About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 623978, 12 pages
http://dx.doi.org/10.1155/2013/623978
Review Article

Functions of Heterogeneous Nuclear Ribonucleoproteins in Stem Cell Potency and Differentiation

1Department of Cardiology, The First Affiliated Hospital, School of Medicine, Zhejiang University, 79 Qingchun Road, Hangzhou, Zhejiang 310003, China
2Department of Reproductive Endocrinology, Women’s Hospital, Zhejiang University School of Medicine, 1 Xueshi Road, Hangzhou, Zhejiang 310006, China
3Centre for Clinical Pharmacology, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London EC1M 6BQ, UK

Received 29 April 2013; Revised 2 July 2013; Accepted 4 July 2013

Academic Editor: Jerome Moreaux

Copyright © 2013 Qishan Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. I. L. Weissman, “Stem cells: units of development, units of regeneration, and units in evolution,” Cell, vol. 100, no. 1, pp. 157–168, 2000. View at Scopus
  2. M. J. Evans and M. H. Kaufman, “Establishment in culture of pluripotential cells from mouse embryos,” Nature, vol. 292, no. 5819, pp. 154–156, 1981. View at Scopus
  3. G. Keller, “Embryonic stem cell differentiation: emergence of a new era in biology and medicine,” Genes & Development, vol. 19, no. 10, pp. 1129–1155, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Jaenisch and R. Young, “Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming,” Cell, vol. 132, no. 4, pp. 567–582, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Mimeault and S. K. Batra, “Recent progress on tissue-resident adult stem cell biology and their therapeutic implications,” Stem Cell Reviews, vol. 4, no. 1, pp. 27–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. A. C. Brignier and A. M. Gewirtz, “Embryonic and adult stem cell therapy,” Journal of Allergy and Clinical Immunology, vol. 125, no. 2, pp. S336–S344, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Li and H. Clevers, “Coexistence of quiescent and active adult stem cells in mammals,” Science, vol. 327, no. 5965, pp. 542–545, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Yu, M. A. Vodyanik, K. Smuga-Otto et al., “Induced pluripotent stem cell lines derived from human somatic cells,” Science, vol. 318, no. 5858, pp. 1917–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Bellin, M. C. Marchetto, F. H. Gage, and C. L. Mummery, “Induced pluripotent stem cells: the new patient?” Nature Reviews Molecular Cell Biology, vol. 13, pp. 713–726, 2012.
  11. S. M. Wu and K. Hochedlinger, “Harnessing the potential of induced pluripotent stem cells for regenerative medicine,” Nature Cell Biology, vol. 13, no. 5, pp. 497–505, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. D. A. Robinton and G. Q. Daley, “The promise of induced pluripotent stem cells in research and therapy,” Nature, vol. 481, no. 7381, pp. 295–305, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Zhu and D. Huangfu, “Human pluripotent stem cells: an emerging model in al biology,” Development, vol. 140, pp. 705–717, 2013.
  14. G. Dreyfuss, M. J. Matunis, S. Piñol-Roma, and C. G. Burd, “hnRNP proteins and the biogenesis of mRNA,” Annual Review of Biochemistry, vol. 62, pp. 289–321, 1993. View at Scopus
  15. F. Weighardt, G. Biamonti, and S. Riva, “The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism,” BioEssays, vol. 18, no. 9, pp. 747–756, 1996. View at Scopus
  16. S. P. Han, Y. H. Tang, and R. Smith, “Functional diversity of the hnRNPs: past, present and perspectives,” Biochemical Journal, vol. 430, no. 3, pp. 379–392, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Dreyfuss, “Structure and function of nuclear and cytoplasmic ribonucleoprotein particles,” Annual Review of Cell Biology, vol. 2, pp. 459–498, 1986. View at Scopus
