Post-transcriptional regulation by poly(ADP-ribosyl)ation of the RNA-binding proteins

International Journal of Molecular Sciences

Volumn 14, Issue 8, 2013, Pages 16168-16183

  Ji, Yingbiao ^a   Tulin, Alexei V ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

Parg; Parp; Poly(ADP ribose); RNA metabolism; RNA binding protein

Indexed keywords

ARGONAUTE PROTEIN; GLYCOSIDASE; GLYCOSIDASE INHIBITOR; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; POLY(ADP RIBOSE) POLYMERASE 1 INHIBITOR; POLY(ADP RIBOSE)GLYCOHYDROLASE; POLY(ADP RIBOSE)GLYCOHYDROLASE INHIBITOR; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ALTERNATIVE RNA SPLICING; ARTICLE; CANCER CHEMOTHERAPY; CELL DIFFERENTIATION; CELL FUNCTION; CELLULAR STRESS RESPONSE; COILED BODY; CYTOPLASM; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DNA DAMAGE; DRUG MECHANISM; GENE SILENCING; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; OVARY CANCER; POLYADENYLATION; PROSTATE CANCER; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN SYNTHESIS INHIBITION; RETINA DEVELOPMENT; RNA PROCESSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

DNA REPAIR; GENE EXPRESSION REGULATION; GLYCOSIDE HYDROLASES; HUMANS; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84881219867     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140816168     Document Type: Article

References (95)

1. Houseley, J.; Tollervey, D. The many pathways of RNA degradation. Cell 2009, 136, 763-776.
2. Keene, J.D. RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8, 533-543.
3. Licatalosi, D.D.; Darnell, R.B. RNA processing and its regulation: Global insights into biological networks. Nat. Rev. Genet. 2010, 11, 75-87.
4. Änkö, M.-L.; Neugebauer, K.M. RNA-protein interactions in vivo: Global gets specific. Trends Biochem. Sci. 2012, 37, 255-262.
5. Lukong, K.E.; Chang, K.W.; Khandjian, E.W.; Richard, S. RNA-binding proteins in human genetic disease. Trends Genet. 2008, 24, 416-425.
6. Matter, N.; Herrlich, P.; Konig, H. Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 2002, 420, 691-695.
7. Satoh, R.; Morita, T.; Takada, H.; Kita, A.; Ishiwata, S.; Doi, A.; Hagihara, K.; Taga, A.; Matsumura, Y.; Tohda, H.; et al. Role of the RNA-binding protein Nrd1 and Pmk1 Mitogen-activated protein kinase in the regulation of myosin mrna stability in fission yeast. Mol. Biol. Cell 2009, 20, 2473-2485.
8. Nir, R.; Grossman, R.; Paroush, Z.; Volk, T. Phosphorylation of the Drosophila melanogaster RNA-Binding Protein HOW by MAPK/ERK Enhances Its Dimerization and Activity. PLoS Genet. 2012, 8, e1002632.
9. Parrott, A.M.; Walsh, M.R.; Reichman, T.W.; Mathews, M.B. RNA binding and phosphorylation determine the intracellular distribution of nuclear factors 90 and 110. J. Mol. Biol. 2005, 348, 281-293.
10. Dammer, E.B.; Fallini, C.; Gozal, Y.M.; Duong, D.M.; Rossoll, W.; Xu, P.; Lah, J.J.; Levey, A.I.; Peng, J.; Bassell, G.J.; et al. Coaggregation of RNA-Binding proteins in a model of TDP-43 proteinopathy with selective RGG motif methylation and a role for RRM1 ubiquitination. PLoS One 2012, 7, e38658.
11. Bhandari, D.; Guha, K.; Bhaduri, N.; Saha, P. Ubiquitination of mRNA cycling sequence binding protein from Leishmania donovani (LdCSBP) modulates the RNA endonuclease activity of its Smr domain. FEBS Lett. 2011, 585, 809-813.
