The RNA-binding protein HuD: A regulator of neuronal differentiation, maintenance and plasticity

BioEssays

Volumn 28, Issue 8, 2006, Pages 822-833

  Deschênes Furry, Julie ^a   Perrone Bizzozero, Nora ^b   Jasmin, Bernard J ^a,c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN HUD; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

CELL MATURATION; CELL PROLIFERATION; HUMAN; IN SITU HYBRIDIZATION; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM; NEUROBLAST; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW;

3' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MODELS, NEUROLOGICAL; MOLECULAR SEQUENCE DATA; NEURONAL PLASTICITY; NEURONS; RNA STABILITY;

EID: 33748949959     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20449     Document Type: Review

References (124)

1. Bashirullah A, Cooperstock RL, Lipshitz HD. 1998. RNA localization in development. Annu Rev Biochem 67:335-394.
2. King ML, Zhou Y, Bubunenko M. 1999. Polarizing genetic information in the egg: RNA localization in the frog oocyte. Bioessays 21:546-557.
3. Hollams EM, Giles KM, Thomson AM, Leedman PJ. 2002. MRNA stability and the control of gene expression: implications for human disease. Neurochem Res 27:957-980.
4. Naveh-Many T, Bell O, Silver J, Kilav R. 2002. Cis and trans acting factors in the regulation of parathyroid hormone (PTH) mRNA stability by calcium and phosphate. FEBS Lett 529:60-64.
5. Conne B, Stutz A, Vassalli JD. 2000. The 3′ untranslated region of messenger RNA: a molecular 'hotspot' for pathology? Nat Med 6:637-641.
6. Mendell JT, Dietz HC. 2001. When the message goes awry: disease-producing mutations that influence mRNA content and performance. Cell 107:411-414.
7. Misquitta CM, Iyer VR, Werstiuk ES, Grover AK. 2001. The role of 3′-untranslated region (3′-UTR) mediated mRNA stability in cardiovascular pathophysiology. Mol Cell Biochem 224:53-67.
8. Perrone-Bizzozero N, Bolognani F. 2002. Role of HuD and other RNA-binding proteins in neural development and plasticity. J Neurosci Res 68:121-126.
9. Gallo JM, Jin P, Thornton CA, Lin H, Robertson J, et al. 2005. The role of RNA and RNA processing in neurodegeneration. J Neurosci 25:10372-10375.
10. Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, et al. 2001. The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21:3888-3900.
11. Jensen KB, Dredge BK, Stefani G, Zhong R, Buckanovich RJ, et al. 2000. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25:359-371.
12. Okano H, Imai T, Okabe M. 2002. Musashi: a translational regulator of cell fate. J Cell Sci 115:1355-1359.
13. Roegiers F, Jan YN. 2000. Staufen: a common component of mRNA transport in oocytes and neurons? Trends Cell Biol 10:220-224.
14. Bassell GJ, Oleynikov Y, Singer RH. 1999. The travels of mRNAs through all cells large and small. FASEB J 13:447-454.
15. Rehbein M, Wege K, Buck F, Schweizer M, Richter D, et al. 2002. Molecular characterization of MARTA1, a protein interacting with the dendritic targeting element of MAP2 mRNAs. J Neurochem 82:1039-1046.
16. Gherzi R, Lee KY, Briata P, Wegmuller D, Moroni C, et al. 2004. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14:571-583.
17. Farina KL, Singer RH. 2002. The nuclear connection in RNA transport and localization. Trends Cell Biol 12:466-472.
18. Huang YS, Carson JH, Barbarese E, Richter JD. 2003. Facilitation of dendritic mRNA transport by CPEB. Genes Dev 17:638-653.
19. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, et al. 2001. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31:261-275.
20. Mendez R, Richter JD. 2001. Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2:521-529.
21. Ross AF, Oleynikov Y, Kislauskis EH, Taneja KL, Singer RH. 1997. Characterization of a beta-actin mRNA zipcode-binding protein. Mol Cell Biol 17:2158-2165.
22. Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM, et al. 2003. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 115:893-904.
23. Wu L, Wells D, Tay J, Mendis D, Abbott MA, et al. 1998. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21:1129-1139.
24. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, et al. 2005. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438:512-515.
25. Guhaniyogi J, Brewer G. 2001. Regulation of mRNA stability in mammalian cells. Gene 265:11-23.
26. Wilson GM, Brewer G. 1999. The search for trans-acting factors controlling messenger RNA decay. Prog Nucleic Acid Res Mol Biol 62:257-291.
27. Antic D, Keene JD. 1997. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation, and posttranscriptional gene expression. Am J Hum Genet 61:273-278.
28. Good PJ. 1995. A conserved family of elav-like genes in vertebrates. Proc Natl Acad Sci USA 92:4557-4561.
29. Keene JD. 1999. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc Natl Acad Sci USA 96:5-7.
30. Liu J, Dalmau J, Szabo A, Rosenfeld M, Huber J, et al. 1995. Paraneoplastic encephalomyelitis antigens bind to the AU-rich elements of mRNA. Neurology 45:544-550.
31. Musunuru K, Darnell RB. 2001. Paraneoplastic neurologic disease antigens: RNA-binding proteins and signaling proteins in neuronal degeneration. Annu Rev Neurosci 24:239-262.
32. Gouble A, Morello D. 2000. Synchronous and regulated expression of two AU-binding proteins, AUF1 and HuR, throughout murine development. Oncogene 19:5377-5384.
33. Szabo A, Dalmau J, Manley G, Rosenfeld M, Wong E, et al. 1991. HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal. Cell 67:325-333.
34. Antar LN, Bassell GJ. 2003. Sunrise at the synapse: the FMRP mRNP shaping the synaptic interface. Neuron 37:555-558.
35. Bardoni B, Mandel JL. 2002. Advances in understanding of fragile X pathogenesis and FMRP function, and in identification of X linked mental retardation genes. Curr Opin Genet Dev 12:284-293.
36. Dalmau J, Furneaux HM, Gralla RJ, Kris MG, Posner JB. 1990. Detection of the anti-Hu antibody in the serum of patients with small cell lung cancer-a quantitative western blot analysis. Ann Neurol 27:544-552.
37. Graus F, Elkon KB, Cordon-Cardo C, Posner JB. 1986. Sensory neuronopathy and small cell lung cancer. Antineuronal antibody that also reacts with the tumor. Am J Med 80:45-52.
38. Anderson KD, Sengupta J, Morin M, Neve RL, Valenzuela CF, et al. 2001. Overexpression of HuD accelerates neurite outgrowth and increases GAP-43 mRNA expression in cortical neurons and retinoic acid-induced embryonic stem cells in vitro. Exp Neurol 168:250-258.
39. Aranda-Abreu GE, Behar L, Chung S, Furneaux H, Ginzburg I. 1999. Embryonic lethal abnormal vision-like RNA-binding proteins regulate neurite outgrowth and tau expression in PC12 cells. J Neurosci 19:6907-6917.
40. Kasashima K, Terashima K, Yamamoto K, Sakashita E, Sakamoto H. 1999. Cytoplasmic localization is required for the mammalian ELAV-like protein HuD to induce neuronal differentiation. Genes Cells 4:667-683.
41. Wakamatsu Y, Weston JA. 1997. Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124:3449-3460.
42. Deschenes-Furry J, Belanger G, Perrone-Bizzozero N, Jasmin BJ. 2003. Post-transcriptional regulation of Acetylcholinesterase mRNAs in nerve growth factor-treated PC12 cells by the RNA-binding protein HuD. J Biol Chem 278:5710-5717.
43. Figueroa A, Cuadrado A, Fan J, Atasoy U, Muscat GE, et al. 2003. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol Cell Biol 23:4991-5004.
44. Noureddine MA, Qin XJ, Oliveira SA, Skelly TJ, van der WJ, et al. 2005. Association between the neuron-specific RNA-binding protein ELAVL4 and Parkinson disease. Hum Genet 117:27-33.
