Axonal mRNA in uninjured and regenerating cortical mammalian axons

Journal of Neuroscience

Volumn 29, Issue 15, 2009, Pages 4697-4707

  Taylor, Anne M ^a,d   Berchtold, Nicole C ^a   Perreau, Victoria M ^a,e   Tu, Christina H ^a   Li Jeon, Noo ^c   Cotman, Carl W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of California at Irvine   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ARTICLE; AXONAL INJURY; CELL ISOLATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; MITOCHONDRION; NERVE FIBER; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; PRIORITY JOURNAL; PROTEIN TRANSPORT; ANIMAL; BIOSYNTHESIS; BRAIN CORTEX; CELL CULTURE; CHEMISTRY; COMPARATIVE STUDY; DNA MICROARRAY; GENETICS; IN VITRO STUDY; ISOLATION AND PURIFICATION; METHODOLOGY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; AXONS; AXOTOMY; CELLS, CULTURED; CEREBRAL CORTEX; NERVE REGENERATION; NEUROGENESIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 65549139891     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6130-08.2009     Document Type: Article

References (55)

1. Aschrafi A, Schwechter AD, Mameza MG, Natera-Naranjo O, Gioio AE, Kaplan BB (2008) MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympa-thetic neurons. J Neurosci 28:12581-12590.
2. Asher RA, Morgenstern DA, Shearer MC, Adcock KH, Pesheva P, Fawcett JW (2002) Versican is upregulated in CNS injury and is a product of oligo-dendrocyte lineage cells. J Neurosci 22:2225-2236. (Pubitemid 35386522)
3. Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, Reichardt LF (2003) Role of beta-catenin in synaptic vesicle localization and pre-synaptic assembly. Neuron 40:719-731. (Pubitemid 37431033)
4. Bassell GJ, Singer RH, Kosik KS (1994) Association of poly(A) mRNA with microtubules in cultured neurons. Neuron 12:571-582. (Pubitemid 24100888)
5. Beaudoin GM 3rd (2006) Con-nectin axons and dendrites. J Cell Biol 174:7-9. (Pubitemid 43992891)
6. Besse F, Ephrussi A (2008) Translational control of localized mRNAs: Re-stricting protein synthesis in space and time. Nat Rev Mol Cell Biol 9:971-980.
7. Blizzard CA, Haas MA, Vickers JC, Dickson TC (2007) Cellular dynamics underlying regeneration of damaged axons differs from initial axon de-velopment. Eur J Neurosci 26:1100-1108. (Pubitemid 47346766)
8. Boulanger LM, Shatz CJ (2004) Immune signalling in neural development, synaptic plasticity and disease. Nat Rev Neurosci 5:521-531. (Pubitemid 38868548)
9. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-1026. (Pubitemid 34075393)
10. Choe CU, Ehrlich BE (2006) The inositol 1,4,5-trisphosphate receptor (IP3R) and its regulators: Sometimes good and sometimes bad teamwork. SciSTKE2006:re15.
11. Chun JT, Gioio AE, Crispino M, Giuditta A, Kaplan BB (1996) Differential compartmentalization of mRNAs in squid giant axon. J Neurochem 67:1806-1812. (Pubitemid 26349652)
12. Gioio AE, Eyman M, Zhang H, Lavina ZS, Giuditta A, Kaplan BB (2001) Local synthesis of nuclear-encoded mitochondrial proteins in the presyn-aptic nerve terminal. J Neurosci Res 64:447-453. (Pubitemid 32521764)
13. Giustetto M, Hegde AN, Si K, Casadio A, Inokuchi K, Pei W, Kandel ER, Schwartz JH (2003) Axonal transport of eukaryotic translation elonga-tion factor 1 {alpha} mRNA couples transcription in the nucleus to long-term facilitation at the synapse. Proc Natl Acad Sci USA 100:13680-13685. (Pubitemid 37444799)
14. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van-Minnen J, Twiss JL, Fainzilber M (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104. (Pubitemid 38032787)
