Heterogeneous nuclear ribonucleoprotein A1 in health and neurodegenerative disease: From structural insights to post-transcriptional regulatory roles

Molecular and Cellular Neuroscience

Volumn 56, Issue , 2013, Pages 436-446

  Bekenstein, Uriya ^a   Soreq, Hermona ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; DNA BINDING PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; MICRORNA; OLIGONUCLEOTIDE; PROTEIN VARIANT; RNA POLYMERASE II; SURVIVAL MOTOR NEURON PROTEIN 1; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ALU SEQUENCE; ALZHEIMER DISEASE; AMYLOID PLAQUE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; AUTOIMMUNITY; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; CONFORMATIONAL TRANSITION; CONSENSUS SEQUENCE; CRYSTAL STRUCTURE; DISEASE SEVERITY; DOWN REGULATION; ENHANCER REGION; ENTORHINAL CORTEX; EXON SKIPPING; EXTRACELLULAR SPACE; GENETIC CONSERVATION; HELA CELL; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; INTERACTIONS WITH RNA; MEMORY; MOLECULAR RECOGNITION; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE CELL CULTURE; NERVE DEGENERATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEIC ACID BASE SUBSTITUTION; OLIGODENDROGLIA; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA BINDING; RNA METABOLISM; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM; SPASTIC PARAPLEGIA; SPINAL CORD DISEASE; SPINAL MUSCULAR ATROPHY; SPLICEOSOME; STRUCTURE ACTIVITY RELATION; SUMOYLATION; TRANSCRIPTION REGULATION;

HUMAN T-LYMPHOTROPIC VIRUS 1; MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; MOLECULAR SEQUENCE DATA; NEURODEGENERATIVE DISEASES; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL;

EID: 84884819817     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.12.002     Document Type: Article

References (116)

1. Allemand E., Guil S., Myers M., Moscat J., Caceres J.F., Krainer A.R. Regulation of heterogeneous nuclear ribonucleoprotein A1 transport by phosphorylation in cells stressed by osmotic shock. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:3605-3610.
2. Ayala Y.M., Pantano S., D'Ambrogio A., Buratti E., Brindisi A., Marchetti C., Romano M., Baralle F.E. Human, Drosophila, and C. elegans TDP43: nucleic acid binding properties and splicing regulatory function. J. Mol. Biol. 2005, 348:575-588.
3. Barbash S., Soreq H. Threshold-independent meta-analysis of Alzheimer's disease transcriptomes shows progressive changes in hippocampal functions, epigenetics and microRNA regulation. Curr. Alzheimer Res. 2012, 9:425-435.
4. Bebee T.W., Dominguez C.E., Samadzadeh-Tarighat S., Akehurst K.L., Chandler D.S. Hypoxia is a modifier of SMN2 splicing and disease severity in a severe SMA mouse model. Hum. Mol. Genet. 2012, 21(19):4301-4313. (Oct 1) (Epub 2012 Jul 3). 10.1093/hmg/dds263.
5. 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.
6. Beyer A.L., Christensen M.E., Walker B.W., LeStourgeon W.M. Identification and characterization of the packaging proteins of core 40S hnRNP particles. Cell 1977, 11:127-138.
7. Biamonti G., Buvoli M., Bassi M.T., Morandi C., Cobianchi F., Riva S. Isolation of an active gene encoding human hnRNP protein A1. Evidence for alternative splicing. J. Mol. Biol. 1989, 207:491-503.
8. Blanchette M., Chabot B. Modulation of exon skipping by high-affinity hnRNP A1-binding sites and by intron elements that repress splice site utilization. EMBO J. 1999, 18:1939-1952.
9. Blencowe B.J. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 2000, 25:106-110.
10. Burd C.G., Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 1994, 265:615-621.
11. Caceres J.F., Krainer A.R. Functional analysis of pre-mRNA splicing factor SF2/ASF structural domains. EMBO J. 1993, 12:4715-4726.
12. Campillos M., Lamas J.R., Garcia M.A., Bullido M.J., Valdivieso F., Vazquez J. Specific interaction of heterogeneous nuclear ribonucleoprotein A1 with the -219T allelic form modulates APOE promoter activity. Nucleic Acids Res. 2003, 31:3063-3070.