45. Burd CG, Dreyfuss G. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615-621.
46. Kenan DJ, Query CC, Keene JD. 1991. RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci 16:214-220.
47. Okano HJ, Darnell RB. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-3037.
48. Inman MV, Levy S, Mock BA, Owens GC. 1998. Gene organization and chromosome location of the neural-specific RNA binding protein Elavl4. Gene 208:139-145.
49. Steller U, Kohls S, Muller B, Soller R, Muller R, et al. 1996. The RNA binding protein HuD: rat cDNA and analysis of the alternative spliced mRNA in neuronal differentiating cell lines P19 and PC12. Brain Res Mol Brain Res 35:285-296.
50. Tora M, Barbera VM, Real FX. 2000. Detection of HuD transcripts by means of reverse transcriptase and polymerase chain reaction: implications for the detection of minimal residual disease in patients with small cell lung cancer. Cancer Lett 161:157-164.
51. Birney E, Kumar S, Krainer AR. 1993. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res 21:5803-5816.
52. Wang X, Tanaka Hall TM. 2001. Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat Struct Biol 8:141-145.
53. Bakheet T, Williams BR, Khabar KS. 2003. ARED 2.0: an update of AU-rich element mRNA database. Nucleic Acids Res 31:421-423.
54. Pascale A, Amadio M, Scapagnini G, Lanni C, Racchi M, et al. 2005. Neuronal ELAV proteins enhance mRNA stability by a PKCalpha-dependent pathway. Proc Natl Acad Sci USA 102:12065-12070.
55. Chung S, Jiang L, Cheng S, Furneaux H. 1996. Purification and properties of HuD, a neuronal RNA-binding protein. J Biol Chem 271:11518-11524.
56. Bakheet T, Williams BR, Khabar KS. 2006. ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34:0111-0114.
57. Chen CY, Shyu AB. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20:465-470.
58. Xu N, Chen CY, Shyu AB. 1997. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol Cell Biol 17:4611-4621.
59. Park-Lee S, Kim S, Laird-Offringa IA. 2003. Characterization of the interaction between neuronal RNA-binding protein HuD and AU-rich RNA. J Biol Chem 278:39801-39808.
60. Toba G, Qui J, Koushika SP, White K. 2002. Ectopic expression of Drosophila ELAV and human HuD in Drosophila wing disc cells reveals functional distinctions and similarities. J Cell Sci 115:2413-2421.
61. Deschenes-Furry J, Belanger G, Mwanjewe J, Lunde JA, Parks RJ, et al. 2005. The RNA-binding protein HuR binds to acetylcholinesterase transcripts and regulates their expression in differentiating skeletal muscle cells. J Biol Chem 280:25361-25368.
62. Mobarak CD, Anderson KD, Morin M, Beckel-Mitchener A, Rogers SL, et al. 2000. The RNA-binding protein HuD is required for GAP-43 mRNA stability, GAP-43 gene expression, and PKC-dependent neurite outgrowth in PC12 cells. Mol Biol Cell 11:3191-3203.
63. Park S, Myszka DG, Yu M, Littler SJ, Laird-Offringa IA. 2000. HuD RNA Recognition Motifs Play Distinct Roles in the Formation of a Stable Complex with AU-Rich RNA. Mol Cell Biol 20:4765-4772.
64. Beckel-Mitchener AC, Miera A, Keller R, Perrone-Bizzozero NI. 2002. Poly(A) Tail Length-dependent Stabilization of GAP-43 mRNA by the RNA-binding Protein HuD. J Biol Chem 277:27996-28002.
65. Anderson KD, Morin MA, Beckel-Mitchener A, Mobarak CD, Neve RL, et al. 2000. Overexpression of HuD, but not of its truncated form HuD I+II, promotes GAP-43 gene expression and neurite outgrowth in PC12 cells in the absence of nerve growth factor. J Neurochem 75:1103-1114.