  18. G. Dreyfuss, V. N. Kim, and N. Kataoka, “Messenger-RNA-binding proteins and the messages they carry,” Nature Reviews Molecular Cell Biology, vol. 3, no. 3, pp. 195–205, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Glisovic, J. L. Bachorik, J. Yong, and G. Dreyfuss, “RNA-binding proteins and post-transcriptional gene regulation,” FEBS Letters, vol. 582, no. 14, pp. 1977–1986, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C. C. Query, R. C. Bentley, and J. D. Keene, “A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein,” Cell, vol. 57, no. 1, pp. 89–101, 1989. View at Scopus
  21. D. W. Hoffman, C. C. Query, B. L. Golden, S. W. White, and J. D. Keene, “RNA-binding domain of the A protein component of the U1 small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 6, pp. 2495–2499, 1991. View at Scopus
  22. G. Dreyfuss, M. S. Swanson, and S. Piñol-Roma, “Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation,” Trends in Biochemical Sciences, vol. 13, no. 3, pp. 86–91, 1988. View at Scopus
  23. K. Nagai, C. Oubridge, T. H. Jessen, J. Li, and P. R. Evans, “Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A,” Nature, vol. 348, no. 6301, pp. 515–520, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Birney, S. Kumar, and A. R. Krainer, “Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors,” Nucleic Acids Research, vol. 21, no. 25, pp. 5803–5816, 1993. View at Scopus
  25. C. Maris, C. Dominguez, and F. H.-T. Allain, “The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression,” FEBS Journal, vol. 272, no. 9, pp. 2118–2131, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. R. Conte, T. Grüne, J. Ghuman et al., “Structure of tandem RNA recognition motifs from polypyrimidine tract binding protein reveals novel features of the RRM fold,” EMBO Journal, vol. 19, no. 12, pp. 3132–3141, 2000. View at Scopus
  27. P. J. Simpson, T. P. Monie, A. Szendröi et al., “Structure and RNA interactions of the N-terminal RRM domains of PTB,” Structure, vol. 12, no. 9, pp. 1631–1643, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Siomi, M. J. Matunis, W. M. Michael, and G. Dreyfuss, “The pre-mRNA binding K protein contains a novel evolutionarily conserved motif,” Nucleic Acids Research, vol. 21, no. 5, pp. 1193–1198, 1993. View at Scopus
  29. R. Valverde, L. Edwards, and L. Regan, “Structure and function of KH domains,” FEBS Journal, vol. 275, no. 11, pp. 2712–2726, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. A. V. Makeyev and S. A. Liebhaber, “The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms,” RNA, vol. 8, no. 3, pp. 265–278, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Kiledjian and G. Dreyfuss, “Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box,” EMBO Journal, vol. 11, no. 7, pp. 2655–2664, 1992. View at Scopus
  32. K. S. Godin and G. Varani, “How arginine-rich domains coordinate mRNA maturation events,” RNA Biology, vol. 4, no. 2, pp. 69–75, 2007. View at Scopus
  33. P. Rajyaguru and R. Parker, “RGG motif proteins: modulators of mRNA functional states,” Cell Cycle, vol. 11, pp. 2594–2599, 2012.
  34. R. Kanhoush, B. Beenders, C. Perrin, J. Moreau, M. Bellini, and M. Penrad-Mobayed, “Novel domains in the hnRNP G/RBMX protein with distinct roles in RNA binding and targeting nascent transcripts,” Nucleus, vol. 1, no. 1, pp. 109–122, 2010. View at Scopus
  35. G. Biamonti and S. Riva, “New insights into the auxiliary domains of eukaryotic RNA binding proteins,” FEBS Letters, vol. 340, no. 1-2, pp. 1–8, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. C. G. Burd, M. S. Swanson, M. Gorlach, and G. Dreyfuss, “Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: a diversity of RNA binding proteins is generated by small peptide inserts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 24, pp. 9788–9792, 1989. View at Publisher · View at Google Scholar · View at Scopus
  37. M. T. Vassileva and M. J. Matunis, “SUMO modification of heterogeneous nuclear ribonucleoproteins,” Molecular and Cellular Biology, vol. 24, no. 9, pp. 3623–3632, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. Q. Liu and G. Dreyfuss, “In vivo and in vitro arginine methylation of RNA-binding proteins,” Molecular and Cellular Biology, vol. 15, no. 5, pp. 2800–2808, 1995. View at Scopus
