The RNA-binding protein MARTA2 regulates dendritic targeting of MAP2 mRNAs in rat neurons

Journal of Neurochemistry

Volumn 124, Issue 5, 2013, Pages 670-684

  Zivraj, Krishna H ^a,d   Rehbein, Monika ^a   Ölschläger Schütt, Janin ^a   Schob, Claudia ^a   Falley, Katrin ^a   Buck, Friedrich ^a   Schweizer, Michaela ^a   Schepis, Antonino ^b   Kremmer, Elisabeth ^c   Richter, Dietmar ^a   Kreienkamp, Hans Jürgen ^a   Kindler, Stefan ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

kinesin; microtubule; molecular motor; ribonucleoprotein particle; RNA transport; trans acting factor

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MAP2 RNA TRANS ACTING PROTEIN 2; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE PROTEIN; PROTEIN KIF5; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; GENE TARGETING; GENETIC TRANSCRIPTION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; RNA TRANSPORT;

ANIMALS; BLOTTING, WESTERN; DENDRITES; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MASS SPECTROMETRY; MICROSCOPY, IMMUNOELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PROTEIN TRANSPORT; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84874035223     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12079     Document Type: Article

References (53)

1. Baumann S., Pohlmann T., Jungbluth M., Brachmann A., and, Feldbrugge M., (2012) Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J. Cell Sci. 125, 2740-2752.
2. Bianco A., Dienstbier M., Salter H. K., Gatto G., and, Bullock S. L., (2010) Bicaudal-D regulates fragile X mental retardation protein levels, motility, and function during neuronal morphogenesis. Curr. Biol. 20, 1487-1492.
3. Blässe P., Guillemin I., Schindler J., Schweizer M., Delpire E., Khiroug L., Friauf E., and, Nothwang H. G., (2006) Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J. Neurosci. 26, 10407-10419. (Pubitemid 44564591)
4. Blichenberg A., Schwanke B., Rehbein M., Garner C. C., Richter D., and, Kindler S., (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J. Neurosci. 19, 8818-8829. (Pubitemid 30226703)
5. Bolognani F., and, Perrone-Bizzozero N. I., (2008) RNA-protein interactions and control of mRNA stability in neurons. J. Neurosci. Res. 86, 481-489. (Pubitemid 351204460)
6. Braddock D. T., Baber J. L., Levens D., and, Clore G. M., (2002a) Molecular basis of sequence-specific single-stranded DNA recognition by KH domains: solution structure of a complex between hnRNP K KH3 and single-stranded DNA. EMBO J. 21, 3476-3485. (Pubitemid 34760579)
7. Braddock D. T., Louis J. M., Baber J. L., Levens D., and, Clore G. M., (2002b) Structure and dynamics of KH domains from FBP bound to single-stranded DNA. Nature 415, 1051-1056. (Pubitemid 34193456)
8. Bramham C. R., and, Wells D. G., (2007) Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8, 776-789. (Pubitemid 47462112)
9. Brendel C., Rehbein M., Kreienkamp H. J., Buck F., Richter D., and, Kindler S., (2004) Characterization of Staufen 1 ribonucleoprotein complexes. Biochem. J. 384, 239-246. (Pubitemid 39656235)
10. Briata P., Forcales S. V., Ponassi M., Corte G., Chen C. Y., Karin M., Puri P. L., and, Gherzi R., (2005) p38-dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts. Mol. Cell 20, 891-903. (Pubitemid 41814878)
11. Briata P., Chen C. Y., Giovarelli M., Pasero M., Trabucchi M., Ramos A., and, Gherzi R., (2011) KSRP, many functions for a single protein. Front. Biosci. 16, 1787-1796.
12. Bullock S. L., (2011) Messengers, motors and mysteries: sorting of eukaryotic mRNAs by cytoskeletal transport. Biochem. Soc. Trans. 39, 1161-1165.
13. Burkhardt J. K., Echeverri C. J., Nilsson T., and, Vallee R. B., (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139, 469-484. (Pubitemid 27459318)
14. Cajigas I. J., Will T., and, Schuman E. M., (2010) Protein homeostasis and synaptic plasticity. EMBO J. 29, 2746-2752.
