Ribosomal distributions in axons of mammalian myelinated fibers

Journal of Neuroscience Research

Volumn 85, Issue 10, 2007, Pages 2087-2098

  Kun, Alejandra ^a,b   Otero, Leonardo ^a   Sotelo Silveira, José R ^a,b   Sotelo, José R ^b  

^a UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^b INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

Author keywords

Anti ribosome antibody; Myelinated axons; RNPs

Indexed keywords

GAMMA GLOBIN; KINESIN; POLYCLONAL ANTIBODY; RIBOSOME PROTEIN; RNA BINDING PROTEIN; SPHINGOLIPID ACTIVATOR PROTEIN 2;

ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOCYTOCHEMISTRY; IMMUNODETECTION; IN SITU HYBRIDIZATION; MYELINATED NERVE; MYELINATION; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SPINAL ROOT;

ANIMALS; AXONS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; NERVE FIBERS, MYELINATED; RATS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, RIBOSOMAL; SCIATIC NERVE; TISSUE DISTRIBUTION;

EID: 34547439282     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21340     Document Type: Article

References (69)

1. Alvarez J, Giuditta A, Koenig E. 2000. Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog Neurobiol 62:1-62.
2. Alvarez J, Torres JC. 1985. Slow axoplasmic transport: a fiction? J Theor Biol 112:627-651.
3. Antic D, Keene JD. 1998. Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J Cell Sci 111:183-197.
4. 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 PC 12 cells. J Neurosci 19:6907-6917.
5. Aronov E, 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.
6. Aronov E, Aranda G, Behar L, Ginzburg I. 2001. Axonal Tau mRNA localization coincides with TAU protein in living neuronal cells and depends on axonal targeting signal. J Neurosci 21:6577-6587.
7. Adas 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.
8. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS. 1998. Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 18:251-265.
9. Benech C, Sotelo JR, Menendez J, Correa-Luna R. 1982. Auto radiographic study of RNA and protein synthesis in sectioned peripheral nerves. Exp Neurol 76:72-82.
10. Bleher R, Martin R. 2001. Ribosomes in the squid giant axon. Neuroscience 107:527-534.
11. Brittis PA, Lu Q, Flanagan JG. 2002. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110:223-235.
12. Bunge MB. 1973. Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture. J Cell Biol 56:713-735.
13. Butler JE, Feldbush TL, McGivern PL, Stewart N. 1978. The enzyme-linked immunosorbent assay (ELISA): a measure of antibody concentration or affinity. Immunochemistry 15:131-136.
14. Calliari A, Sotelo-Silveira J, Costa MC, Nogueira J, Cameron LC, Kun A, Benech J, Sotelo JR. 2002. Myosin Va is locally synthesized following nerve injury. Cell Motil Cytoskeleton 51:169-176.
15. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
16. Crispino M, Kaplan BB, Martin R, Alvarez J, Chun JT, Benech JC, Giuditta A. 1997. Active polysomes are present in the large presynaptic endings of the synaptosomal fraction from squid brain. J Neurosci 17:7694-7702.
17. Gainer H, Tasaki I, Lasek RJ. 1977. Evidence for the glia-neuron protein transfer hypothesis from intracellular perfusion studies of squid giant axons. J Cell Biol 74:524-530.
18. Gambetti P, Autilio-Gambetti L, Shafer B, Pfaff LD. 1973. Quantitative auto radiographic study of labeled RNA in rabbit optic nerve after intraocular injection of (3H) uridine. J Cell Biol 59:677-684.
19. Giuditta A, Cupello A, Lazzarini G. 1980. Ribosomal RNA in the axoplasm of the squid giant axon. J Neurochem 34:1757-1760.
20. Giuditta A, Hunt T, Santella L. 1986. Messenger RNA in squid axoplasm. Neurochem Intern 8:435-442.