  39. E. Blackwell and S. Ceman, “Arginine methylation of RNA-binding proteins regulates cell function and differentiation,” Molecular Reproduction and Development, vol. 79, no. 3, pp. 163–175, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. L. P. Ford, W. E. Wright, and J. W. Shay, “A model for heterogeneous nuclear ribonucleoproteins in telomere and telomerase regulation,” Oncogene, vol. 21, no. 4, pp. 580–583, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. M. C. Mahajan, G. J. Narlikar, G. Boyapaty, R. E. Kingston, and S. M. Weissman, “Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at the β-globin locus control region,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 42, pp. 15012–15017, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. K.-H. Shin, M. K. Kang, and N.-H. Park, “Heterogeneous nuclear ribonucleoprotein G, nitric oxide, and oral carcinogenesis,” Nitric Oxide, vol. 19, no. 2, pp. 125–132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. He and R. Smith, “Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B,” Cellular and Molecular Life Sciences, vol. 66, no. 7, pp. 1239–1256, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Chen, M. Hewison, and J. S. Adams, “Functional characterization of heterogeneous nuclear ribonuclear protein C1/C2 in vitamin D resistance: a novel response element-binding protein,” Journal of Biological Chemistry, vol. 281, no. 51, pp. 39114–39120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. H. S. Choi, C. K. Hwang, K. Y. Song, P.-Y. Law, L.-N. Wei, and H. H. Loh, “Poly(C)-binding proteins as transcriptional regulators of gene expression,” Biochemical and Biophysical Research Communications, vol. 380, no. 3, pp. 431–436, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Martinez-Contreras, P. Cloutier, L. Shkreta, J.-F. Fisette, T. Revil, and B. Chabot, “hnRNP proteins and splicing control,” Advances in Experimental Medicine and Biology, vol. 623, pp. 123–147, 2007. View at Scopus
  47. O. P. Singh, “Functional diversity of hnRNP proteins,” Indian Journal of Biochemistry and Biophysics, vol. 38, no. 3, pp. 129–134, 2001. View at Scopus
  48. A. M. Krecic and M. S. Swanson, “hnRNP complexes: composition, structure, and function,” Current Opinion in Cell Biology, vol. 11, no. 3, pp. 363–371, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. B. Carpenter, C. MacKay, A. Alnabulsi et al., “The roles of heterogeneous nuclear ribonucleoproteins in tumour development and progression,” Biochimica et Biophysica Acta, vol. 1765, no. 2, pp. 85–100, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Kafasla, I. Mickleburgh, M. Llorian, et al., “Defining the roles and interactions of PTB,” Biochemical Society Transactions, vol. 40, pp. 815–820, 2012.
  51. M. Shibayama, S. Ohno, T. Osaka et al., “Polypyrimidine tract-binding protein is essential for early mouse development and embryonic stem cell proliferation,” FEBS Journal, vol. 276, no. 22, pp. 6658–6668, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Cornelis, Y. Bruynooghe, G. Denecker, S. Van Huffel, S. Tinton, and R. Beyaert, “Identification and characterization of a novel cell cycle-regulated internal ribosome entry site,” Molecular Cell, vol. 5, no. 4, pp. 597–605, 2000. View at Scopus
  53. C. Petretti, M. Savoian, E. Montembault, D. M. Glover, C. Prigent, and R. Giet, “The PITSLRE/CDK11p58 protein kinase promotes centrosome maturation and bipolar spindle formation,” EMBO Reports, vol. 7, no. 4, pp. 418–424, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Ohno, M. Shibayama, M. Sato, A. Tokunaga, and N. Yoshida, “Polypyrimidine tract-binding protein regulates the cell cycle through IRES-dependent translation of CDK11p58 in mouse embryonic stem cells,” Cell Cycle, vol. 10, no. 21, pp. 3706–3713, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. D. D. Licatalosi, M. Yano, J. J. Fak et al., “Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain,” Genes & Development, vol. 26, pp. 1626–1642, 2012.