13. Caputi M., Mayeda A., Krainer A.R., Zahler A.M. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 1999, 18:4060-4067.
14. Cartegni L., Krainer A.R. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 2002, 30:377-384.
15. Cartegni L., Maconi M., Morandi E., Cobianchi F., Riva S., Biamonti G. hnRNP A1 selectively interacts through its Gly-rich domain with different RNA-binding proteins. J. Mol. Biol. 1996, 259:337-348.
16. Cartegni L., Hastings M.L., Calarco J.A., de Stanchina E., Krainer A.R. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am. J. Hum. Genet. 2006, 78:63-77.
17. Casas-Finet J.R., Smith J.D., Kumar A., Kim J.G., Wilson S.H., Karpel R.L. Mammalian heterogeneous ribonucleoprotein A1 and its constituent domains. Nucleic acid interaction, structural stability and self-association. J. Mol. Biol. 1993, 229:873-889.
18. Chen M., Zhang J., Manley J.L. Turning on a fuel switch of cancer: hnRNP proteins regulate alternative splicing of pyruvate kinase mRNA. Cancer Res. 2010, 70:8977-8980.
19. Cobianchi F., Karpel R.L., Williams K.R., Notario V., Wilson S.H. Mammalian heterogeneous nuclear ribonucleoprotein complex protein A1. Large-scale overproduction in Escherichia coli and cooperative binding to single-stranded nucleic acids. J. Biol. Chem. 1988, 263:1063-1071.
20. Damgaard C.K., Tange T.O., Kjems J. hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure. RNA 2002, 8:1401-1415.
21. Ding J., Hayashi M.K., Zhang Y., Manche L., Krainer A.R., Xu R.M. Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA. Genes Dev. 1999, 13:1102-1115.
22. Donev R., Newall A., Thome J., Sheer D. A role for SC35 and hnRNPA1 in the determination of amyloid precursor protein isoforms. Mol. Psychiatry 2007, 12:681-690.
23. Dreyfuss G., Matunis M.J., Pinol-Roma S., Burd C.G. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 1993, 62:289-321.
24. Dutta R., Trapp B.D. Pathogenesis of axonal and neuronal damage in multiple sclerosis. Neurology 2007, 68:S22-S31. (discussion S43-54).
25. Eperon I.C., Makarova O.V., Mayeda A., Munroe S.H., Caceres J.F., Hayward D.G., Krainer A.R. Selection of alternative 5' splice sites: role of U1 snRNP and models for the antagonistic effects of SF2/ASF and hnRNP A1. Mol. Cell. Biol. 2000, 20:8303-8318.
26. Filipowicz W., Bhattacharyya S.N., Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet. 2008, 9:102-114.
27. Fisette J.F., Toutant J., Dugre-Brisson S., Desgroseillers L., Chabot B. hnRNP A1 and hnRNP H can collaborate to modulate 5' splice site selection. RNA 2010, 16:228-238.
28. Friedman Y., Naamati G., Linial M. MiRror: a combinatorial analysis web tool for ensembles of microRNAs and their targets. Bioinformatics 2010, 26:1920-1921.
29. Fujimoto T., Nakamura T., Nishiura Y., Ichinose K., Furuya T., Shirabe S., Eguchi K. Up-regulation of interleukin-12 receptor expression in peripheral blood mononuclear cells of patients with HTLV-I-associated myelopathy/tropical spastic paraparesis. J. Neurol. Sci. 2002, 196:21-26.
30. Fukuda H., Katahira M., Tsuchiya N., Enokizono Y., Sugimura T., Nagao M., Nakagama H. Unfolding of quadruplex structure in the G-rich strand of the minisatellite repeat by the binding protein UP1. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:12685-12690.
31. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
32. Gherzi R., Chen C.Y., Trabucchi M., Ramos A., Briata P. The role of KSRP in mRNA decay and microRNA precursor maturation. Wiley Interdiscip. Rev. RNA 2010, 1:230-239.
33. Gomez-Isla T., Price J.L., McKeel D.W., Morris J.C., Growdon J.H., Hyman B.T. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 1996, 16:4491-4500.
34. Gorlach M., Wittekind M., Beckman R.A., Mueller L., Dreyfuss G. Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J. 1992, 11:3289-3295.
