Microtubule-dependent ribosome localization in neurons.

Kentaro Noma, Alexandr Goncharov, Mark H Ellisman, Yishi Jin
Author Information
  1. Kentaro Noma: Division of Biological Sciences, Neurobiology Section, University of California, San Diego, San Diego, United States. ORCID
  2. Alexandr Goncharov: Division of Biological Sciences, Neurobiology Section, University of California, San Diego, San Diego, United States.
  3. Mark H Ellisman: National Center for Research in Biological Systems, Department of Neurosciences, School of Medicine, University of California, San Diego, San Diego, United States.
  4. Yishi Jin: Division of Biological Sciences, Neurobiology Section, University of California, San Diego, San Diego, United States. ORCID

Abstract

Subcellular localization of ribosomes defines the location and capacity for protein synthesis. Methods for in vivo visualizing ribosomes in multicellular organisms are desirable in mechanistic investigations of the cell biology of ribosome dynamics. Here, we developed an approach using split GFP for tissue-specific visualization of ribosomes in . Labeled ribosomes are detected as fluorescent puncta in the axons and synaptic terminals of specific neuron types, correlating with ribosome distribution at the ultrastructural level. We found that axonal ribosomes change localization during neuronal development and after axonal injury. By examining mutants affecting axonal trafficking and performing a forward genetic screen, we showed that the microtubule cytoskeleton and the JIP3 protein UNC-16 exert distinct effects on localization of axonal and somatic ribosomes. Our data demonstrate the utility of tissue-specific visualization of ribosomes , and provide insight into the mechanisms of active regulation of ribosome localization in neurons.