12. Ji, Y.; Tulin, A.V. The roles of PARP1 in gene control and cell differentiation. Curr. Opin. Genet. Dev. 2010, 20, 512-518.
13. Luo, X.; Kraus, W.L. On PAR with PARP: Cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev. 2012, 26, 417-432.
14. D'Amours, D.; Desnoyers, S.; D'Silva, I.; Poirier, G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342, 249-268.
15. Krietsch, J.; Rouleau, M.; Pic, E.; Ethier, C.; Dawson, T.M.; Dawson, V.L.; Masson, J.Y.; Poirier, G.G.; Gagné, J.P. Reprogramming cellular events by poly (ADP-ribose)-binding proteins. Mol. Asp. Med. 2012, in press.
16. Hanai, S.; Kanai, M.; Ohashi, S.; Okamoto, K.; Yamada, M.; Takahashi, H.; Miwa, M. Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2004, 101, 82-86.
17. Koh, D.W.; Lawler, A.M.; Poitras, M.F.; Sasaki, M.; Wattler, S.; Nehls, M.C.; Stöger, T.; Poirier, G.G.; Dawson, V.L.; Dawson, T.M. Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc. Natl. Acad. Sci. USA 2004, 101, 17699-17704.
18. Tulin, A.; Naumova, N.M.; Menon, A.K.; Spradling, A.C. Drosophila Poly(ADP-Ribose) Glycohydrolase mediates chromatin structure and SIR2-Dependent silencing. Genetics 2006, 172, 363-371.
19. Krishnakumar, R.; Kraus, W.L. The PARP side of the nucleus: Molecular actions, physiological outcomes, and clinical targets. Mol. Cell 2010, 39, 8-24.
20. Thomas, C.; Tulin, A.V. Poly-ADP-Ribose polymerase: Machinery for nuclear processes. Mol. Asp. Med. 2013, in press.
21. Chaudhury, A.; Chander, P.; Howe, P.H. Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles. RNA 2010, 16, 1449-1462.
22. Kostka, G.N.; Schweiger, A. ADP-ribosylation of proteins associated with heterogeneous nuclear RNA in rat liver nuclei. Biochim. Biophys. Acta (BBA) 1982, 696, 139-144.
23. Prasad, S.; Walent, J.; Dritschilo, A. ADP-Ribosylation of heterogeneous ribonucleoproteins in HeLa cells. Biochem. Biophys. Res. Commun. 1994, 204, 772-779.
24. Gagné, J.P.; Hunter, J.M.; Labrecque, B.; Chabot, B.; Poirier, G.G. A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)binding proteins. Biochem. J. 2003, 371, 331-340.
25. Gagné, J.P.; Pic, E.; Isabelle, M.; Krietsch, J.; Ethier, C.; Paquet, E.; Kelly, I.; Boutin, M.; Moon, K.M.; Foster, L.J.; et al. Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res. 2012, 40, 7788-7805.
26. Isabelle, M.; Moreel, X.; Gagné, J.P.; Rouleau, M.; Ethier, C.; Gagné, P.; Hendzel, M.J.; Poirier, G.G. Investigation of PARP-1, PARP-2, and PARG interactomes by affinity-purification mass spectrometry. Proteome Sci. 2010, 8, 22.
27. Jiang, H.; Kim, J.H.; Frizzell, K.M.; Kraus, W.L.; Lin, H. Clickable NAD analogues for labeling substrate proteins of Poly(ADP-ribose) polymerases. J. Am. Chem. Soc. 2010, 132, 9363-9372.
28. Chiou, S.H.; Jiang, B.H.; Yu, Y.L.; Chou, S.J.; Tsai, P.H.; Chang, W.C.; Chen, L.K.; Chen, L.H.; Chien, Y.; Chiou, G.Y. Poly(ADP-ribose) polymerase 1 regulates nuclear reprogramming and promotes iPSC generation without c-Myc. J. Exper. Med. 2013, 210, 85-98.