35. Guil S., Caceres J.F. The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat. Struct. Mol. Biol. 2007, 14:591-596.
36. Guil S., Long J.C., Caceres J.F. hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Mol. Cell. Biol. 2006, 26:5744-5758.
37. Han S.P., Friend L.R., Carson J.H., Korza G., Barbarese E., Maggipinto M., Hatfield J.T., Rothnagel J.A., Smith R. Differential subcellular distributions and trafficking functions of hnRNP A2/B1 spliceoforms. Traffic 2010, 11:886-898.
38. Han S.P., Tang Y.H., Smith R. Functional diversity of the hnRNPs: past, present and perspectives. Biochem. J. 2010, 430:379-392.
39. Hanin G., Soreq H. Cholinesterase-targeting microRNAs identified in silico affect specific biological processes. Front. Mol. Neurosci. 2011, 4:28.
40. He Y., Smith R. Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B. Cell. Mol. Life Sci. 2009, 66:1239-1256.
41. Herrick G., Alberts B. Purification and physical characterization of nucleic acid helix-unwinding proteins from calf thymus. J. Biol. Chem. 1976, 251:2124-2132.
42. Hua Y., Vickers T.A., Okunola H.L., Bennett C.F., Krainer A.R. Antisense masking of an hnRNP A1/A2 intronic splicing silencer corrects SMN2 splicing in transgenic mice. Am. J. Hum. Genet. 2008, 82:834-848.
43. Idriss H., Kumar A., Casas-Finet J.R., Guo H., Damuni Z., Wilson S.H. Regulation of in vitro nucleic acid strand annealing activity of heterogeneous nuclear ribonucleoprotein protein A1 by reversible phosphorylation. Biochemistry 1994, 33:11382-11390.
44. Inoue A., Arao Y., Omori A., Ichinose S., Nishio K., Yamamoto N., Kinoshita Y., Mita S. Identification of S1 proteins B2, C1 and D1 as AUF1 isoforms and their major role as heterogeneous nuclear ribonucleoprotein proteins. Biochem. J. 2003, 372:775-785.
45. Izaurralde E., Jarmolowski A., Beisel C., Mattaj I.W., Dreyfuss G., Fischer U. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 1997, 137:27-35.
46. Kan Z.Y., Lin Y., Wang F., Zhuang X.Y., Zhao Y., Pang D.W., Hao Y.H., Tan Z. G-quadruplex formation in human telomeric (TTAGGG)4 sequence with complementary strand in close vicinity under molecularly crowded condition. Nucleic Acids Res. 2007, 35:3646-3653.
47. Kashima T., Manley J.L. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 2003, 34:460-463.
48. Kashima T., Rao N., David C.J., Manley J.L. hnRNP A1 functions with specificity in repression of SMN2 exon 7 splicing. Hum. Mol. Genet. 2007, 16:3149-3159.
49. Kiledjian M., Dreyfuss G. Primary structure and binding-activity of the Hnrnp U-protein - binding Rna through Rgg box. EMBO J. 1992, 11:2655-2664.
50. Kim V.N. MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 2005, 6:376-385.
51. Kumar A., Wilson S.H. Studies of the strand-annealing activity of mammalian hnRNP complex protein A1. Biochemistry 1990, 29:10717-10722.
52. Kumar A., Williams K.R., Szer W. Purification and domain structure of core hnRNP proteins A1 and A2 and their relationship to single-stranded DNA-binding proteins. J. Biol. Chem. 1986, 261:11266-11273.
53. Lau J.S., Baumeister P., Kim E., Roy B., Hsieh T.Y., Lai M., Lee A.S. Heterogeneous nuclear ribonucleoproteins as regulators of gene expression through interactions with the human thymidine kinase promoter. J. Cell. Biochem. 2000, 79:395-406.
54. Lee S.M., Dunnavant F.D., Jang H., Zunt J., Levin M.C. Autoantibodies that recognize functional domains of hnRNPA1 implicate molecular mimicry in the pathogenesis of neurological disease. Neurosci. Lett. 2006, 401:188-193.
55. Lee S., Xu L., Shin Y., Gardner L., Hartzes A., Dohan F.C., Raine C., Homayouni R., Levin M.C. A potential link between autoimmunity and neurodegeneration in immune-mediated neurological disease. J. Neuroimmunol. 2011, 235:56-69.
