A Hierarchy of Hu RNA Binding Proteins in Developing and Adult Neurons
Open accessAbstract
The Hu proteins are a group of antigens targeted in an immune-mediated neurodegenerative disorder associated with cancer. We have cloned and characterized four members of the Hu gene family from mouse. We find that the Hu genes encode a large number of alternatively spliced transcripts to produce a series of related neuron-specific RNA binding proteins. Despite this complexity, we have discerned several ordered features of Hu expression. In the embryo, specific Hu genes are expressed in a hierarchy during early neurogenesis. In the E16 developing cortex, mHuB is induced in very early postmitotic neurons exiting the ventricular zone, mHuD is expressed in migrating neurons of the intermediate zone, and mHuC is expressed in mature cortical plate neurons. Such a hierarchy suggests distinct functional roles for each gene in developing neurons. In the adult, all neurons express some set of Hu mRNA and protein. However, specific patterns are evident such that individual neuronal types in the hippocampus, cerebellum, olfactory cortex, neocortex, and elsewhere express from one to several Hu genes. The complexity of potential protein variants within a gene family and of different Hu family members within a neuron suggests a diverse array of function. Given the strong homologies among the Hu proteins, the Drosophila neurogenic gene elav , and the Drosophila splicing factor sxl , we predict that different combinations of Hu proteins determine different neuron-specific aspects of post-transcriptional RNA regulation. Our findings of specific developmental patterns of expression and the correlation between immune targeting of the Hu proteins and adult neurodegenerative disease suggest that the Hu proteins are critical in both the proper development and function of mature neurons.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the developing mouse and rat cerebral cortex, HuD mRNA is present in proliferating neuronal stem/progenitor cells in the ventricular zone, neuroblasts migrating in the intermediate zones, and terminally differentiating neurons in the cortical plate.
“In the developing mouse and rat cerebral cortex, HuD mRNA is present in proliferating neuronal stem/progenitor cells in the ventricular zone, neuroblasts migrating in the intermediate zones, and terminally differentiating neurons in the cortical plate (Okano and Darnell 1997; Clayton et al. 1998).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Okano and Darnell 1997
The Figure 7 caption and “Hierarchies of mHu mRNA expression in developing neurons” section report mHuD mRNA in the intermediate zone and at diminishing levels in the cortical plate, but say it is very weak or absent in differentiated neurons. The section says mHuD mRNA is first evident in intermediate-zone neurons, contrary to the claim of its presence in proliferating ventricular-zone cells. These observations concern mouse cortex; the passages do not report rat cortex. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredHuD is one of the earliest markers of the neuronal phenotype.
“Converging findings suggest that HuD is one of the earliest markers of the neuronal phenotype (Good 1995; Okano and Darnell 1997; Wakamatsu and Weston 1997; Hambardzumyan et al. 2009).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Okano and Darnell 1997
The Abstract reports mHuD expression in migrating neurons during early cortical development, supporting its association with an early neuronal stage. But the sections “Hierarchies of mHu mRNA expression in developing neurons” and “The role of Hu proteins in neural development” identify mHuB, not mHuD, as expressed in the earliest postmitotic neurons. The paper therefore does not establish HuD as one of the earliest markers of the neuronal phenotype. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn the adult mouse and rodent nervous system, HuD mRNA expression is mostly restricted to specific neuronal populations, including large pyramidal-like neurons in layer V of the neocortex and cerebellar cortex (Purkinje cells), the four Cornu Amonis (CA1-4) regions of the hippocampus, dorsal root ganglia, motor neurons in the spinal cord, mitral cells in the olfactory bulb, ganglion and internal P
“In the adult mouse and rodent nervous system, expression of HuD mRNA is mostly restricted to specific neuronal populations, including large pyramidal-like neurons in layer V of the neocortex and cerebellar cortex (Purkinje cells), the four Cornu Amonis (CA1-4) regions of the hippocampus, dorsal root ganglia, and motor neurons in the spinal cord, mitral cells in the olfactory bulb, ganglion and int”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Okano and Darnell 1997
The ‘mHu mRNA expression in adult brain’ section (page unavailable) reports HuD mRNA in layer 5 neocortical neurons, hippocampal pyramidal neurons, dorsal root ganglia, and olfactory mitral cells. But the paper explicitly says HuD is absent from Purkinje cells; it also does not identify spinal motor neurons as HuD-expressing, saying instead that spinal-cord neurons predominantly express HuC. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe HuD protein has a molecular weight of approximately 40 kDa and contains three RNA recognition motifs (RRMs) with a linker region separating the second and third RRM.