66. Abe R, Sakashita E, Yamamoto K, Sakamoto H. 1996. Two different RNA binding activities for the AU-rich element and the poly(A) sequence of the mouse neuronal protein mHuC. Nucleic Acids Res 24:4895-4901.
67. Ma WJ, Chung S, Furneaux H. 1997. The Elav-like proteins bind to AU-rich elements and to the poly(A) tail of mRNA. Nucleic Acids Res 25:3564-3569.
68. Akamatsu W, Okano HJ, Osumi N, Inoue T, Nakamura S, et al. 1999. Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc Natl Acad Sci USA 96:9885-9890.
69. Chagnovich D, Cohn SL. 1996. Binding of a 40-kDa protein to the N-myc 3′-untranslated region correlates with enhanced N-myc expression in human neuroblastoma. J Biol Chem 271:33580-33586.
70. Cuadrado A, Navarro-Yubero C, Furneaux H, Kinter J, Sonderegger P, et al. 2002. HuD binds to three AU-rich sequences in the 3′-UTR of neuroserpin mRNA and promotes the accumulation of neuroserpin mRNA and protein. Nucleic Acids Res 30:2202-2211.
71. Joseph B, Orlian M, Furneaux H. 1998. p21(waf1) mRNA contains a conserved element in its 3′-untranslated region that is bound by the Elav-like mRNA-stabilizing proteins. J Biol Chem 273:20511-20516.
72. Manohar CF, Short ML, Nguyen A, Nguyen NN, Chagnovich D, et al. 2002. HuD, a neuronal-specific RNA-binding protein, increases the in vivo stability of MYCN RNA. J Biol Chem 277:1967-1973.
73. Wein G, Rossler M, Klug R, Herget T. 2003. The 3′-UTR of the mRNA coding for the major protein kinase C substrate MARCKS contains a novel CU-rich element interacting with the mRNA stabilizing factors HuD and HuR. Eur J Biochem 270:350-365.
74. Chung S, Eckrich M, Perrone-Bizzozero N, Kohn DT, Furneaux H. 1997. The Elav-like proteins bind to a conserved regulatory element in the 3′-untranslated region of GAP-43 mRNA. J Biol Chem 272:6593-6598.
75. Layer PG, Willbold E. 1995. Novel functions of cholinesterases in development, physiology and disease. Prog Histochem Cytochem 29:1-94.
76. Soreq H, Seidman S. 2001. Acetylcholinesterase-new roles for an old actor. Nat Rev Neurosci 2:294-302.
77. Fan XC, Steitz JA. 1998. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc Natl Acad Sci USA 95:15293-15298.
78. Saito K, Fujiwara T, Katahira J, Inoue K, Sakamoto H. 2004. TAP/NXF1, the primary mRNA export receptor, specifically interacts with a neuronal RNA-binding protein HuD. Biochem Biophys Res Commun 321:291-297.
79. Aronov S, Aranda G, Behar L, Ginzburg I. 2002. Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J Cell Sci 115:3817-3827
80. Smith CL, Afroz R, Bassell GJ, Furneaux HM, Perrone-Bizzozero NI, et al. 2004. GAP-43 mRNA in growth cones is associated with HuD and ribosomes. J Neurobiol 61:222-235.
81. Atlas R, Behar L, Elliott E, Ginzburg I. 2004. The insulin-like growth factor mRNA binding-protein IMP-1 and the Ras-regulatory protein G3BP associate with tau mRNA and HuD protein in differentiated P19 neuronal cells. J Neurochem 89:613-626.
82. Nielsen J, Christiansen J, Lykke-Andersen J, Johnsen AH, Wewer UM, et al. 1999. A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol Cell Biol 19:1262-1270.
83. Bolognani F, Merhege MA, Twiss J, Perrone-Bizzozero NI. 2004. Dendritic localization of the RNA-binding protein HuD in hippocampal neurons: association with polysomes and upregulation during contextual learning. Neurosci Lett 371:152-157.