29. Isabelle, M.; Gagné, J.P.; Gallouzi, I.E.; Poirier, G.G. Quantitative proteomics and dynamic imaging reveal that G3BP-mediated stress granule assembly is poly(ADP-ribose)-dependent following exposure to MNNG-induced DNA alkylation. J. Cell Sci. 2012, 125, 4555-4566.
30. Pinnola, A.; Naumova, N.; Shah, M.; Tulin, A.V. Nucleosomal core histones mediate dynamic regulation of Poly(ADP-ribose) polymerase 1 protein binding to chromatin and induction of its enzymatic activity. J. Biol. Chem. 2007, 282, 32511-32519.
31. Ji, Y.; Tulin, A.V. Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucl. Acids Res. 2009, 37, 3501-3513.
32. Pleschke, J.M.; Kleczkowska, H.E.; Strohm, M.; Althaus, F.R. Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem. 2000, 275, 40974-40980.
33. Ji, Y.; Tulin, A.V. Poly(ADP-ribose) controls DE-cadherin-dependent stem cell maintenance and oocyte localization. Nat. Commun. 2012, 3, 760.
34. Ji, Y. Noncovalent pADPr Interaction with Proteins and Competition with RNA for Binding to Proteins, in Poly(ADP-ribose) Polymerase; Tulin, A.V., Ed.; Humana Press: Clifton, NJ, USA, 2011; pp. 83-91.
35. Huelga, S.C.; Vu, A.Q.; Arnold, J.D.; Liang, T.Y.; Liu, P.P.; Yan, B.Y.; Donohue, J.P.; Shiue, L.; Hoon, S.; Brenner, S.; et al. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep. 2012, 1, 167-178.
36. Tulin, A.; Spradling, A.C. Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 2003, 299, 560-562.
37. Malanga, M.; Czubaty, A.; Girstun, A.; Staron, K.; Althaus, F.R. Poly(ADP-ribose) binds to the splicing factor ASF/SF2 and regulates its phosphorylation by DNA topoisomerase I. J. Biol. Chem. 2008, 283, 19991-19998.
38. Gagné, J.P.; Isabelle, M.; Lo, K.S.; Bourassa, S.; Hendzel, M.J.; Dawson, V.L.; Dawson, T.M.; Poirier, G.G. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 2008, 36, 6959-6976.
39. Long, J.C.; Caceres, J.F. The SR protein family of splicing factors: Master regulators of gene expression. Biochem. J. 2009, 417, 15-27.
40. Stamm, S. Regulation of alternative splicing by reversible protein phosphorylation. J. Biol. Chem. 2008, 283, 1223-1227.
41. Richard, P.; Manley, J.L. Transcription termination by nuclear RNA polymerases. Genes Dev. 2009, 23, 1247-1269.
42. Shi, Y.; di Giammartino, D.C.; Taylor, D.; Sarkeshik, A.; Rice, W.J.; Yates, J.R., III; Frank, J.; Manley, J.L. Molecular architecture of the human Pre-mRNA 3' processing complex. Mol. Cell 2009, 33, 365-376.
43. Di Giammartino, D.C.; Shi, Y.; Manley, J.L. PARP1 represses PAP and inhibits polyadenylation during heat shock. Mol. Cell 2013, 49, 7-17.
44. Hutvagner, G.; Simard, M.J. Argonaute proteins: Key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 2008, 9, 22-32.
45. Leung, A.K.; Vyas, S.; Rood, J.E.; Bhutkar, A.; Sharp, P.A.; Chang, P. Poly(ADP-Ribose) regulates stress responses and MicroRNA activity in the cytoplasm. Mol. Cell 2011, 42, 489-499.
46. Bonnal, S.; Pileur, F.; Orsini, C.; Parker, F.; Pujol, F.; Prats, A.C.; Vagner, S. Heterogeneous nuclear ribonucleoprotein A1 is a novel internal ribosome entry site trans-acting factor that modulates alternative initiation of translation of the fibroblast growth factor 2 mRNA. J. Biol. Chem.2005, 280, 4144-4153.