15. Chen C. Y., Gherzi R., Ong S. E., Chan E. L., Raijmakers R., Pruijn G. J., Stoecklin G., Moroni C., Mann M., and, Karin M., (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107, 451-464. (Pubitemid 33152781)
16. Chung H. J., and, Levens D., (2005) c-myc expression: keep the noise down! Mol. Cells 20, 157-166.
17. Chung H. J., Liu J., Dundr M., Nie Z., Sanford S., and, Levens D., (2006) FBPs are calibrated molecular tools to adjust gene expression. Mol. Cell. Biol. 26, 6584-6597. (Pubitemid 44277896)
18. Dahm R., Kiebler M., and, Macchi P., (2007) RNA localisation in the nervous system. Semin. Cell Dev. Biol. 18, 216-223. (Pubitemid 46756364)
19. Danckwardt S., Gantzert A. S., Macher-Goeppinger S., Probst H. C., Gentzel M., Wilm M., Grone H. J., Schirmacher P., Hentze M. W., and, Kulozik A. E., (2011) p38 MAPK controls prothrombin expression by regulated RNA 3′ end processing. Mol. Cell 41, 298-310.
20. Davidovic L., Jaglin X. H., Lepagnol-Bestel A. M., Tremblay S., Simonneau M., Bardoni B., and, Khandjian E. W., (2007) The fragile X mental retardation protein is a molecular adaptor between the neurospecific KIF3C kinesin and dendritic RNA granules. Hum. Mol. Genet. 16, 3047-3058. (Pubitemid 350131323)
21. Davis-Smyth T., Duncan R. C., Zheng T., Michelotti G., and, Levens D., (1996) The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J. Biol. Chem. 271, 31679-31687. (Pubitemid 26408632)
22. Dictenberg J. B., Swanger S. A., Antar L. N., Singer R. H., and, Bassell G. J., (2008) A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell 14, 926-939. (Pubitemid 351757204)
23. Falley K., Schütt J., Iglauer P., Menke K., Maas C., Kneussel M., Kindler S., Wouters F. S., Richter D., and, Kreienkamp H. J., (2009) Shank1 mRNA: dendritic transport by kinesin and translational control by the 5′untranslated region. Traffic 10, 844-857.
24. Gherzi R., Lee K. Y., Briata P., Wegmuller D., Moroni C., Karin M., and, Chen C. Y., (2004) A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell 14, 571-583. (Pubitemid 38739081)
25. Gu W., Pan F., Zhang H., Bassell G. J., and, Singer R. H., (2002) A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons. J. Cell Biol. 156, 41-51. (Pubitemid 34846934)
26. Hachet O., and, Ephrussi A., (2004) Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428, 959-963. (Pubitemid 38560311)
27. Hirokawa N., (2006) mRNA transport in dendrites: RNA granules, motors, and tracks. J. Neurosci. 26, 7139-7142.
28. Huang Y. S., Carson J. H., Barbarese E., and, Richter J. D., (2003) Facilitation of dendritic mRNA transport by CPEB. Genes Dev. 17, 638-653. (Pubitemid 36307548)
29. Iacoangeli A., Rozhdestvensky T. S., Dolzhanskaya N., Tournier B., Schütt J., Brosius J., Denman R. B., Khandjian E. W., Kindler S., and, Tiedge H., (2008) On BC1 RNA and the fragile X mental retardation protein. Proc. Natl Acad. Sci. USA 105, 734-739. (Pubitemid 351171777)
30. Jansen R. P., and, Niessing D., (2012) Assembly of mRNA-protein complexes for directional mRNA transport in eukaryotes-an overview. Curr. Protein Pept. Sci. 13, 284-293.
31. Jeong J. H., Nam Y. J., Kim S. Y., Kim E. G., Jeong J., and, Kim H. K., (2007) The transport of Staufen2-containing ribonucleoprotein complexes involves kinesin motor protein and is modulated by mitogen-activated protein kinase pathway. J. Neurochem. 102, 2073-2084. (Pubitemid 47329284)
32. Johnson E. M., Kinoshita Y., Weinreb D. B., Wortman M. J., Simon R., Khalili K., Winckler B., and, Gordon J., (2006) Role of Pur alpha in targeting mRNA to sites of translation in hippocampal neuronal dendrites. J. Neurosci. Res. 83, 929-943.
33. Kanai Y., Dohmae N., and, Hirokawa N., (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525. (Pubitemid 39094678)
34. Kindler S., and, Kreienkamp H. J., (2012) Dendritic mRNA targeting and translation, in Synaptic Plasticity (, Kreutz M. R., and, Sala C., eds), pp. 285-305, Springer-Verlag, Wien.