  56. X. Song, C.-H. Zhu, C. Doan, and T. Xie, “Germline stem cells anchored by adherens junctions in the Drosophila ovary niches,” Science, vol. 296, no. 5574, pp. 1855–1857, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Ji and A. V. Tulin, “Poly(ADP-ribose) controls DE-cadherin-dependent stem cell maintenance and oocyte localization,” Nature Communications, vol. 3, article 760, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Assou, T. Le Carrour, S. Tondeur et al., “A meta-analysis of human embryonic stem cells transcriptome integrated into a web-based expression atlas,” Stem Cells, vol. 25, no. 4, pp. 961–973, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. D. Van Hoof, J. Muñoz, S. R. Braam et al., “Phosphorylation dynamics during early differentiation of human embryonic stem cells,” Cell Stem Cell, vol. 5, no. 2, pp. 214–226, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. H. S. Choi, W.-T. Kim, H. Kim et al., “Identification and characterization of adenovirus early region 1B-associated protein 5 as a surface marker on undifferentiated human embryonic stem cells,” Stem Cells and Development, vol. 20, no. 4, pp. 609–620, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. S. L. Lessnick and M. Ladanyi, “Molecular pathogenesis of Ewing sarcoma: new therapeutic and transcriptional targets,” Annual Review of Pathology, vol. 7, pp. 145–159, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Cho, H. Shen, H. Yu et al., “Ewing sarcoma gene Ews regulates hematopoietic stem cell senescence,” Blood, vol. 117, no. 4, pp. 1156–1166, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Kovar, G. Jug, D. N. T. Aryee et al., “Among genes involved in the RB dependent cell cycle regulatory cascade, the p16 tumor suppressor gene is frequently lost in the Ewing family of tumors,” Oncogene, vol. 15, no. 18, pp. 2225–2232, 1997. View at Scopus
  64. K. Sawicka, M. Bushell, K. A. Spriggs, and A. E. Willis, “Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein,” Biochemical Society Transactions, vol. 36, no. 4, pp. 641–647, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. H. S. Choi, H. M. Lee, Y. J. Jang, C. H. Kim, and C. J. Ryu, “Heterogeneous nuclear ribonucleoprotein A2/B1 regulates the selfrenewal and pluripotency of human embryonic stem cells via the control of the G1/S transition,” Stem Cells, 2013. View at Publisher · View at Google Scholar
  66. F. O. Fackelmayer and A. Richter, “Purification of two isoforms of hnRNP-U and characterization of their nucleic acid binding activity,” Biochemistry, vol. 33, no. 34, pp. 10416–10422, 1994. View at Scopus
  67. F. Göhring and F. O. Fackelmayer, “The scaffold/matrix attachment region binding protein hnRNP-U (SAF-A) is directly bound to chromosomal DNA in vivo: a chemical cross-linking study,” Biochemistry, vol. 36, no. 27, pp. 8276–8283, 1997. View at Publisher · View at Google Scholar · View at Scopus
  68. D. Vizlin-Hodzic, H. Johansson, J. Ryme, T. Simonsson, and S. Simonsson, “SAF-A has a role in transcriptional regulation of Oct4 in ES cells through promoter binding,” Cellular Reprogramming, vol. 13, no. 1, pp. 13–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. T. Ohno, M. Ouchida, L. Lee, Z. Gatalica, V. N. Rao, and E. S. P. Reddy, “The EWS gene, involved in Ewing family of tumors, malignant melanoma of soft parts and desmoplastic small round cell tumors, codes for an RNA binding protein with novel regulatory domains,” Oncogene, vol. 9, no. 10, pp. 3087–3097, 1994. View at Scopus
  70. Y. Iko, T. S. Kodama, N. Kasai et al., “Domain architectures and characterization of an RNA-binding protein, TLS,” Journal of Biological Chemistry, vol. 279, no. 43, pp. 44834–44840, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. T. H. Rabbitts, “Chromosomal translocations in human cancer,” Nature, vol. 372, no. 6502, pp. 143–149, 1994. View at Publisher · View at Google Scholar · View at Scopus
  72. W. A. May, S. L. Lessnick, B. S. Braun et al., “The Ewing's sarcoma EWS/FLI-1 fusion gene encodes a more potent transcriptional activator and is a more powerful transforming gene than FLI- 1,” Molecular and Cellular Biology, vol. 13, no. 12, pp. 7393–7398, 1993. View at Scopus