“The HuD protein, like all Hu members, has a molecular weight of ∼40 kDa and contains three RNA recognition motifs (RRMs) with a linker region separating the second and third RRM (Fig. 1C; Good 1995; Liu et al. 1995; Okano and Darnell 1997).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Okano and Darnell 1997
The spatial expression of HuD mRNA is partially unique compared to HuB and HuC.
“In situ hybridization analyses of nELAV expression in the mouse brain at day 14 of embryogenesis (E14) have revealed that the spatial expression of HuD mRNA is also partially unique compared to HuB and HuC (Okano and Darnell 1997), thus further supporting the notion that HuD is not completely functionally redundant.”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Okano and Darnell 1997
ELAVL2, ELAVL3 and ELAVL4 show neuronal-specific expression.
“whereas ELAVL2 (also known as HuB), ELAVL3 (also known as HuC) and ELAVL4 (also known as HuD) show neuronal-specific expression”
From The neurogenetics of alternative splicing (2016) · cites this paper as [119]
ELAVL1 is widely expressed in non-neuronal tissues.
“ELAVL1 (also known as HuR or HuA) is widely expressed in non-neuronal tissues”
From The neurogenetics of alternative splicing (2016) · cites this paper as [119]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
Shaw, G. D., & Kamen, R. (1986) · Cell · doi:10.1016/0092-8674(86)90341-7 · Cited by 3,946 · see citing works
Conserved Structures and Diversity of Functions of RNA-Binding Proteins
Burd, C. G., & Dreyfuss, G. (1994) · Science · doi:10.1126/science.8036511 · Cited by 1,878 · see citing works
hnRNP PROTEINS AND THE BIOGENESIS OF mRNA
Dreyfuss, G., Matunis, M. J., Piñol-Roma, S., & Burd, C. G. (1993) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.62.070193.001445 · Cited by 1,558 · see citing works
An autoradiographic analysis of histogenesis in the mouse cerebellum
Miale, I. L., & Sidman, R. L. (1961) · Experimental Neurology · doi:10.1016/0014-4886(61)90055-3 · Cited by 1,015 · see citing works
Dalmau, J., Graus, F., Rosenblum, M. K., & Posner, J. B. (1992) · MEDICINE · doi:10.1097/00005792-199203000-00001 · Cited by 819 · see citing works
Devys, D., Lutz, Y., Rouyer, N., Bellocq, J., & Mandel, J. (1993) · Nature Genetics · doi:10.1038/ng0893-335 · Cited by 781 · see citing works
Cloning and Characterization of HuR, a Ubiquitously Expressed Elav-like Protein
Ma, W.-J., Cheng, S., Campbell, C., Wright, A., & Furneaux, H. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.14.8144 · Cited by 667 · see citing works
Birney, E., Kumar, S., & Krainer, A. R. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.25.5803 · Cited by 665 · see citing works
The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein.