35. Kindler S., Dieterich D. C., Schütt J., Sahin J., Karpova A., Mikhaylova M., Schob C., Gundelfinger E. D., Kreienkamp H. J., and, Kreutz M. R., (2009) Dendritic mRNA targeting of Jacob and N-methyl-d-aspartate-induced nuclear translocation after calpain-mediated proteolysis. J. Biol. Chem. 284, 25431-25440.
36. Kolev N. G., and, Huber P. W., (2003) VgRBP71 stimulates cleavage at a polyadenylation signal in Vg1 mRNA, resulting in the removal of a cis-acting element that represses translation. Mol. Cell 11, 745-755. (Pubitemid 36385127)
37. Kress T. L., Yoon Y. J., and, Mowry K. L., (2004) Nuclear RNP complex assembly initiates cytoplasmic RNA localization. J. Cell Biol. 165, 203-211. (Pubitemid 38544523)
38. Kroll T. T., Zhao W. M., Jiang C., and, Huber P. W., (2002) A homolog of FBP2/KSRP binds to localized mRNAs in Xenopus oocytes. Development 129, 5609-5619. (Pubitemid 36054606)
39. Kurth I., Thompson D. A., Ruther K., et al,. (2007) Targeted disruption of the murine retinal dehydrogenase gene Rdh12 does not limit visual cycle function. Mol. Cell. Biol. 27, 1370-1379. (Pubitemid 46239819)
40. Levens D., (2008) How the c-myc promoter works and why it sometimes does not. J. Natl. Cancer Inst. Monogr. 39, 41-43.
41. Ling S. C., Fahrner P. S., Greenough W. T., and, Gelfand V. I., (2004) Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc. Natl Acad. Sci. USA 101, 17428-17433. (Pubitemid 39657421)
42. Linker K., Pautz A., Fechir M., Hubrich T., Greeve J., and, Kleinert H., (2005) Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR. Nucleic Acids Res. 33, 4813-4827. (Pubitemid 41418881)
43. Monshausen M., Putz U., Rehbein M., Schweizer M., DesGroseillers L., Kuhl D., Richter D., and, Kindler S., (2001) Two rat brain Staufen isoforms differentially bind RNA. J. Neurochem. 76, 155-165. (Pubitemid 32044378)
44. Okabe S., and, Hirokawa N., (1989) Rapid turnover of microtubule- associated protein MAP2 in the axon revealed by microinjection of biotinylated MAP2 into cultured neurons. Proc. Natl Acad. Sci. USA 86, 4127-4131. (Pubitemid 19154749)
45. Pan F., Hüttelmaier S., Singer R. H., and, Gu W., (2007) ZBP2 facilitates binding of ZBP1 to beta-actin mRNA during transcription. Mol. Cell. Biol. 27, 8340-8351. (Pubitemid 350234245)
46. Rehbein M., Kindler S., Horke S., and, Richter D., (2000) Two trans-acting rat-brain proteins, MARTA1 and MARTA2, interact specifically with the dendritic targeting element in MAP2 mRNAs. Brain Res. Mol. Brain Res. 79, 192-201. (Pubitemid 30495545)
47. Rehbein M., Wege K., Buck F., Schweizer M., Richter D., and, Kindler S., (2002) Molecular characterization of MARTA1, a protein interacting with the dendritic targeting element of MAP2 mRNAs. J. Neurochem. 82, 1039-1046. (Pubitemid 34966616)
48. Schepis A., Stauber T., and, Krijnse Locker J., (2007) Kinesin-1 plays multiple roles during the vaccinia virus life cycle. Cell. Microbiol. 9, 1960-1973. (Pubitemid 47087087)
49. Schütt J., Falley K., Richter D., Kreienkamp H. J., and, Kindler S., (2009) Fragile X mental retardation protein regulates the levels of scaffold proteins and glutamate receptors in postsynaptic densities. J. Biol. Chem. 284, 25479-25487.
50. Tang S. J., Meulemans D., Vazquez L., Colaco N., and, Schuman E., (2001) A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 32, 463-475. (Pubitemid 33082047)
51. Trabucchi M., Briata P., Garcia-Mayoral M., Haase A. D., Filipowicz W., Ramos A., Gherzi R., and, Rosenfeld M. G., (2009) The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459, 1010-1014.
52. Villace P., Marion R. M., and, Ortin J., (2004) The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs. Nucleic Acids Res. 32, 2411-2420. (Pubitemid 38854795)
53. Vollmeister E., Schipper K., and, Feldbrugge M., (2012) Microtubule-dependent mRNA transport in the model microorganism Ustilago maydis. RNA Biol. 9, 261-268.