  73. D. D. K. Prasad, M. Ouchida, L. Lee, V. N. Rao, and E. S. P. Reddy, “TLS/FUS fusion domain of TLS/FUS-erg chimeric protein resulting from the t(16;21) chromosomal translocation in human myeloid leukemia functions as a transcriptional activation domain,” Oncogene, vol. 9, no. 12, pp. 3717–3729, 1994. View at Scopus
  74. K. A. W. Lee, “Molecular recognition by the EWS transcriptional activation domain,” Advances in Experimental Medicine and Biology, vol. 725, pp. 106–125, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. T. Sugawara, H. Oguro, M. Negishi et al., “FET family proto-oncogene Fus contributes to self-renewal of hematopoietic stem cells,” Experimental Hematology, vol. 38, no. 8, pp. 696–706, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. E. C. Torchia, S. Jaishankar, and S. J. Baker, “Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells,” Cancer Research, vol. 63, no. 13, pp. 3464–3468, 2003. View at Scopus
  77. S. Eliazer, J. Spencer, D. Ye, E. Olson, and R. L. Ilaria Jr., “Alteration of mesodermal cell differentiation by EWS/FLI-1, the oncogene implicated in Ewing's sarcoma,” Molecular and Cellular Biology, vol. 23, no. 2, pp. 482–492, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Riggi, L. Cironi, P. Provero et al., “Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells,” Cancer Research, vol. 65, no. 24, pp. 11459–11468, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. N. Riggi, M.-L. Suvà, D. Suvà et al., “EWS-FLI-1 expression triggers a ewing's sarcoma initiation program in primary human mesenchymal stem cells,” Cancer Research, vol. 68, no. 7, pp. 2176–2185, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. N. Riggi, M.-L. Suvà, C. De Vito et al., “EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells,” Genes & Development, vol. 24, no. 9, pp. 916–932, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. Q. Z. Xiao, G. Wang, Z. L. Luo, and Q. B. Xu, “The mechanism of stem cell differentiation into smooth muscle cells,” Thrombosis and Haemostasis, vol. 104, no. 3, pp. 440–448, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. L. Zhang, Y. J. Zhou, J. H. Zhu, and Q. B. Xu, “An updated view on stem cell differentiation into smooth muscle cells,” Vascular Pharmacology, vol. 56, pp. 280–287, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. Q. Xiao, L. Zeng, Z. Zhang, Y. Hu, and Q. Xu, “Stem cell-derived Sca-1+ progenitors differentiate into smooth muscle cells, which is mediated by collagen IV-integrin α1/β1/αv and PDGF receptor pathways,” American Journal of Physiology, vol. 292, no. 1, pp. C342–C352, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. Q. Xiao, Z. Luo, A. E. Pepe, A. Margariti, L. Zeng, and Q. Xu, “Embryonic stem cell differentiation into smooth muscle cells is mediated by Nox4-produced H2O2,” American Journal of Physiology, vol. 296, no. 4, pp. C711–C723, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Margariti, Q. Xiao, A. Zampetaki et al., “Splicing of HDAC7 modulates the SRF-myocardin complex during stem-cell differentiation towards smooth muscle cells,” Journal of Cell Science, vol. 122, no. 4, pp. 460–470, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. A. E. Pepe, Q. Xiao, A. Zampetaki et al., “Crucial role of Nrf3 in smooth muscle cell differentiation from stem cells,” Circulation Research, vol. 106, no. 5, pp. 870–879, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. L. Zhang, M. Jin, A. Margariti et al., “Sp1-dependent activation of HDAC7 is required for platelet-derived growth factor-BB-induced smooth muscle cell differentiation from stem cells,” Journal of Biological Chemistry, vol. 285, no. 49, pp. 38463–38472, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. Q. Xiao, A. E. Pepe, G. Wang et al., “Nrf3-Pla2g7 interaction plays an essential role in smooth muscle differentiation from stem cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 32, no. 3, pp. 730–744, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. X. Zheng, Y. Wu, L. Zhu et al., “Angiotensin II promotes of mouse embryonic stem cells to smooth muscle cells through PI3-kinase signaling pathway and NF-kappaB,” Differentiation, vol. 85, pp. 41–54, 2013.
  90. Y. Huang, L. Lin, X. Yu, et al., “Functional involvements of heterogeneous nuclear ribonucleoprotein A1 in smooth muscle differentiation from stem cells in vitro and in vivo,” Stem Cells, vol. 31, pp. 906–917, 2013.