47. Rodríguez, M.I.; González-Flores, A.; Dantzer, F.; Collard, J.; de Herreros, A.G.; Oliver, F.J. Poly(ADP-ribose)-dependent regulation of Snail1 protein stability. Oncogene 2011, 30, 4365-4372.
48. Gagné, J.P.; Bonicalzi, M.E.; Gagné, P.; Ouellet, M.E.; Hendzel, M.J.; Poirier, G.G. Poly(ADP-riboose) glycohydrolase is a component of the FMRP-associated messenger ribonucleoparticles. Biochem. J. 2005, 392, 499-509.
49. Boamah, E.K.; Kotova, E.; Garabedian, M.; Jarnik, M.; Tulin, A.V. Poly(ADP-Ribose) polymerase 1 (PARP-1) regulates ribosomal biogenesis in Drosophila nucleoli. PLoS Genet. 2012, 8, e1002442.
50. Tulin, A.; Stewart, D.; Spradling, A.C. The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev. 2002, 16, 2108-2119.
51. Boisvert, F.M.; van Koningsbruggen, S.; Navascués, J.; Lamond, A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8, 574-585.
52. Guetg, C.; Scheifele, F.; Rosenthal, F.; Hottiger, M.O.; Santoro, R. Inheritance of Silent rDNA chromatin is mediated by PARP1 via Noncoding RNA. Mol. Cell 2012, 45, 790-800.
53. Isabelle, M.; Gallouzi, I.E.; Poirier, G.G. PARP1 parylation promotes silent locus transmission in the nucleolus: The suspicion confirmed. Mol. Cell 2012, 45, 706-707.
54. Guerrero, P.A.; Maggert, K.A. The CCCTC-Binding Factor (CTCF) of Drosophila contributes to the regulation of the ribosomal DNA and nucleolar stability. PLoS One 2011, 6, e16401.
55. Tao, Z.; Gao, P.; Liu, H.W. Studies of the expression of human Poly(ADP-ribose) Polymerase-1 in Saccharomyces cerevisiae and identification of PARP-1 substrates by yeast proteome microarray screening. Biochemistry 2009, 48, 11745-11754.
56. Machyna, M.; Heyn, P.; Neugebauer, K.M. Cajal. bodies: Where form meets function. Wiley Interdisciplinary Rev. RNA 2013, 4, 17-34.
57. Kotova, E.; Jarnik, M.; Tulin, A.V. Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genet. 2009, 5, e1000387.
58. Cioce, M.; Cioce, M.; Boulon, S.; Matera, A.G.; Lamond, A.I. UV-induced fragmentation of Cajal bodies. J. Cell Biol. 2006, 175, 401-413.
59. Krietsch, J.; Caron, M.C.; Gagné, J.P.; Ethier, C.; Vignard, J.; Vincent, M.; Rouleau, M.; Hendzel, M.J.; Poirier, G.G.; Masson, J.Y. PARP activation regulates the RNA-binding protein NONO in the DNA damage response to DNA double-strand breaks. Nucleic Acids Res. 2012, 400, 10287-10301.
60. Adamson, B.; Smogorzewska, A.; Sigoillot, F.D.; King, R.W.; Elledge, S.J. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol. 2012, 14, 318-328.
61. Hong, Z.; Jiang, J.; Ma, J.; Dai, S.; Xu, T.; Li, H.; Yasui, A. The Role of hnRPUL1 Involved in DNA damage response is related to PARP1. PLoS One 2013, 8, e60208.
62. Prasanth, K.V.; Rajendra, T.K.; Lal, A.K.; Lakhotia, S.C. Omega speckles-A novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J. Cell Sci. 2000, 113, 3485-3497.
63. Jolly, C.; Lakhotia, S.C. Human sat III and Drosophila hsr transcripts: A common paradigm for regulation of nuclear RNA processing in stressed cells. Nucleic Acids Res. 2006, 34, 5508-5514.