Siomi, H., Siomi, M. C., Nussbaum, R. L., & Dreyfuss, G. (1993) · Cell · doi:10.1016/0092-8674(93)90420-u · Cited by 641 · see citing works
Szabo, A., Dalmau, J., Manley, G., Rosenfeld, M., Wong, E., Henson, J., Posner, J. B., & Furneaux, H. M. (1991) · Cell · doi:10.1016/0092-8674(91)90184-z · Cited by 553 · see citing works
The Nonamer UUAUUUAUU Is the Key AU-Rich Sequence Motif That Mediates mRNA Degradation
Zubiaga, A. M., Belasco, J. G., & Greenberg, M. E. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.4.2219 · Cited by 543 · see citing works
The pre-mRNA binding K protein contains a novel evolutionary conserved motif
Siomi, H., Matunis, M. J., Michael, W. M., & Dreyfuss, G. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.5.1193 · Cited by 533 · see citing works
Mouse-Musashi-1, a Neural RNA-Binding Protein Highly Enriched in the Mammalian CNS Stem Cell
Sakakibara, S., Imai, T., Hamaguchi, K., Okabe, M., Aruga, J., Nakajima, K., Yasutomi, D., Nagata, T., Kurihara, Y., Uesugi, S., et al. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0130 · Cited by 526 · see citing works
Self-citationHu neuronal proteins are expressed in proliferating neurogenic cells
Marusich, M. F., Furneaux, H. M., Henion, P. D., & Weston, J. A. (1994) · Journal of Neurobiology · doi:10.1002/neu.480250206 · Cited by 485 · see citing works
Ullrich, B., Ushkaryov, Y. A., & Südhof, T. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90306-2 · Cited by 460 · see citing works
Tissue specific expression of FMR-1 provides evidence for a functional role in fragile X syndrome
Hinds, H. L., Ashley, C. T., Sutcliffe, J. S., Nelson, D. L., Warren, S. T., Housman, D. E., & Schalling, M. (1993) · Nature Genetics · doi:10.1038/ng0193-36 · Cited by 396 · see citing works
Fujita, S. (1967) · The Journal of Cell Biology · doi:10.1083/jcb.32.2.277 · Cited by 371 · see citing works
Neuronal antinuclear antibody in sensory neuronopathy from lung cancer
Graus, F., Cordon‐Cardo, C., & Posner, J. B. (1985) · Neurology · doi:10.1212/wnl.35.4.538 · Cited by 367 · see citing works
The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages
Robinow, S., & White, K. (1988) · Developmental Biology · doi:10.1016/0012-1606(88)90139-x · Cited by 365 · see citing works
Nakamura, M., Okano, H., Blendy, J. A., & Montell, C. (1994) · Neuron · doi:10.1016/0896-6273(94)90460-x · Cited by 359 · see citing works
Self-citationLevine, T., Gao, F., King, P. H., Andrews, L. G., & Keene, J. D. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.6.3494 · Cited by 356 · see citing works
Lagnado, C. A., Brown, C. Y., & Goodall, G. J. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.7984-7995.1994 · Cited by 330 · see citing works
A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer.Preprint
Min, H., Turck, C. W., Nikolic, J. M., & Black, D. L. (1997) · Genes & Development · doi:10.1101/gad.11.8.1023 · Cited by 330 · see citing works
A conserved family of elav-like genes in vertebrates.