Keywords

References

  1. Front Neural Circuits. 2009 Nov 04;3:17 [PMID: 19915727]
  2. Dev Biol. 1981 Mar;82(2):358-70 [PMID: 7227647]
  3. Nature. 1978 Feb 23;271(5647):764-6 [PMID: 625347]
  4. Annu Rev Cell Dev Biol. 2013;29:271-97 [PMID: 23844582]
  5. Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):3982-7 [PMID: 21368137]
  6. Genetics. 2009 Oct;183(2):607-17, 1SI-4SI [PMID: 19652181]
  7. J Neurosci. 1983 Jan;3(1):177-88 [PMID: 6822854]
  8. Mol Cell Biol. 2005 Jan;25(1):100-13 [PMID: 15601834]
  9. J Neurosci. 2008 Oct 22;28(43):11024-9 [PMID: 18945910]
  10. Cell. 2011 Apr 29;145(3):383-397 [PMID: 21529712]
  11. Nat Genet. 2008 Nov;40(11):1375-83 [PMID: 18953339]
  12. Cell Motil Cytoskeleton. 1993;25(1):1-9 [PMID: 8519063]
  13. Nature. 2003 Oct 16;425(6959):686-91 [PMID: 14562095]
  14. Genetics. 1974 May;77(1):71-94 [PMID: 4366476]
  15. Proc Natl Acad Sci U S A. 2007 Sep 18;104(38):15132-7 [PMID: 17848506]
  16. Genes Dev. 1989 Jun;3(6):870-81 [PMID: 2744465]
  17. Cell. 2009 Mar 20;136(6):1148-60 [PMID: 19268344]
  18. Cell. 1997 Dec 26;91(7):927-38 [PMID: 9428516]
  19. Nature. 2010 Sep 9;467(7312):218-22 [PMID: 20829795]
  20. J Exp Med. 1985 Aug 1;162(2):459-71 [PMID: 2410526]
  21. Microbiol Mol Biol Rev. 2007 Sep;71(3):477-94 [PMID: 17804668]
  22. Mol Cell. 2009 Apr 10;34(1):3-11 [PMID: 19362532]
  23. J Neurosci. 2000 Nov 15;20(22):8390-400 [PMID: 11069946]
  24. J Cell Biol. 1982 Apr;93(1):15-23 [PMID: 7068753]
  25. Neuron. 2002 Oct 24;36(3):507-19 [PMID: 12408852]
  26. Cell. 2014 Oct 23;159(3):635-46 [PMID: 25307933]
  27. Cell. 2009 Sep 4;138(5):1005-18 [PMID: 19737525]
  28. Science. 2015 Apr 10;348(6231):201-7 [PMID: 25859040]
  29. Mol Biol Cell. 2002 May;13(5):1778-91 [PMID: 12006669]
  30. Eur J Cell Biol. 1983 Sep;31(2):334-40 [PMID: 6641742]
  31. Mol Cell Proteomics. 2006 Apr;5(4):635-51 [PMID: 16352523]
  32. Nucleic Acids Res. 2014 Jul;42(Web Server issue):W252-8 [PMID: 24782522]
  33. J Biol Chem. 2013 Jan 25;288(4):2532-45 [PMID: 23195953]
  34. Dev Cell. 2012 Oct 16;23 (4):716-28 [PMID: 23000142]
  35. J Cell Biol. 2003 Mar 17;160(6):817-21 [PMID: 12642609]
  36. Neuron. 2013 Jun 19;78(6):971-85 [PMID: 23791193]
  37. Genetics. 2013 May;194(1):143-61 [PMID: 23633144]
  38. Development. 2005 Jul;132(13):3079-92 [PMID: 15930100]
  39. Curr Biol. 2012 Jun 19;22(12):1057-65 [PMID: 22658602]
  40. Cell Motil Cytoskeleton. 1989;14(3):401-15 [PMID: 2479489]
  41. Bioessays. 2008 Jan;30(1):10-4 [PMID: 18081006]
  42. Brain Res. 1987 Sep 8;420(1):73-81 [PMID: 3676755]
  43. Nature. 1992 Oct 29;359(6398):859-61 [PMID: 1436062]
  44. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6577-82 [PMID: 8692859]
  45. Neuron. 2011 Sep 22;71(6):1043-57 [PMID: 21943602]
  46. Curr Biol. 2009 Aug 25;19(16):1362-7 [PMID: 19615905]
  47. Cell. 2017 Jun 1;169(6):1051-1065.e18 [PMID: 28575669]
  48. Mol Cell. 2005 Aug 19;19(4):437-47 [PMID: 16109369]
  49. J Neurosci. 1997 Oct 15;17(20):7694-702 [PMID: 9315891]
  50. Science. 2011 Dec 16;334(6062):1524-9 [PMID: 22096102]
  51. Cell. 2016 Feb 11;164(4):757-69 [PMID: 26871635]
  52. Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13939-44 [PMID: 19666516]
  53. Science. 2014 Nov 7;346(6210):1257521 [PMID: 25378630]
  54. Mol Biol Cell. 2005 Jul;16(7):3273-88 [PMID: 15843430]
  55. Nat Methods. 2012 Jun 28;9(7):676-82 [PMID: 22743772]
  56. Science. 2014 Jan 24;343(6169):419-22 [PMID: 24458642]
  57. Nat Neurosci. 2006 Oct;9(10):1247-56 [PMID: 16980963]
  58. Biochem Soc Trans. 2006 Nov;34(Pt 5):828-32 [PMID: 17052208]
  59. Cell. 2014 Jun 5;157(6):1262-78 [PMID: 24906146]
  60. Nature. 2015 Jan 1;517(7532):33-8 [PMID: 25409156]
  61. Cell. 2010 May 14;141(4):632-44 [PMID: 20434207]
  62. Neuron. 2001 Nov 8;32(3):489-501 [PMID: 11709159]
  63. Mol Microbiol. 2012 Jul;85(1):21-38 [PMID: 22624875]
  64. J Cell Sci. 1998 Nov;111 ( Pt 21):3157-66 [PMID: 9763510]
  65. J Cell Biol. 2002 Jan 21;156(2):337-48 [PMID: 11807096]
  66. Biochem Biophys Res Commun. 2000 Oct 22;277(2):476-86 [PMID: 11032747]
  67. J Neurosci. 2001 Dec 1;21(23):9291-303 [PMID: 11717363]
  68. Nat Commun. 2016 Mar 18;7:11046 [PMID: 26988139]
  69. J Cell Sci. 1999 Feb;112 ( Pt 3):395-403 [PMID: 9885292]
  70. J Neurosci. 1996 Feb 15;16(4):1400-11 [PMID: 8778291]
  71. J Neurosci. 1982 Mar;2(3):284-91 [PMID: 7062109]
  72. Results Probl Cell Differ. 2009;48:173-91 [PMID: 19137268]
  73. Neuron. 2001 Dec 6;32(5):787-800 [PMID: 11738026]
  74. Nat Neurosci. 2006 Oct;9(10):1265-73 [PMID: 16980965]
  75. Proc Natl Acad Sci U S A. 1981 May;78(5):2737-41 [PMID: 6789322]
  76. Nature. 2011 Nov 23;480(7375):63-8 [PMID: 22113615]
  77. Nat Rev Mol Cell Biol. 2001 Jun;2(6):444-56 [PMID: 11389468]
  78. J Biophys Biochem Cytol. 1955 Jan;1(1):59-68 [PMID: 14381428]
  79. J Cell Sci. 2010 Jul 1;123(Pt 13):2228-37 [PMID: 20530576]
  80. J Cell Biol. 2008 Nov 17;183(4):635-40 [PMID: 19001126]
  81. Nat Biotechnol. 2005 Jan;23(1):102-7 [PMID: 15580262]
  82. Cell. 2008 Nov 14;135(4):738-48 [PMID: 19013281]
  83. Science. 2000 Nov 17;290(5495):1364-8 [PMID: 11082065]

Grants

  1. P41 GM103412/NIGMS NIH HHS
  2. R37 NS035546/NINDS NIH HHS
  3. /Howard Hughes Medical Institute

MeSH Term

Adaptor Proteins, Signal Transducing
Animals
Biological Transport
Caenorhabditis elegans
Caenorhabditis elegans Proteins
Green Fluorescent Proteins
Microtubules
Neurons
Ribosomes
Staining and Labeling

Chemicals

Adaptor Proteins, Signal Transducing
Caenorhabditis elegans Proteins
unc-16 protein, C elegans
Green Fluorescent Proteins

Word Cloud

Created with Highcharts 10.0.0ribosomeslocalizationribosomeaxonalproteintissue-specificvisualizationdevelopmentinjuryneuronsSubcellulardefineslocationcapacitysynthesisMethodsvivovisualizingmulticellularorganismsdesirablemechanisticinvestigationscellbiologydynamicsdevelopedapproachusingsplitGFPLabeleddetectedfluorescentpunctaaxonssynapticterminalsspecificneurontypescorrelatingdistributionultrastructurallevelfoundchangeneuronalexaminingmutantsaffectingtraffickingperformingforwardgeneticscreenshowedmicrotubulecytoskeletonJIP3UNC-16exertdistincteffectssomaticdatademonstrateutilityprovideinsightmechanismsactiveregulationMicrotubule-dependentCelegansMEC-15/F-boxUNC-16/JIP3axonneurosciencesynapse

Similar Articles

Cited By