64. Anderson, P.; Kedersha, N. RNA granules: Post-Transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 2009, 10, 430-436.
65. Buchan, J.R.; Parker, R. Eukaryotic stress granules: The ins and outs of translation. Mol. Cell 2009, 36, 932-941.
66. Gibson, B.A.; Kraus, W.L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol. 2012, 13, 411-424.
67. Ahel, D.; Horejsí, Z.; Wiechens, N.; Polo, S.E.; Garcia-Wilson, E.; Ahel, I.; Flynn, H.; Skehel, M.; West, S.C.; Jackson, S.P.; et al. Poly(ADP-ribose)-Dependent Regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 2009, 325, 1240-1243.
68. Lieber, M.R. The Mechanism of Double-Strand DNA break repair by the nonhomologous DNA End-Joining pathway. Ann. Rev. Biochem. 2010, 79, 181-211.
69. Shav-Tal, Y.; Zipori, D. PSF and p54nrb/NonO-Multi-functional nuclear proteins. FEBS Lett. 2002, 531, 109-114.
70. Song, X.; Zhu, C.H.; Doan, C.; Xie, T. Germline stem cells anchored by adherens junctions in the drosophila ovary niches. Science 2002, 296, 1855-1857.
71. Godt, D.; Tepass, U. Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 1998, 395, 387-391.
72. Lai, Y.S.; Chang, C.W.; Pawlik, K.M.; Zhou, D.; Renfrow, M.B.; Townes, T.M. SRY (sex determining region Y)-box2 (Sox2)/poly ADP-ribose polymerase 1 (Parp1) complexes regulate pluripotency. Proc. Natl. Acad. Sci. USA 2012, 109, 3772-3777.
73. Doege, C.A.; Inoue, K.; Yamashita, T.; Rhee, D.B.; Travis, S.; Fujita, R.; Guarnieri, P.; Bhagat, G.; Vanti, W.B.; Shih, A.; et al. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 2012, 488, 652-655.
74. Ji, Y.; Jarnik, M.; Tulin, A.V. Poly(ADP-ribose) glycohydrolase and poly(ADP-ribose)-interacting protein Hrp38 regulate pattern formation during Drosophila eye development. Gene 2013 526, 187-194.
75. Tepass, U.; Harris, K.P. Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol. 2007, 17, 26-35.
76. Martín-Oliva, D.; Ferrer-Martín, R.M.; Santos, A.M.; Carrasco, M.C.; Sierra, A.; Marín-Teva, J.L.; Calvente, R.; Navascués, J.; Cuadros, M.A. Simultaneous cell death and upregulation of Poly(ADP-Ribose) polymerase-1 expression in early postnatal mouse retina. Invest. Ophthalmol. Vis. Sci. 2011, 52, 7445-7454.
77. Paquet-Durand, F.O.; Silva, J.; Talukdar, T.; Johnson, L.E.; Azadi, S.; van Veen, T.; Ueffing, M.; Hauck, S.M.; Ekström, P.A. Excessive activation of poly (ADP-ribose) polymerase contributes to inherited photoreceptor degeneration in the retinal degeneration 1 mouse. J. Neurosci. 2007, 27, 10311-10319.
78. Rouleau, M.l.; Patel, A.; Hendzel, M.J.; Kaufmann, S.H.; Poirier, G.G. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer 2010, 10, 293-301.
79. Brenner, J.C.; Ateeq, B.; Li, Y.; Yocum, A.K.; Cao, Q.; Asangani, I.A.; Patel, S.; Wang, X.; Liang, H.; Yu, J.; et al. Mechanistic rationale for inhibition of Poly(ADP-Ribose) polymerase in ETS gene fusion-positive prostate cancer. Cancer Cell 2011, 19, 664-678.
80. Schiewer, M.J.; Goodwin, J.F.; Han, S.; Brenner, J.C.; Augello, M.A.; Dean, J.L.; Liu, F.; Planck, J.L.; Ravindranathan, P.; Chinnaiyan, A.M.; et al. Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov. 2012, 2, 1134-1149.