Good, P. J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4557 · Cited by 319 · see citing works
Buckanovich, R. J., Posner, J. B., & Darnell, R. B. (1993) · Neuron · doi:10.1016/0896-6273(93)90077-5 · Cited by 318 · see citing works
Self-citationThe elav Gene Product of Drosophila , Required in Neurons, Has Three RNP Consensus Motifs
Robinow, S., Campos, A. R., Yao, K., & White, K. (1988) · Science · doi:10.1126/science.3144044 · Cited by 300 · see citing works
Abitbol, M. M., Ménini, C., Delezoide, A., Rhyner, T. A., Vekemans, M. J. J., & Mallet, J. J. (1993) · Nature Genetics · doi:10.1038/ng0693-147 · Cited by 284 · see citing works
Darnell, R. B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4529 · Cited by 276 · see citing works
Self-citationDalmau, J. O., Furneaux, H., Cordon‐Cardo, C., & Posner, J. B. (1992) · PubMed Central · Cited by 261 · see citing works
Barami, K., Iversen, K., Furneaux, H., & Goldman, S. A. (1995) · Journal of Neurobiology · doi:10.1002/neu.480280108 · Cited by 209 · see citing works
Buckanovich, R., Yang, Y., & Darnell, R. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-03-01114.1996 · Cited by 192 · see citing works
Self-citationLagnado, C. A., Brown, C. Y., & Goodall, G. J. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.7984 · Cited by 188 · see citing works
King, P. H., Levine, T., Fremeau, R. T., & Keene, J. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-04-01943.1994 · Cited by 167 · see citing works
Yao, K., Samson, M., Reeves, R. K., & White, K. (1993) · Journal of Neurobiology · doi:10.1002/neu.480240604 · Cited by 165 · see citing works
Hu antigens: Reactivity with hu antibodies, tumor expression, and major immunogenic sites
Manley, G. T., Smitt, P. A. E. S., Dalmau, J. O., & Posner, J. B. (1995) · Annals of Neurology · doi:10.1002/ana.410380117 · Cited by 161 · see citing works
Gao, F., Carson, C. C., Levine, T., & Keene, J. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.23.11207 · Cited by 156 · see citing works
Gibbs, R. B., & Pfaff, D. W. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410304 · Cited by 155 · see citing works
Mammalian splicing factor SF1 is encoded by variant cDNAs and binds to RNA.
Arning, S., Grüter, P., Bilbe, G., et al. (1996) · PubMed · Cited by 154 · see citing works
Immediate differentiation of ganglion cells following mitosis in the developing retina
Waid, D. K., & McLoon, S. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90245-7 · Cited by 135 · see citing works
Paraneoplastic Encephalomyelitis Antigens Bind to the AU-rich Elements of mRNA
Liu, J., Dalmau, J., Szabo, A., Rosenfeld, M., Huber, J., & Furneaux, H. (1995) · Neurology · doi:10.1212/wnl.45.3.544 · Cited by 122 · see citing works
Levine, T., Gao, F., King, P. H., et al. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.6.3494-3504.1993 · Cited by 109 · see citing works
Richter, K., Good, P., & Dawid, I. B. (1990) · PubMed · Cited by 101 · see citing works
Corradi, J., Yang, C., Darnell, J. C., Dalmau, J. O., & Darnell, R. B. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-04-01406.1997 · Cited by 97 · see citing works
Self-citationBellen, H. J., Kooyer, S., D'Evelyn, D., & Pearlman, J. (1992) · Genes & Development · doi:10.1101/gad.6.11.2125 · Cited by 92 · see citing works
Kim, Y., & Baker, B. S. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-01045.1993 · Cited by 87 · see citing works
Sakai, K., Gofuku, M., Kitagawa, Y., Ogasawara, T., Hirose, G., Yamazaki, M., Koh, C. S., Yanagisawa, N., & Steinman, L. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.1358 · Cited by 85 · cited 3× · see citing works
“…Xenopus elrA (Good, 1995) and human HuR (Ma et al., 1996) genes], mHuB (homologous to human Hel-N1; Levine et al., 1993), mHuC [corresponding to the human HuC gene (Szabo et al., 1991), also known as ple21 (Sakai et al., 1993)], and mHuD (corresponding to the human HuD gene; Szabo et al., 1991).”
BackgroundImataka, H., Nakayama, K., Yasumoto, K., et al. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32045-8 · Cited by 57 · see citing works
Dropcho, E. J., & King, P. H. (1994) · Annals of Neurology · doi:10.1002/ana.410360212 · Cited by 48 · see citing works
Abe, R. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.11.2011 · Cited by 47 · see citing works
Posner, J. B. (1995) · Perspectives in biology and medicine · doi:10.1353/pbm.1995.0043 · Cited by 30 · see citing works
AU-rich intronic elements affect pre-mRNA 5' splice site selection in Drosophila melanogaster.