  91. G. Wang, Q. Xiao, Z. Luo, S. Ye, and Q. Xu, “Functional impact of heterogeneous nuclear ribonucleoprotein A2/B1 in smooth muscle differentiation from stem cells and embryonic arteriogenesis,” Journal of Biological Chemistry, vol. 287, no. 4, pp. 2896–2906, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. Q. Z. Xiao, G. Wang, X. K. Yin et al., “Chromobox protein homolog 3 is essential for stem cell differentiation to smooth muscles in vitro and in embryonic arteriogenesis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 8, pp. 1842–1852, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Grüllich, R. M. Duvoisin, M. Wiedmann, and K. van Leyen, “Inhibition of 15-lipoxygenase leads to delayed organelle degradation in the reticulocyte,” FEBS Letters, vol. 489, no. 1, pp. 51–54, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. D. H. Ostareck, A. Ostareck-Lederer, M. Wilm, B. J. Thiele, M. Mann, and M. W. Hentze, “mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3' end,” Cell, vol. 89, no. 4, pp. 597–606, 1997. View at Scopus
  95. D. H. Ostareck, A. Ostareck-Lederer, I. N. Shatsky, and M. W. Hentze, “Lipoxygenase mRNA silencing in erythroid differentiation: the 3′UTR regulatory complex controls 60S ribosomal subunit joining,” Cell, vol. 104, no. 2, pp. 281–290, 2001. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Ostareck-Lederer, D. H. Ostareck, C. Cans et al., “c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs,” Molecular and Cellular Biology, vol. 22, no. 13, pp. 4535–4543, 2002. View at Publisher · View at Google Scholar · View at Scopus
  97. I. S. Naarmann, C. Harnisch, N. Flach et al., “mRNA silencing in human erythroid cell maturation: heterogeneous nuclear ribonucleoprotein K controls the expression of its regulator c-Src,” Journal of Biological Chemistry, vol. 283, no. 26, pp. 18461–18472, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. Y. Zermati, C. Garrido, S. Amsellem et al., “Caspase activation is required for terminal erythroid differentiation,” Journal of Experimental Medicine, vol. 193, no. 2, pp. 247–254, 2001. View at Publisher · View at Google Scholar · View at Scopus
  99. I. S. Naarmann-de Vries, H. Urlaub, D. H. Ostareck, and A. Ostareck-Lederer, “Caspase-3 cleaves hnRNP K in erythroid differentiation,” Cell Death and Disease, vol. 4, article e548, 2013.
  100. X. Wang, M. Kiledjian, I. M. Weiss, and S. A. Liebhaber, “Detection and characterization of a 3' untranslated region ribonucleoprotein complex associated with human α-globin mRNA stability,” Molecular and Cellular Biology, vol. 15, no. 3, pp. 1769–1777, 1995. View at Scopus
  101. A. N. Chkheidze, D. L. Lyakhov, A. V. Makeyev, J. Morales, J. Kong, and S. A. Liebhaber, “Assembly of the α-globin mRNA stability complex reflects binary interaction between the pyrimidine-rich 3' untranslated region determinant and poly(C) binding protein αCP,” Molecular and Cellular Biology, vol. 19, no. 7, pp. 4572–4581, 1999. View at Scopus
  102. X. Ji, J. Kong, R. P. Carstens, and S. A. Liebhaber, “The 3′ untranslated region complex involved in stabilization of human α-globin mRNA assembles in the nucleus and serves an independent role as a splice enhancer,” Molecular and Cellular Biology, vol. 27, no. 9, pp. 3290–3302, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. X. Ji, J. Kong, and S. A. Liebhaber, “An RNA-protein complex links enhanced nuclear 3′ processing with cytoplasmic mRNA stabilization,” EMBO Journal, vol. 30, no. 13, pp. 2622–2633, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. X. Ji, J. Wan, M. Vishnu, Y. Xing, and S. A. Liebhaber, “AlphaCP poly(C) binding proteins act as global regulators of alternative polyadenylation,” Molecular and Cellular Biology, vol. 33, pp. 2560–2573, 2013.
