The RNA Binding Protein ESRP1 Fine-Tunes the Expression of Pluripotency-Related Factors in Mouse Embryonic Stem Cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Fagoonee, Sharmila ^a   Bearzi, Claudia ^b,c   Di Cunto, Ferdinando ^a   Clohessy, John G ^d   Rizzi, Roberto ^b,c   Reschke, Markus ^d   Tolosano, Emanuela ^a   Provero, Paolo ^a   Pandolfi, Pier Paolo ^d   Silengo, Lorenzo ^a   Altruda, Fiorella ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b IRCCS MULTIMEDICA   (Italy)

^c CNR   (Italy)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; RNA BINDING PROTEIN; RNA BINDING PROTEIN ESRP1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL RENEWAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REGULATORY MECHANISM; TERATOMA; TRANSCRIPTION REGULATION; TUMOR VOLUME;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; EMBRYONIC STEM CELLS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84883193285     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072300     Document Type: Article

References (48)

1. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
2. Niwa H, Miyazaki J, Smith AG, (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24: 372-376.
3. Pei D, (2009) Regulation of pluripotency and reprogramming by transcription factors. J Biol Chem 284: 3365-3369.
4. Kopp JL, Ormsbee BD, Desler M, Rizzino A, (2008) Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells. Stem Cells 26: 903-911.
5. Lengerke C, Fehm T, Kurth R, Neubauer H, Scheble V, et al. (2011) Expression of the embryonic stem cell marker SOX2 in early-stage breast carcinoma. BMC Cancer 11: 42.
6. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, et al. (2005) Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280: 24731-24737.
7. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, et al. (2009) Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 18: 1093-1108.
8. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS, (2009) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137: 647-658.
9. Sampath P, Pritchard DK, Pabon L, Reinecke H, Schwartz SM, et al. (2008) A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2: 448-460.
10. Heinrich EM, Dimmeler S, (2012) MicroRNAs and stem cells: control of pluripotency, reprogramming, and lineage commitment. Circ Res 110: 1014-1022.
11. Martinez NJ, Gregory RI, (2010) MicroRNA gene regulatory pathways in the establishment and maintenance of ESC identity. Cell Stem Cell 7: 31-35.
12. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, et al. (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501.
13. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R, (2007) DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 39: 380-385.
14. Elatmani H, Dormoy-Raclet V, Dubus P, Dautry F, Chazaud C, et al. (2011) The RNA-binding protein Unr prevents mouse embryonic stem cells differentiation toward the primitive endoderm lineage. Stem Cells 29: 1504-1516.
15. Narva E, Rahkonen N, Emani MR, Lund R, Pursiheimo JP, et al. (2012) RNA-binding protein L1TD1 interacts with LIN28 via RNA and is required for human embryonic stem cell self-renewal and cancer cell proliferation. Stem Cells 30: 452-460.
16. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, et al. (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300.
17. Wright JE, Ciosk R, (2013) RNA-based regulation of pluripotency. Trends Genet 29: 99-107.
18. Abujarour R, Efe J, Ding S, (2010) Genome-wide gain-of-function screen identifies novel regulators of pluripotency. Stem Cells 28: 1487-1497.
19. Piro RM, Ala U, Molineris I, Grassi E, Bracco C, et al. (2011) An atlas of tissue-specific conserved coexpression for functional annotation and disease gene prediction. Eur J Hum Genet 19: 1173-1180.
20. Ivanov I, Lo KC, Hawthorn L, Cowell JK, Ionov Y, (2007) Identifying candidate colon cancer tumor suppressor genes using inhibition of nonsense-mediated mRNA decay in colon cancer cells. Oncogene 26: 2873-2884.
21. Wakayama T, Rodriguez I, Perry AC, Yanagimachi R, Mombaerts P, (1999) Mice cloned from embryonic stem cells. Proc Natl Acad Sci U S A 96: 14984-14989.
22. Fagoonee S, Hobbs RM, De Chiara L, Cantarella D, Piro RM, et al. (2010) Generation of functional hepatocytes from mouse germ line cell-derived pluripotent stem cells in vitro. Stem Cells Dev 19: 1183-1194.