McCullough, A. J., & Schuler, M. A. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.12.7689 · Cited by 27 · see citing works
AU-Rich Intronic Elements Affect Pre-mRNA 5′ Splice Site Selection in Drosophila melanogaster
McCullough, A. J., & Schuler, M. A. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.12.7689-7697.1993 · Cited by 11 · see citing works
Posner, J. B., & Furneaux, H. M. (1990) · PubMed · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Adult neurogenesis: from precursors to network and physiology
Abrous, D. N., Koehl, M., & Le Moal, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00055.2003 · Cited by 971 · see citing works
RBM20, a gene for hereditary cardiomyopathy, regulates titin splicing
Guo, W., Schafer, S., Greaser, M. L., Radke, M. H., Liss, M., Govindarajan, T., Maatz, H., Schulz, H., Li, S., Parrish, A. M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2693 · Cited by 589 · see citing works
Diverse molecular functions of Hu proteins
Hinman, M. N., & Lou, H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8252-6 · Cited by 587 · see citing works
Nova-1 Regulates Neuron-Specific Alternative Splicing and Is Essential for Neuronal Viability
Jensen, K. B., Dredge, B. K., Stefani, G., Zhong, R., Buckanovich, R. J., Okano, H. J., Yang, Y. Y. L., & Darnell, R. B. (2000) · Neuron · doi:10.1016/s0896-6273(00)80900-9 · Cited by 426 · see citing works
Self-citationThe neurogenetics of alternative splicing
Vuong, C. K., Black, D. L., & Zheng, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.27 · Cited by 340 · see citing works
The bHLH Gene<i>Hes1</i>as a Repressor of the Neuronal Commitment of CNS Stem Cells
Nakamura, Y., Sakakibara, S.-I., Miyata, T., Ogawa, M., Shimazaki, T., Weiss, S., Kageyama, R., & Okano, H. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00283.2000 · Cited by 316 · see citing works
“TuJ1 and Hu are very early markers for postmitotic neurons that have just finished their final cell division (Lee et al., 1990; Menezes and Luskin, 1994; Sakakibara et al., 1996; Okano and Darnell, 1997; Wakamatsu and Weston, 1997), whereas MAP2 and neurofilament are late neuronal markers for postmigratory, mature neu…”
BackgroundSelf-citationDarnell, J. C., Fraser, C. E., Mostovetsky, O., Stefani, G., Jones, T. A., Eddy, S. R., & Darnell, R. B. (2005) · Genes & Development · doi:10.1101/gad.1276805 · Cited by 287 · see citing works
Self-citationInce-Dunn, G., Okano, H. J., Jensen, K. B., Park, W.-Y., Zhong, R., Ule, J., Mele, A., Fak, J. J., Yang, C., Zhang, C., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.009 · Cited by 212 · see citing works
Self-citationYang, Y. Y. L., Yin, G. L., & Darnell, R. B. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13254 · Cited by 219 · see citing works
Self-citationThe RNA-binding protein HuD regulates neuronal cell identity and maturation
Akamatsu, W., Fujihara, H., Mitsuhashi, T., Yano, M., Shibata, S., Hayakawa, Y., Okano, H. J., Sakakibara, S.-I., Takano, H., Takano, T., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407523102 · Cited by 222 · see citing works
Self-citationRNA Protein Interaction in Neurons
Darnell, R. B. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062912-114322 · Cited by 181 · see citing works
Self-citationMcKee, A. E., Minet, E., Stern, C., Riahi, S., Stiles, C. D., & Silver, P. A. (2005) · BMC Developmental Biology · doi:10.1186/1471-213x-5-14 · Cited by 166 · see citing works
Defining a neuron: neuronal ELAV proteins
Pascale, A., Amadio, M., & Quattrone, A. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7017-y · Cited by 158 · see citing works
