bouizar Z, Spyratos F, De vernejoul MC (1999) The parathyroid hormonerelated protein (PTHrP) gene: use of downstream TATA promotor and PTHrP 1-139 coding pathways in primary breast cancers vary with the occurrence of bone metastasis. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 14: 406-414. (Pubitemid 29106717)
55. Southby J, Murphy LM, Martin TJ, Gillespie MT (1996) Cell-specific and regulator-induced promoter usage and messenger ribonucleic acid splicing for parathyroid hormone-related protein. Endocrinology 137: 1349-1357. (Pubitemid 26095252)
56. Zeisel A, Amir A, Kostler WJ, Domany E (2010) Intensity dependent estimation of noise in microarrays improves detection of differentially expressed genes. BMC Bioinformatics 11: 400.
57. Celotto AM, Graveley BR (2002) Exon-specific RNAi: a tool for dissecting the functional relevance of alternative splicing. RNA 8: 718-724. (Pubitemid 34620449)
58. Huesken D, Lange J, Mickanin C, Weiler J, Asselbergs F, et al. (2005) Design of a genome-wide siRNA library using an artificial neural network. Nature biotechnology 23: 995-1001. (Pubitemid 41114034)
59. Yata K, Lloyd J, Maslen S, Bleuyard JY, Skehel M, et al. (2012) Plk1 and CK2 act in concert to regulate Rad51 during DNA double strand break repair. Molecular cell 45: 371-383.