21. Giuditta A, Kaplan BB, van Minen J, Alvarez J, Koenig E. 2002. Axonal and presynaptic protein synthesis: new insights into the biology of the neuron. Trends Neurosci 25:400-404.
22. Giuditta A, Matafora S, Felsani A, Del Rio A. 1977. Factors for protein synthesis in the axoplasm of squid giant axons. J Neurochem 28:1393-1395.
23. Giuditta A, Menichini E, Perrone Capano C, Langella M, Martin R, Castigli E, Kaplan BB. 1991. Active polysomes in the axoplasm of the squid giant axon. J Neurosci Res 28:18-28.
24. Hengst U, Cox LJ, Macosko EZ, Jaffrey SR. 2006. Functional and selective RNA interference in developing axons and growth cones. J Neurosci 26:5727-5732.
25. Kiebler MA, Bassell GJ. 2006. Neuronal RNA granules: movers and makers. Neuron 51:685-690.
26. Kindler S, Wang H, Richter D, Tiedge H. 2005. RNA transport and local control of translation. Annu Rev Cell Dev Biol 21:223-245.
27. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Elhsman MH, Bassell GJ, Kosik KS. 1996. Translocation of RNA granules in living neurons. J Neurosci 16:7812-7820.
28. Koenig E. 1979. Ribosomal RNA in Mauthner axon: implication for a protein synthesizing machinery in the myelinated axon. Brain Res 174:95-107.
29. Koenig E, Giuditta A. 1999. Protein-synthesizing machinery in the axon compartment. Neuroscience 89:5-15.
30. Koenig E, Martin R. 1996. Cortical plaque-like structures identify ribosome-containing domains in the Mauthner cell axon. J Neurosci 16:1400-1411.
31. Koenig E, Martin R, Titmus M, Sotelo-Silveira JR. 2000. Cryptic peripheral ribosomal domains distributed intermittendy along mammalian myelinated axons. J Neurosci 20:8390-8400.
32. Krichevsky AM, Kosik KS. 2001. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683-696.
33. Lee SK, Hollenbeck PJ. 2003. Organization and translation of mRNA in sympathetic axons. J Cell Sci 16:4467-4478.
34. Li YC, Cheng CX, Li YN, Shimada O, Atsumi S. 2005a. Beyond the initial axon segment of the spinal motor axon: fasciculated microtubules and polyribosomal clusters. J Anat 206:535-542.
35. Li YC, Li YN, Cheng CX, Sakamoto H, Kawate T, Shimada O, Atsumi S. 2005b. Subsurface cisterna-lined axonal invaginations and double-walled vesicles at the axonal-myelin sheath interface. Neurosci Res 53:298-303.
36. Martin KC. 2004. Local protein synthesis during axon guidance and synaptic plasticity. Curr Opin Neurobiol 14:305-310.
37. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER. 1997. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927-938.
38. Martin R, Fritz W, Giuditta A. 1989. Visualization of polyribosomes in the postsynaptic area of the squid giant synapse by electron spectroscopy imaging. J Neurocytol 18:11-18.
39. Martin R, Vaida B, Bleher R, Crispino M, Giuditta A. 1998 Protein synthesizing units in presynaptic and postsynaptic domains of squid neurons. J Cell Sci 111:3157-3166.
40. Ming GL, Wong ST, Henley J, Yuan XB, Song HJ, Spitzer NC, Poo MM. 2002 Adaptation in the chemotactic guidance of nerve growth cones. Nature 417:411-418.
41. Mobarak CD, Anderson KD, Morin M, Beckel-Mitchener A, Rogers SL, Fumeaux H, King P, Perrone-Bizzozero NI. 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.
42. Muslimov IA, Titmus M, Koenig E, Tiedge H. 2002. Transport of neuronal BC1 RNA in Mauthner axons. J Neurosci 22:4293-4301.
43. Pannese E, Ledda M. 1991. Ribosomes in myelinated axons of the rabbit spinal ganglion neurons. J Submicrosc Cytol Pathol 23:33-38.
44. Pearce J, Lnenicka GA, Govind CK. 2003. Regenerating crayfish motor axons assimilate glial cells and sprout in cultured explants. J Comp Neurol 464:449-462.
45. Perrone-Capano C, Crispino M, Menichini E, Kaplan BB, Giuditta A. 1999. Ribosomal RNAs synthesized by isolated squid nerves and ganglia differ from native ribosomal RNAs. J Neurochem 72:910-978.