81. Tulin, A. Re-evaluating PARP1 inhibitor in cancer. Nat. Biotechnol. 2011, 29, 1078-1079.
82. Sofola, O.A.; Jin, P.; Qin, Y.; Duan, R.; Liu, H.; de Haro, M.; Nelson, D.L.; Botas, J. RNA-Binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a drosophila model of FXTAS. Neuron 2007, 55, 565-571.
83. Jin, P.; Duan, R.; Qurashi, A.; Qin, Y.; Tian, D.; Rosser, T.C.; Liu, H.; Feng, Y.; Warren, S.T. Pur [alpha] Binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a drosophila model of fragile X tremor/ataxia syndrome. Neuron 2007, 55, 556-564.
84. Sengupta, S.; Lakhotia, S.C. Altered expressions of the noncoding hsromega gene enhances poly-Q-induced neurotoxicity in Drosophila. RNA Biol. 2006, 3, e1-e8.
85. Mallik, M.; Lakhotia, S.C. Improved activities of CREB binding protein, heterogeneous nuclear ribonucleoproteins and proteasome following downregulation of noncoding hsrω transcripts help suppress Poly(Q) pathogenesis in fly models. Genetics 2010, 184, 927-945.
86. Berson, A.; Barbash, S.; Shaltiel, G.; Goll, Y.; Hanin, G.; Greenberg, D.S.; Ketzef, M.; Becker, A.J.; Friedman, A.; Soreq, H. Cholinergic-associated loss of hnRNP-A/B in Alzheimer's disease impairs cortical splicing and cognitive function in mice. EMBO Mol. Med. 2012, 4, 730-742.
87. Kim, H.J.; Kim, N.C.; Wang, Y.D.; Scarborough, E.A.; Moore, J.; Diaz, Z.; MacLea, K.S.; Freibaum, B.; Li, S.; Molliex, A.; et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 2013, 495, 467-473.
88. Bagni, C.; Tassone, F.; Neri, G.; Hagerman, R. Fragile X syndrome: Causes, diagnosis, mechanisms, and therapeutics. J. Clin. Invest. 2012, 122, 4314-4322.
89. Pino, I.; Pío, R.; Toledo, G.; Zabalegui, N.; Vicent, S.; Rey, N.; Lozano, M.D.; Torre, W.; García-Foncillas, J.; Montuenga, L.M. Altered patterns of expression of members of the heterogeneous nuclear ribonucleoprotein (hnRNP) family in lung cancer. Lung Cancer 2003, 41, 131-143.
90. Zhou, Z.J.; Dai, Z.; Zhou, S.L.; Fu, X.T.; Zhao, Y.M.; Shi, Y.H.; Zhou, J.; Fan, J. Overexpression of HnRNP A1 promotes tumor invasion through regulating CD44v6 and indicates poor prognosis for hepatocellular carcinoma. Int. J. Cancer 2013, 132, 1080-1089.
91. Ushigome, M.; Ubagai, T.; Fukuda, H.; Tsuchiya, N.; Sugimura, T.; Takatsuka, J.; Nakagama, H. Up-regulation of hnRNP A1 gene in sporadic human colorectal cancers. Int. J. Oncol. 2005, 26, 635-640.
92. He, Z.Y.; Wen, H.; Shi, C.B. Up-regulation of hnRNP A1, Ezrin, tubulin β-2C and Annexin A1 in sentinel lymph nodes of colorectal cancer. World J. Gastroenterol. 2010, 16, 4670-4676.
93. David, C.J.; Chen, M.; Assanah, M.; Canoll, P.; Manley, J.L. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2009, 463, 364-368.
94. Warburg, O. On the origin of cancer cells. Science 1956, 123, 309-314.
95. Luo, W.; Hu, H.; Chang, R.; Zhong, J.; Knabel, M.; O'Meally, R.; Cole, R.N.; Pandey, A.; Semenza, G.L. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 2011, 145, 732-744.