15. Hillefors M, Gioio AE, Mameza MG, Kaplan BB (2007) Axon viability and mitochondrial function are dependent on local protein synthesis in sympathetic neurons. Cell Mol Neurobiol 27:701-716. (Pubitemid 47485283)
16. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6:201-214. (Pubitemid 40342415)
17. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003a) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15.
18. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003b) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
19. Junutula JR, De Maziéere AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, Klumperman J, Scheller RH (2004) Rabl4 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 15:2218-2229. (Pubitemid 38580640)
20. Kaeser PS, Kwon HB, Chiu CQ, Deng L, Castillo PE, Siidhof TC (2008) RIM 1 alpha and RIMlbeta are synthesized from distinct promoters of the RIM1 gene to mediate differential but overlapping synaptic functions. J Neurosci 28:13435-13447.
21. Kleiman R, Banker G, Steward O (1994) Development of subcellular mRNA compartmentation in hippocampal neurons in culture. J Neurosci 14:1130-1140. (Pubitemid 24081910)
22. Koenig E, Martin R, Titmus M, Sotelo-Silveira JR (2000) Cryptic peripheral ribosomal domains distributed intermittently along mammalian myelin-ated axons. J Neurosci 20:8390-8400.
23. Kwiatkowski AV, Weis WI, Nelson WJ (2007) Catenins: Playing both sides of the synapse. Curr Opin Cell Biol 19:551-556. (Pubitemid 350016851)
24. Lee SK, Hollenbeck PJ (2003) Organization and translation of mRNA in sympathetic axons. J Cell Sci 116:4467-4478. (Pubitemid 37369601)
25. Lim BK, Matsuda N, Poo MM (2008) Ephrin-B reverse signaling promotes structural and functional synaptic maturation in vivo. Nat Neurosci 11:160-169.
26. Maehlen J, Schröoder HD, Klareskog L, Olsson T, Kristensson K (1988) Axo-tomy induces MHC class I antigen expression on rat nerve cells. Neurosci Lett 92:8-13. (Pubitemid 18217412)
27. Moccia R, Chen D, Lyles V, Kapuya E, E Y, Kalachikov S, Spahn CM, Frank 1, Kandel ER, Barad M, Martin KC (2003) An unbiased cDNA library pre-pared from isolated Aplysia sensory neuron processes is enriched for cy-toskeletal and translational mRNAs. J Neurosci 23:9409-9417. (Pubitemid 37323041)
28. Okabe N, Shimizu K, Ozaki-Kuroda K, Nakanishi H, Morimoto K, Takeuchi M, Katsumaru H, Murakami F, Takai Y (2004) Contacts between the commissural axons and the floor plate cells are mediated by nectins. Dev Biol 273:244-256. (Pubitemid 39140901)
29. Oliveira AL, Thams S, Lidman O, Piehl F, Hokfelt T, Karre K, Lindåa H, Cullheim S (2004) From The Cover: A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl AcadSciUSA 101:17843-17848.
30. Olsson T, Kristensson K, Ljungdahl A, Maehlen J, Holmdahl R, Klareskog L (1989) Gamma-interferon-like immunoreactivity in axotomized rat motor neurons. J Neurosci 9:3870-3875. (Pubitemid 20004881)
31. Park JW, Vahidi B, Taylor AM, Rhee SW, Jeon NL (2006) Microfluidic cul-ture platform for neuroscience research. Nat Protocols 1:2128-2136. (Pubitemid 46773335)
32. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, Fainzilber M (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45:715-726. (Pubitemid 40320706)
33. Piper M, Holt C (2004) RNA translation in axons. Annu Rev Cell Dev Biol 20:505-523. (Pubitemid 39488648)
34. Poon MM, Choi SH, Jamieson CA, Geschwind DH, Martin KC (2006) Identification of Process-Localized mRNAs from Cultured Rodent Hip-pocampal Neurons. J Neurosci 26:13390-13399. (Pubitemid 46011650)
35. Rhee SW, Taylor AM, Tu CH, Cribbs DH, Cotman CW, Jeon NL (2005) Patterned cell culture inside microfluidic devices. Lab Chip 5:102-107. (Pubitemid 40139347)