56. Lemmens R., Moore M.J., Al-Chalabi A., Brown R.H., Robberecht W. RNA metabolism and the pathogenesis of motor neuron diseases. Trends Neurosci. 2010, 33:249-258.
57. Leser G.P., Martin T.E. Changes in heterogeneous nuclear RNP core polypeptide complements during the cell cycle. J. Cell Biol. 1987, 105:2083-2094.
58. Levin M.C., Lee S.M., Kalume F., Morcos Y., Dohan F.C., Hasty K.A., Callaway J.C., Zunt J., Desiderio D.M., Stuart J.M. Autoimmunity due to molecular mimicry as a cause of neurological disease. Nat. Med. 2002, 8:509-513.
59. Levy C., Khaled M., Iliopoulos D., Janas M.M., Schubert S., Pinner S., Chen P.H., Li S.Q., Fletcher A.L., Yokoyama S., Scott K.L., Garraway L.A., Song J.S., Granter S.R., Turley S.J., Fisher D.E., Novina C.D. Intronic miR-211 assumes the tumor suppressive function of its host gene in melanoma. Mol. Cell 2010, 40:841-849.
60. Li H.P., Zhang X., Duncan R., Comai L., Lai M.M. Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription-regulatory region of mouse hepatitis virus RNA. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:9544-9549.
61. Li T., Evdokimov E., Shen R.F., Chao C.C., Tekle E., Wang T., Stadtman E.R., Yang D.C., Chock P.B. Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: a proteomic analysis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8551-8556.
62. Lorson C.L., Rindt H., Shababi M. Spinal muscular atrophy: mechanisms and therapeutic strategies. Hum. Mol. Genet. 2010, 19:R111-R118.
63. Lothstein L., Arenstorf H.P., Chung S.Y., Walker B.W., Wooley J.C., LeStourgeon W.M. General organization of protein in HeLa 40S nuclear ribonucleoprotein particles. J. Cell Biol. 1985, 100:1570-1581.
64. Ma A.S., Moran-Jones K., Shan J., Munro T.P., Snee M.J., Hoek K.S., Smith R. Heterogeneous nuclear ribonucleoprotein A3, a novel RNA trafficking response element-binding protein. J. Biol. Chem. 2002, 277:18010-18020.
65. Marchand V., Mereau A., Jacquenet S., Thomas D., Mougin A., Gattoni R., Stevenin J., Branlant C. A Janus splicing regulatory element modulates HIV-1 tat and rev mRNA production by coordination of hnRNP A1 cooperative binding. J. Mol. Biol. 2002, 323:629-652.
66. Mayeda A., Munroe S.H., Caceres J.F., Krainer A.R. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 1994, 13:5483-5495.
67. Mayeda A., Munroe S.H., Xu R.M., Krainer A.R. Distinct functions of the closely related tandem RNA-recognition motifs of hnRNP A1. RNA 1998, 4:1111-1123.
68. Mears W.E., Rice S.A. The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J. Virol. 1996, 70:7445-7453.
69. Merrill B.M., Stone K.L., Cobianchi F., Wilson S.H., Williams K.R. Phenylalanines that are conserved among several RNA-binding proteins form part of a nucleic acid-binding pocket in the A1 heterogeneous nuclear ribonucleoprotein. J. Biol. Chem. 1988, 263:3307-3313.
70. Michael W.M., Choi M., Dreyfuss G. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell 1995, 83:415-422.
71. Michlewski G., Caceres J.F. Antagonistic role of hnRNP A1 and KSRP in the regulation of Let-7a biogenesis. Nat. Struct. Mol. Biol. 2010, 17:1011-1018.
72. Municio M.M., Lozano J., Sanchez P., Moscat J., Diaz-Meco M.T. Identification of heterogeneous ribonucleoprotein A1 as a novel substrate for protein kinase C zeta. J. Biol. Chem. 1995, 270:15884-15891.
73. Myer V.E., Steitz J.A. Isolation and characterization of a novel, low abundance hnRNP protein: A0. RNA 1995, 1:171-182.
74. Myers J.C., Shamoo Y. Human UP1 as a model for understanding purine recognition in the family of proteins containing the RNA recognition motif (RRM). J. Mol. Biol. 2004, 342:743-756.