23. Hobbs RM, Seandel M, Falciatori I, Rafii S, Pandolfi PP, (2010) Plzf regulates germline progenitor self-renewal by opposing mTORC1. Cell 142: 468-479.
24. Ryu BY, Kubota H, Avarbock MR, Brinster RL, (2005) Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci U S A 102: 14302-14307.
25. Hobbs RM, Fagoonee S, Papa A, Webster K, Altruda F, et al. (2012) Functional antagonism between Sall4 and Plzf defines germline progenitors. Cell Stem Cell 10: 284-298.
26. Bussolati B, Moggio A, Collino F, Aghemo G, D'Armento G, et al. (2012) Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133+ progenitors through Oct4/miR-145 balance. Am J Physiol Renal Physiol 302: F116-128.
27. Bussolati B, Bruno S, Grange C, Ferrando U, Camussi G, (2008) Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J 22: 3696-3705.
28. Tanimura N, Saito M, Ebisuya M, Nishida E, Ishikawa F, (2013) Stemness-related factor Sall4 interacts with transcription factors Oct-3/4 and Sox2 and occupies Oct-Sox elements in mouse embryonic stem cells. J Biol Chem 288: 5027-5038.
29. Ge Y, Zhou F, Chen H, Cui C, Liu D, et al. (2010) Sox2 is translationally activated by eukaryotic initiation factor 4E in human glioma-initiating cells. Biochem Biophys Res Commun 397: 711-717.
30. Zhang J, Tam WL, Tong GQ, Wu Q, Chan HY, et al. (2006) Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat Cell Biol 8: 1114-1123.
31. Madan B, Madan V, Weber O, Tropel P, Blum C, et al. (2009) The pluripotency-associated gene Dppa4 is dispensable for embryonic stem cell identity and germ cell development but essential for embryogenesis. Mol Cell Biol 29: 3186-3203.
32. Leontieva OV, Ionov Y, (2009) RNA-binding motif protein 35A is a novel tumor suppressor for colorectal cancer. Cell Cycle 8: 490-497.
33. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP, (2009) ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell 33: 591-601.
34. Rizzi R, Di Pasquale E, Portararo P, Papait R, Cattaneo P, et al. (2012) Post-natal cardiomyocytes can generate iPS cells with an enhanced capacity toward cardiomyogenic re-differentation. Cell Death Differ 19: 1162-1174.
35. Samavarchi-Tehrani P, Golipour A, David L, Sung HK, Beyer TA, et al. (2010) Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 7: 64-77.
36. Kang NY, Yun SW, Ha HH, Park SJ, Chang YT, (2011) Embryonic and induced pluripotent stem cell staining and sorting with the live-cell fluorescence imaging probe CDy1. Nat Protoc 6: 1044-1052.
37. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, et al. (2005) Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 174: 6477-6489.
38. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, et al. (2007) Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449: 346-350.
39. Tolkunova EN, Malashicheva AB, Chikhirzhina EV, Kostyleva EI, Zeng W, et al. (2009) [E-cadherin as a novel surface marker of spermatogonial stem cells]. Tsitologiia 51: 212-218.
40. Jin J, Jing W, Lei XX, Feng C, Peng S, et al. (2011) Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes. Nucleic Acids Res 39: 3724-3734.
41. Warzecha CC, Shen S, Xing Y, Carstens RP, (2009) The epithelial splicing factors ESRP1 and ESRP2 positively and negatively regulate diverse types of alternative splicing events. RNA Biol 6: 546-562.
42. Warzecha CC, Jiang P, Amirikian K, Dittmar KA, Lu H, et al. (2010) An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO J 29: 3286-3300.
43. Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, et al. (2011) CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Invest 121: 1064-1074.
44. Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, et al. (2012) Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun 3: 883.
45. Di Modugno F, Iapicca P, Boudreau A, Mottolese M, Terrenato I, et al. (2012) Splicing program of human MENA produces a previously undescribed isoform associated with invasive, mesenchymal-like breast tumors. Proc Natl Acad Sci U S A 109: 19280-19285.
46. Chen X, Xu H, Yuan P, Fang F, Huss M, et al. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
47. Walker E, Chang WY, Hunkapiller J, Cagney G, Garcha K, et al. (2010) Polycomb-like 2 associates with PRC2 and regulates transcriptional networks during mouse embryonic stem cell self-renewal and differentiation. Cell Stem Cell 6: 153-166.
48. Wurth L, (2012) Versatility of RNA-Binding Proteins in Cancer. Comp Funct Genomics 2012: 178525.