36. Rust RS (1994) Energy metabolism of developing brain. Curr Opin Neurol 7:160-165. (Pubitemid 24096877)
37. Scarpulla RC (2008) Transcriptional paradigms in mammalian mitochon-drial biogenesis and function. Physiol Rev 88:611-638.
38. Sotelo-Silveira J, Crispino M, Puppo A, Sotelo JR, Koenig E (2008) Myelin-ated axons contain beta-actin mRNA and ZBP-1 in periaxoplasmic ribo-somal plaques and depend on cyclic AMP and F-actin integrity for in vitro translation. J Neurochem 104:545-557. (Pubitemid 350293879)
39. Süudhof TC (2008) Neuroligins and neurexins link synaptic function to cog-nitive disease. Nature 455:903-911.
40. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49-58. (Pubitemid 44466643)
41. Sutton MA, Taylor AM, Ito HT, Pham A, Schuman EM (2007) Postsynaptic decoding of neural activity: Eef2 as a biochemical sensor coupling min-iature synaptic transmission to local protein synthesis. Neuron 55:648-661.
42. Taylor AM, Rhee SW, Tu CH, Cribbs DH, Cotman CW, Jeon NL (2003) Microfluidic multicompartment device for neuroscience research. Lang-muir 19:1551-1556.
43. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL (2005) A microfluidic culture platform for CNS axonal injury, regener-ation and transport. Nat Methods 2:599-605. (Pubitemid 41086851)
44. Tsokas P, Grace EA, Chan P, Ma T, Sealfon SC, Iyengar R, Landau EM, Blitzer RD (2005) Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J Neurosci 25:5833-5843. (Pubitemid 40847896)
45. van Niekerk EA, Willis DE, Chang JH, Reumann K, Heise T, Twiss JL (2007) Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc Natl Acad Sci U S A 104:12913-12918. (Pubitemid 47255254)
46. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW (2005) Axonal protein synthesis and degradation are necessary for effi-cient growth cone regeneration. J Neurosci 25:331-342. (Pubitemid 40105603)
47. Vik-Mo EO, Oltedal L, Hoivik EA, Kleivdal H, Eidet J, Davanger S (2003) Sec6 is localized to the plasma membrane of mature synaptic terminals and is transported with secretogranin II-containing vesicles. Neuro-science 119:73-85. (Pubitemid 36577412)
48. von Gertten C, Flores Morales A, Holmin S, Mathiesen T, Nordqvist AC (2005) Genomic responses in rat cerebral cortex after traumatic brain injury. BMC Neurosci 6:69. (Pubitemid 41800116)
49. Weiner OD, Zorn AM, Krieg PA, Bittner GD (1996) Medium weight neurotilament mRNA in goldfish Mauthner axoplasm. Neurosci Lett 213:83-86. (Pubitemid 26252830)
50. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL (2005) Differential transport and local trans-lation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 25:778-791. (Pubitemid 40170992)
51. Willis DE, Twiss JL (2006) The evolving roles of axonally synthesized pro-teins in regeneration. Curr Opin Neurobiol 16:111-118. (Pubitemid 43221861)
52. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL (2007) Extracellular stimuli specifically regulate localized levels of individual neuronal mR-NAs. J Cell Biol 178:965-980. (Pubitemid 47443320)
53. Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, Urquhart ER, Jaffrey SR (2005) Local translation of RhoA regulates growth cone collapse. Nature 436:1020-1024. (Pubitemid 41191685)
54. Yudin D, Hanz S, Yoo S, Iavnilovitch E, Willis D, Gradus T, Vuppalanchi D, Segal-Ruder Y, Ben-Yaakov K, Hieda M, Yoneda Y, Twiss JL, Fainzilber M (2008) Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron 59:241-252.
55. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL (2001) A functional role for intra-axonal protein synthesis dur-ing axonal regeneration from adult sensory neurons. J Neurosci 21:9291-9303. (Pubitemid 33096873)