75. Nadler S.G., Merrill B.M., Roberts W.J., Keating K.M., Lisbin M.J., Barnett S.F., Wilson S.H., Williams K.R. Interactions of the A1 heterogeneous nuclear ribonucleoprotein and its proteolytic derivative, UP1, with RNA and DNA: evidence for multiple RNA binding domains and salt-dependent binding mode transitions. Biochemistry 1991, 30:2968-2976.
76. Nakielny S., Dreyfuss G. The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals. J. Cell Biol. 1996, 134:1365-1373.
77. Nasim F.U., Hutchison S., Cordeau M., Chabot B. High-affinity hnRNP A1 binding sites and duplex-forming inverted repeats have similar effects on 5' splice site selection in support of a common looping out and repression mechanism. RNA 2002, 8:1078-1089.
78. Niwa R., Zhou F., Li C., Slack F.J. The expression of the Alzheimer's amyloid precursor protein-like gene is regulated by developmental timing microRNAs and their targets in Caenorhabditis elegans. Dev. Biol. 2008, 315:418-425.
79. Noble M. The possible role of myelin destruction as a precipitating event in Alzheimer's disease. Neurobiol. Aging 2004, 25:25-31.
80. Okunola H.L., Krainer A.R. Cooperative-binding and splicing-repressive properties of hnRNP A1. Mol. Cell. Biol. 2009, 29:5620-5631.
81. Pandolfo M., Valentini O., Biamonti G., Morandi C., Riva S. Single stranded DNA binding proteins derive from hnRNP proteins by proteolysis in mammalian cells. Nucleic Acids Res. 1985, 13:6577-6590.
82. Papagiannakopoulos T., Shapiro A., Kosik K.S. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 2008, 68:8164-8172.
83. Paramasivam M., Membrino A., Cogoi S., Fukuda H., Nakagama H., Xodo L.E. Protein hnRNP A1 and its derivative Up1 unfold quadruplex DNA in the human KRAS promoter: implications for transcription. Nucleic Acids Res. 2009, 37:2841-2853.
84. Patry C., Bouchard L., Labrecque P., Gendron D., Lemieux B., Toutant J., Lapointe E., Wellinger R., Chabot B. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res. 2003, 63:7679-7688.
85. Pesiridis G.S., Lee V.M., Trojanowski J.Q. Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis. Hum. Mol. Genet. 2009, 18:R156-R162.
86. Pinol-Roma S., Dreyfuss G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 1992, 355:730-732.
87. Pokrishevsky E., Grad L.I., Yousefi M., Wang J., Mackenzie I.R., Cashman N.R. Aberrant localization of FUS and TDP43 is associated with misfolding of SOD1 in amyotrophic lateral sclerosis. PLoS One 2012, 7:e35050.
88. Pontius B.W., Berg P. Rapid assembly and disassembly of complementary DNA strands through an equilibrium intermediate state mediated by A1 hnRNP protein. J. Biol. Chem. 1992, 267:13815-13818.
89. Rajpurohit R., Paik W.K., Kim S. Effect of enzymic methylation of heterogeneous ribonucleoprotein particle A1 on its nucleic-acid binding and controlled proteolysis. Biochem. J. 1994, 304(Pt 3):903-909.
90. Rebane A., Aab A., Steitz J.A. Transportins 1 and 2 are redundant nuclear import factors for hnRNP A1 and HuR. RNA 2004, 10:590-599.
91. Reed R., Hurt E. A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 2002, 108:523-531.
92. Riva S., Morandi C., Tsoulfas P., Pandolfo M., Biamonti G., Merrill B., Williams K.R., Multhaup G., Beyreuther K., Werr H., et al. Mammalian single-stranded DNA binding protein UP I is derived from the hnRNP core protein A1. EMBO J. 1986, 5:2267-2273.
93. Samarina O.P., Lukanidin E.M., Molnar J., Georgiev G.P. Structural organization of nuclear complexes containing DNA-like RNA. J. Mol. Biol. 1968, 33:251-263.
94. Serrano-Pozo A., Frosch M.P., Masliah E., Hyman B.T. Neuropathological alterations in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2011, 1:a006189.