84. Antic D, Lu N, Keene JD. 1999. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev 13:449-461.
85. Yano M, Okano HJ, Okano H. 2005. Involvement of Hu and heterogeneous nuclear ribonucleoprotein K in neuronal differentiation through p21 mRNA post-transcriptional regulation. J Biol Chem 280:12690-12699.
86. Barami K, Iversen K, Furneaux H, Goldman SA. 1995. Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebram. J Neurobiol 28:82-101.
87. Marusich MF, Furneaux HM, Henion PD, Weston JA. 1994. Hu neuronal proteins are expressed in proliferating neurogenic cells. J Neurobiol 25:143-155.
88. Weickert CS, Webster MJ, Colvin SM, Herman MM, Hyde TM, et al. 2000. Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J Comp Neurol 423:359-372.
89. Clayton GH, Perez GM, Smith RL, Owens GC. 1998. Expression of mRNA for the elav-like neural-specific RNA binding protein, HuD, during nervous system development. Brain Res Dev Brain Res 109:271-280.
90. Okano H, Akamatsu W, Yano M, Mitsuhashi T, Fujihara H, et al. 2005. RNA-Binding Protein Hu Family Regulates Neural Stem Cell Proliferation and Differentiation. Abstract viewer/Itinerary Planner. Washington, DC: Society for Neuroscience Program No. 598.13.
91. Akamatsu W, Fujihara H, Mitsuhashi T, Yano M, Shibata S, et al. 2005. The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc Natl Acad Sci USA 102:4625-4630.
92. Malter JA. 2001. Regulation of mRNA Stability in the Nervous System and Beyond. J Neurosci Res 66:311-316.
93. Bolognani F, Tanner DC, Merhege M, Deschenes-Furry J, Jasmin B, et al. 2006. In vivo post-transcriptional regulation of GAP-43 mRNA by overexpression of the RNA-binding protein HuD. J Neurochem 96:790-801.
94. Campos AR, Grossman D, White K. 1985. Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J Neurogenet 2:197-218.
95. Jimenez F, Campos-Ortega JA. 1987. Genes in subdivision 1B of the Drosophila melanogaster X-chromosome and their influence on neural development. J Neurogenet 4:179-200.
96. Dalmau J, Furneaux HM, Rosenblum MK, Graus F, Posner JB. 1991. Detection of the anti-Hu antibody in specific regions of the nervous system and tumor from patients with paraneoplastic encephalomyelitis/sensory neuronopathy. Neurology 41:1757-1764.
97. Pascale A, Gusev PA, Amadio M, Dottorini T, Govoni S, et al. 2004. Increase of the RNA-binding protein HuD and posttranscriptional upregulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci USA 101:1217-1222.
98. Quattrone A, Pascale A, Nogues X, Zhao W, Gusev P, et al. 2001. Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proc Natl Acad Sci USA 98:11668-11673.
99. Deschenes-Furry JL, Mousavi K, Smith LE, Parks RJ, Perrone-Bizzonero N, et al. 2003. Post-transcriptional regulation of acetylcholinesterase mRNAs in akotomized neurons. Abstract viewer/Itinerary Planner. Washington, DC: Society for Neuroscience Program No. 471.15.
100. Anderson KD, Merhege MA, Morin M, Bolognani F, Perrone-Bizzozero NI. 2003. Increased expression and localization of the RNA-binding protein HuD and GAP-43 mRNA to cytoplasmic granules in DRG neurons during nerve regeneration. Exp Neurol 183:100-108.
101. Anderson KD, Steward O. 2003. In vivo Expression of the Neuronal-specific RNA-binding Protein HuD in Reference to a Potential Target mRNA (GAP-43) in the Mouse Facial Nucleus During Regeneration. Abstract viewer/Itinerary Planner. Washington, DC: Society for Neuroscience Program No. 78.17.
102. Barreau C, Paillard L, Osborne HB. 2005. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33:7138-7150.
103. Lu JY, Schneider RJ. 2004. Tissue distribution of AU-rich mRNA-binding proteins involved in regulation of mRNA decay. J Biol Chem 279:12974-12979.
104. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, et al. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23:3092-3102.
105. Raineri I, Wegmueller D, Gross B, Certa U, Moroni C. 2004. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res 32:1279-1288.
106. Kiledjian M, DeMaria CT, Brewer G, Novick K. 1997. Identification of AUF1 (heterogeneous nuclear ribonucleoprotein D) as a component of the alpha-globin mRNA stability complex. Mol Cell Biol 17:4870-4876.
107. Sela-Brown A, Silver J, Brewer G, Naveh-Many T. 2000. Identification of AUF1 as a parathyroid hormone mRNA 3′-untranslated region-binding protein that determines parathyroid hormone mRNA stability. J Biol Chem 275:7424-7429.
108. Nassar F, Wegnez M. 2001. Characterization of two promoters of the Xenopus laevis elrD gene. Biochem Biophys Res Commun 283:392-398.
109. King PH. 1996. Cloning the 5′ flanking region of neuron-specific Hel-N1: evidence for positive regulatory elements governing cell-specific transcription. Brain Res 723:141-147.
110. Park HC, Kim CH, Bae YK, Yeo SY, Kim SH, et al. 2000. Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev Biol 227:279-293.
111. Zhao C, He X, Tian C, Meng A. 2006. Two GC-rich boxes in huC promoter play distinct roles in controlling its neuronal specific expression in zebrafish embryos. Biochem Biophys Res Commun 342:214-220.
112. Yao KM, White K. 1994. Neural specificity of elav expression: defining a Drosophila promoter for directing expression to the nervous system J Neurochem 63:41-51.
113. Cuadrado A, Navarro-Yubero C, Furneaux H, Munoz A. 2003. Neuronal HuD gene encoding a mRNA stability regulator is transcriptionally repressed by thyroid hormone. J Neurochem 86:763-773.
114. Abe R, Uyeno Y, Yamamoto K, Sakamoto H. 1994. Tissue-specific expression of the gene encoding a mouse RNA binding protein homologous to human HuD antigen. DNA Res 1:175-180.
115. Samson ML. 1998. Evidence for 3′ untranslated region-dependent autoregulation of the Drosophila gene encoding the neuronal nuclear RNA-binding protein ELAV. Genetics 150:723-733.
116. Yanowitz JL, Deshpande G, Calhoun G, Schedl PD. 1999. An N-terminal truncation uncouples the sex-transforming and dosage compensation functions of sex-lethal. Mol Cell Biol 19:3018-3028.
117. Abe R, Yamamoto K, Sakamoto H. 1996. Target specificity of neuronal RNA-binding protein, Mel-N1: direct binding to the 3′ untranslated region of its own mRNA. Nucleic Acids Res 24:2011-2016.
118. Borgeson CD, Samson ML. 2005. Shared RNA-binding sites for interacting members of the Drosophila ELAV family of neuronal proteins. Nucleic Acids Res 33:6372-6383.
119. Li H, Park S, Kilburn B, Jelinek MA, Henschen-Edman A, et al. 2002. Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated arginine methyltransferase. J Biol Chem 277:44623-44630.
120. Wang W, Fan J, Yang X, Furer-Galban S, Lopez dS I, et al. 2002. AMP-activated kinase regulates cytoplasmic HuR. Mol Cell Biol 22:3425-3436.
121. Fujiwara T, Mori Y, Chu DL, Koyama Y, Miyata S, et al. 2006. CARM1 Regulates Proliferation of PC12 Cells by Methylating HuD. Mol Cell Biol 26:2273-2285.
122. Williamson JR. 2000. Induced fit in RNA-protein recognition. Nat Struct Biol 7:834-837.
123. Kasashima K, Sakashita E, Saito K, Sakamoto H. 2002. Complex formation of the neuron-specific ELAV-like Hu RNA-binding proteins. Nucleic Acids Res 30:4519-4526.
124. Irwin N, Chao S, Goritchenko L, Horiuchi A, Greengard P, et al. 2002. Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19. Proc Natl Acad Sci USA 99:12427-12431.