Iwano, T., Masuda, A., Kiyonari, H., Enomoto, H., & Matsuzaki, F. (2012) · Development · doi:10.1242/dev.080002 · Cited by 155 · see citing works
De Rubeis, S., & Bagni, C. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.09.013 · Cited by 126 · see citing works
Neuronal ELAV proteins enhance mRNA stability by a PKCα-dependent pathway
Pascale, A., Amadio, M., Scapagnini, G., Lanni, C., Racchi, M., Provenzani, A., Govoni, S., Alkon, D. L., & Quattrone, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504702102 · Cited by 129 · see citing works
Bronicki, L. M., & Jasmin, B. J. (2013) · RNA · doi:10.1261/rna.039164.113 · Cited by 126 · see citing works
NOVA-dependent regulation of cryptic NMD exons controls synaptic protein levels after seizure
Eom, T., Zhang, C., Wang, H., Lay, K., Fak, J., Noebels, J. L., & Darnell, R. B. (2013) · eLife · doi:10.7554/elife.00178 · Cited by 118 · see citing works
Self-citationMansfield, K. D., & Keene, J. D. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr1114 · Cited by 112 · see citing works
A role for the ELAV RNA-binding proteins in neural stem cells: stabilization of<i>Msi1</i>mRNA
Ratti, A., Fallini, C., Cova, L., Fantozzi, R., Calzarossa, C., Zennaro, E., Pascale, A., Quattrone, A., & Silani, V. (2006) · Journal of Cell Science · doi:10.1242/jcs.02852 · Cited by 86 · see citing works
DeBoer, E. M., Azevedo, R., Vega, T. A., Brodkin, J., Akamatsu, W., Okano, H., Wagner, G. C., & Rasin, M.-R. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3703-13.2014 · Cited by 72 · see citing works
Self-citationRatti, A., Fallini, C., Colombrita, C., Pascale, A., Laforenza, U., Quattrone, A., & Silani, V. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m706082200 · Cited by 66 · see citing works
Samson, M.-L. (1998) · Genetics · doi:10.1093/genetics/150.2.723 · Cited by 51 · see citing works
Promotion of exon 6 inclusion in HuD pre-mRNA by Hu protein family members
Wang, H., Molfenter, J., Zhu, H., & Lou, H. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq028 · Cited by 49 · see citing works
Deschênes-Furry, J., Mousavi, K., Bolognani, F., Neve, R. L., Parks, R. J., Perrone-Bizzozero, N. I., & Jasmin, B. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4626-06.2007 · Cited by 43 · see citing works
RNA–Binding Protein HuD as a Versatile Factor in Neuronal and Non–Neuronal Systems
Jung, M., & Lee, E. K. (2021) · Biology · doi:10.3390/biology10050361 · Cited by 39 · see citing works
- Authors
- Okano, H. J., & Darnell, R. B.
- Affiliations
- Rockefeller University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1997-05-01
- Volume
- 17
- Issue
- 9
- Pages
- 3024-3037
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6573636
- OpenAlex
- W2170375626
- Cited by
- 379
- References
- 55
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 9 · 2023: 9 · 2022: 14 · 2021: 11 · 2020: 10 · 2019: 10 · 2018: 12 · 2017: 8 · 2016: 11 · 2015: 10 · 2014: 15 · 2013: 17 · 2012: 21
- FWCI
- 5.57
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Irma T. Hirschl Trust
- National Cancer Institute (CA 09673-18, T32CA009673)
- National Institute of Neurological Disorders and Stroke (R01 NS34389, R01NS034389)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- HU protein, RNA-binding proteins, alternative splicing, neurogenesis, neuronal differentiation, hubs, HUD, HuC, ELAV, Sxl, neurodegenerative diseases, mouse brain development
- MeSH terms
- Animals, Bacterial Proteins, Carrier Proteins, Cloning, Molecular, DNA-Binding Proteins, Humans, Immunohistochemistry, Neurons, RNA, In Situ Hybridization, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