95. Shaked I., Meerson A., Wolf Y., Avni R., Greenberg D., Gilboa-Geffen A., Soreq H. MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity 2009, 31:965-973.
96. Shamoo Y., Krueger U., Rice L.M., Williams K.R., Steitz T.A. Crystal structure of the two RNA binding domains of human hnRNP A1 at 1.75A resolution. Nat. Struct. Biol. 1997, 4:215-222.
97. Shen E.C., Henry M.F., Weiss V.H., Valentini S.R., Silver P.A., Lee M.S. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 1998, 12:679-691.
98. Singh A.K., Lakhotia S.C. The hnRNP A1 homolog Hrp36 is essential for normal development, female fecundity, omega speckle formation and stress tolerance in Drosophila melanogaster. J. Biosci. 2012, 37:659-678.
99. Siomi H., Dreyfuss G. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 1995, 129:551-560.
100. Sueoka E., Yukitake M., Iwanaga K., Sueoka N., Aihara T., Kuroda Y. Autoantibodies against heterogeneous nuclear ribonucleoprotein B1 in CSF of MS patients. Ann. Neurol. 2004, 56:778-786.
101. Sun H., Chasin L.A. Multiple splicing defects in an intronic false exon. Mol. Cell. Biol. 2000, 20:6414-6425.
102. Sun Q., Mayeda A., Hampson R.K., Krainer A.R., Rottman F.M. General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev. 1993, 7:2598-2608.
103. Tange T.O., Damgaard C.K., Guth S., Valcarcel J., Kjems J. The hnRNP A1 protein regulates HIV-1 tat splicing via a novel intron silencer element. EMBO J. 2001, 20:5748-5758.
104. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 1991, 30:572-580.
105. Trabucchi M., Briata P., Garcia-Mayoral M., Haase A.D., Filipowicz W., Ramos A., Gherzi R., Rosenfeld M.G. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009, 459:1010-1014.
106. Valentini O., Biamonti G., Pandolfo M., Morandi C., Riva S. Mammalian single-stranded DNA binding proteins and heterogeneous nuclear RNA proteins have common antigenic determinants. Nucleic Acids Res. 1985, 13:337-346.
107. Valentini S.R., Weiss V.H., Silver P.A. Arginine methylation and binding of Hrp1p to the efficiency element for mRNA 3'-end formation. RNA 1999, 5:272-280.
108. van der Houven van Oordt W., Diaz-Meco M.T., Lozano J., Krainer A.R., Moscat J., Caceres J.F. The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J. Cell Biol. 2000, 149:307-316.
109. Villa C., Fenoglio C., De Riz M., Clerici F., Marcone A., Benussi L., Ghidoni R., Gallone S., Cortini F., Serpente M., Cantoni C., Fumagalli G., Martinelli Boneschi F., Cappa S., Binetti G., Franceschi M., Rainero I., Giordana M.T., Mariani C., Bresolin N., Scarpini E., Galimberti D. Role of hnRNP-A1 and miR-590-3p in neuronal death: genetics and expression analysis in patients with Alzheimer disease and frontotemporal lobar degeneration. Rejuvenation Res. 2011, 14:275-281.
110. Vitali J., Ding J., Jiang J., Zhang Y., Krainer A.R., Xu R.M. Correlated alternative side chain conformations in the RNA-recognition motif of heterogeneous nuclear ribonucleoprotein A1. Nucleic Acids Res. 2002, 30:1531-1538.
111. Wahl M.C., Will C.L., Luhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009, 136:701-718.
112. Walker B.W., Lothstein L., Baker C.L., LeStourgeon W.M. The release of 40S hnRNP particles by brief digestion of HeLa nuclei with micrococcal nuclease. Nucleic Acids Res. 1980, 8:3639-3657.
113. Wegorzewska I., Bell S., Cairns N.J., Miller T.M., Baloh R.H. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18809-18814.
114. Weighardt F., Biamonti G., Riva S. The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism. Bioessays 1996, 18:747-756.
115. Zhu J., Mayeda A., Krainer A.R. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 2001, 8:1351-1361.
116. Zhu D., Xu G., Ghandhi S., Hubbard K. Modulation of the expression of p16INK4a and p14ARF by hnRNP A1 and A2 RNA binding proteins: implications for cellular senescence. J. Cell. Physiol. 2002, 193:19-25.