46. Piper M, Holt C. 2004. RNA translation in axons. Annu Rev Cell Dev Biol 20:505-523.
47. Rapallino MV, Cupello A, Giuditta A. 1988. Axoplasmic RNA species synthesized in the isolated squid giant axon. Neurochem Res 13:625-631.
48. Skoff RP, Hamberger V. 1974. Fine structure of dendritic and axonal growth cones in embryonic chick spinal cord. J Comp Neurol 153:107-148.
49. Smith CL, Afroz R, Bassell GJ, Furneaux HM, Perrone-Bizzozero NI, Burry RW. 2004. GAP-43 mRNA in growth cones is associated with HuD and ribosomes. J Neurobiol 61:222-235.
50. Sotelo JR, Benech C, Kun A. 1992. Local radiolabeling of the 68 kDa neurofilament protein in rat sciatic nerves. Neurosci Lett 144:174-176.
51. Sotelo JR, Verdes JM, Kun A, Benech JC, Sotelo-Silveira JR, Calliari A. 1997. Regulation of neuronal protein synthesis by calcium. In: Sotelo JR, Benech JC, editors. Calcium and cellular metabolism, transport and regulation. New York: Plenum Press. p 125-142.
52. Sotelo-Silveira JR, Calliari A, Cardenas M, Koenig E, Sotelo JR. 2004. Myosin Va and kinesin II motor proteins are concentrated in ribosomal domains (periaxoplasmic ribosomal plaques) of myelinated axons. J Neurobiol 60:187-196.
53. Sotelo-Silveira JR, Calliari A, Kun A, Benech JC, Sanguinetti C, Chalar C, Sotelo JR. 2000. Neurofilament mRNAs are present and translated in the normal and severed sciatic nerve. J Neurosci Res 62:65-74.
54. Sotelo-Silveira JR, Calliari A, Kun A, Koenig E, Sotelo JR. 2006. RNA trafficking in axons. Traffic 7:508-515.
55. Sotelo-Silveira JR, Koenig E. 2000 Localization of beta-actin mRNA in cryptic ribosomal periaxoplasmic plaque domains of myelinated axons. Mol Biol Cell 11:800.
56. Suter M, Butler JE. 1986. The immunochemistry of sandwich ELISA. II. A novel system prevents the denaturation of capture antibodies. Immunol Lett 13:313-316.
57. Tennyson VM. 1965. Electron microscopic study of the developing neuroblast of the dorsal root ganglio of the rabbit embryo. J Comp Neurol 124:267-318.
58. Tennyson VM. 1970. The fine structure of the axon and growth cone of the dorsal root neuroblast of the rabbit embryo. J Cell Biol 44:62-79.
59. Twiss JL, van Minnen J. 2006. New insights into neuronal regeneration: the role of axonal protein synthesis in pathfinding and axonal extension. J Neurotrauma 23:295-308.
60. van Kesteren RE, Carter C, Dissel HM, van Minnen J, Gouwenberg Y, Syed NI, Spencer GE, Smit AB. 2006. Local synthesis of actin-binding protein beta-thymosin regulates neurite outgrowth. J Neurosci 26:152-157.
61. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW. 2005. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 25:331-342.
62. Willis DE, Twiss JL. 2006 The evolving roles of axonally synthesized proteins in regeneration. Curr Opin Neurobiol 16:111-118.
63. 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 translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 25:778-791.
64. 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.
65. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ. 2001. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31:261-275.
66. Zhang HL, Pan F, Hong D, Shenoy SM, Singer RH, Bassell GJ. 2003. Active transport of the survival motor neuron protein and the role of exon-7 in cytoplasmic localization. Neuroscience 23:6627-6637.
67. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL. 2001 A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 21:9291-9303.
68. Zéléna J. 1970. Ribosome-like particles in myelinated axons of the rat. Brain Res 24:359-363.
69. Zéléna J. 1972. Ribosomes in myelinated axons of dorsal root ganglia. Z Zellforsch Mikrosk Anat 124:217-229.