  105. M. Kiledjian, C. T. Demaria, G. Brewer, and K. Novick, “Identification of AUF1 (Heterogeneous nuclear ribonucleoprotein D) as a component of the α-globin mRNA stability complex,” Molecular and Cellular Biology, vol. 17, no. 10, p. 6202, 1997, Erratum in: Molecular and Cellular Biology vol. 17, no.8, pp. 4871–4874, 1997. View at Scopus
  106. J. Yu and J. E. Russell, “Structural and functional analysis of an mRNP complex that mediates the high stability of human β-globin mRNA,” Molecular and Cellular Biology, vol. 21, no. 17, pp. 5879–5888, 2001. View at Publisher · View at Google Scholar · View at Scopus
  107. K. S. Kabnick and D. E. Housman, “Determinants that contribute to cytoplasmic stability of human c-fos and β-globin mRNAs are located at several sites in each mRNA,” Molecular and Cellular Biology, vol. 8, no. 8, pp. 3244–3250, 1988. View at Scopus
  108. S. van Zalen, G. R. Jeschke, E. O. Hexner, and J. E. Russell, “AUF-1 and YB-1 are critical determinants of β-globin mRNA expression in erythroid cells,” Blood, vol. 119, no. 4, pp. 1045–1053, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. Z. Wang and M. Kiledjian, “The poly(A)-binding protein and an mRNA stability protein jointly regulate an endoribonuclease activity,” Molecular and Cellular Biology, vol. 20, no. 17, pp. 6334–6341, 2000. View at Publisher · View at Google Scholar · View at Scopus
  110. Z. Wang, N. Day, P. Trifillis, and M. Kiledjian, “An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro,” Molecular and Cellular Biology, vol. 19, no. 7, pp. 4552–4560, 1999. View at Scopus
  111. B. Calabretta and D. Perrotti, “The biology of CML blast crisis,” Blood, vol. 103, no. 11, pp. 4010–4022, 2004. View at Publisher · View at Google Scholar · View at Scopus
  112. A. Iervolino, G. Santilli, R. Trotta et al., “hnRNP A1 nucleocytoplasmic shuttling activity is required for normal myelopoiesis and BCR/ABL leukemogenesis,” Molecular and Cellular Biology, vol. 22, no. 7, pp. 2255–2266, 2002. View at Publisher · View at Google Scholar · View at Scopus
  113. D. Perrotti, S. Bonatti, R. Trotta et al., “TLS/FUS, a pro-oncogene involved in multiple chromosomal translocations, is a novel regulator of BCR/ABL-mediated leukemogenesis,” EMBO Journal, vol. 17, no. 15, pp. 4442–4455, 1998. View at Publisher · View at Google Scholar · View at Scopus
  114. D.-E. Zhang, P. Zhang, N.-D. Wang, C. J. Hetherington, G. J. Darlington, and D. G. Tenen, “Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein α-deficient mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 2, pp. 569–574, 1997. View at Publisher · View at Google Scholar · View at Scopus
  115. K. Keeshan, G. Santilli, F. Corradini, D. Perrotti, and B. Calabretta, “Transcription activation function of C/EBPα is required for induction of granulocytic differentiation,” Blood, vol. 102, no. 4, pp. 1267–1275, 2003. View at Publisher · View at Google Scholar · View at Scopus
  116. D. Perrotti, V. Cesi, R. Trotta et al., “BCR-ABL suppresses C/EBPα expression through inhibitory action of hnRNP E2,” Nature Genetics, vol. 30, no. 1, pp. 48–58, 2002. View at Publisher · View at Google Scholar · View at Scopus
  117. S. C. Ji, R. Santhanam, R. Trotta et al., “High levels of the BCR/ABL oncoprotein are required for the MAPK-hnRNP-E2-dependent suppression of C/EBPα-driven myeloid differentiation,” Blood, vol. 110, no. 3, pp. 994–1003, 2007. View at Publisher · View at Google Scholar · View at Scopus
  118. S. Gong, C. Zheng, M. L. Doughty et al., “A gene expression atlas of the central nervous system based on bacterial artificial chromosomes,” Nature, vol. 425, no. 6961, pp. 917–925, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. E. S. Lein, M. J. Hawrylycz, N. Ao et al., “Genome-wide atlas of gene expression in the adult mouse brain,” Nature, vol. 445, no. 7124, pp. 168–176, 2007. View at Publisher · View at Google Scholar · View at Scopus
  120. J. R. Sinnamon, C. B. Waddell, S. Nik, E. I. Chen, and K. Czaplinski, “Hnrpab regulates neural development and neuron cell survival after glutamate stimulation,” RNA, vol. 18, no. 4, pp. 704–719, 2012. View at Publisher · View at Google Scholar · View at Scopus