Regulation of axon regeneration by the RNA repair and splicing pathway

Nature Neuroscience

Volumn 18, Issue 6, 2015, Pages 817-825

  Song, Yuanquan ^a   Sretavan, David ^b   Salegio, Ernesto A ^a   Berg, Jim ^a,c   Huang, Xi ^a   Cheng, Tong ^a   Xiong, Xin ^a   Meltzer, Shan ^a   Han, Chun ^a,d   Nguyen, Trong Tuong ^b   Bresnahan, Jacqueline C ^a   Beattie, Michael S ^a   Jan, Lily Yeh ^a   Jan, Yuh Nung ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^d School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHEASE; PROTEIN; RNA LIGASE; RTCA PROTEIN; RTCB PROTEIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; LIGASE; RNA; RNA 3'-TERMINAL PHOSPHATE CYCLASE; XBP1 PROTEIN, DROSOPHILA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CATALYST; CELL STRESS; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; FEMALE; IN VITRO STUDY; MALE; MAMMAL; MOUSE; NERVE CELL; NERVE CRUSH; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; OPTIC NERVE CRUSH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; RETINA GANGLION CELL; RNA METABOLISM; RNA REPAIR; RNA SPLICING; RODENT; SIGNAL TRANSDUCTION; ANIMAL; AXON; CELL CULTURE; NERVE REGENERATION; OPTIC NERVE; PATHOLOGY; PHYSIOLOGY; SCIATIC NERVE;

ANIMALS; AXONS; CELLS, CULTURED; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; LIGASES; MICE; NERVE CRUSH; NERVE REGENERATION; OPTIC NERVE; RETINAL GANGLION CELLS; RNA; RNA SPLICING; SCIATIC NERVE;

EID: 84929947727     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4019     Document Type: Article

References (55)

1. Filbin, M.T. Recapitulate development to promote axonal regeneration: good or bad approach? Phil. Trans. R. Soc. Lond. B 361, 1565-1574 (2006).
2. Fitch, M.T. & Silver, J. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 209, 294-301 (2008).
3. Goldberg, J.L., Klassen, M.P., Hua, Y. & Barres, B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 296, 1860-1864 (2002).
4. Schwab, M.E. & Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370 (1996).
5. Case, L.C. & Tessier-Lavigne, M. Regeneration of the adult central nervous system. Curr. Biol. 15, R749-R753 (2005).
6. Harel, N.Y. & Strittmatter, S.M. Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci. 7, 603-616 (2006).
7. Moore, D.L. et al. KLF family members regulate intrinsic axon regeneration ability. Science 326, 298-301 (2009).
8. Park, K.K. et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322, 963-966 (2008).
9. Smith, P.D. et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 64, 617-623 (2009).
10. Sun, F. & He, Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr. Opin. Neurobiol. 20, 510-518 (2010).
11. Yiu, G. & He, Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617-627 (2006).
12. Chen, L. et al. Axon regeneration pathways identified by systematic genetic screening in C. elegans. Neuron 71, 1043-1057 (2011).
13. Nix, P. et al. Axon regeneration genes identified by RNAi screening in C. elegans. J. Neurosci. 34, 629-645 (2014).
14. Song, Y. et al. Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. Genes Dev. 26, 1612-1625 (2012).
15. Bonilla, I.E., Tanabe, K. & Strittmatter, S.M. Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J. Neurosci. 22, 1303-1315 (2002).
16. Costigan, M. et al. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 3, 16 (2002).
17. Fischer, D., Petkova, V., Thanos, S. & Benowitz, L.I. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 24, 8726-8740 (2004).
18. Nilsson, A., Moller, K., Dahlin, L., Lundborg, G. & Kanje, M. Early changes in gene expression in the dorsal root ganglia after transection of the sciatic nerve; effects of amphiregulin and PAI-1 on regeneration. Brain Res. Mol. Brain Res. 136, 65-74 (2005).
19. Veldman, M.B., Bemben, M.A., Thompson, R.C. & Goldman, D. Gene expression analysis of zebrafish retinal ganglion cells during optic nerve regeneration identifies KLF6a and KLF7a as important regulators of axon regeneration. Dev. Biol. 312, 596-612 (2007).
20. Araki, T. & Milbrandt, J. Ninjurin, a novel adhesion molecule, is induced by nerve injury and promotes axonal growth. Neuron 17, 353-361 (1996).
21. Genschik, P., Billy, E., Swianiewicz, M. & Filipowicz, W. The human RNA 3'-Terminal phosphate cyclase is a member of a new family of proteins conserved in Eucarya, Bacteria and Archaea. EMBO J. 16, 2955-2967 (1997).
22. Liu, K. et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 13, 1075-1081 (2010).
23. Gabel, C.V., Antoine, F., Chuang, C.F., Samuel, A.D. & Chang, C. Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. Development 135, 1129-1136 (2008).
24. Popow, J. et al. HSPC117 is the essential subunit of a human tRNA splicing ligase complex. Science 331, 760-764 (2011).
25. Remus, B.S. & Shuman, S. A kinetic framework for tRNA ligase and enforcement of a 2'-phosphate requirement for ligation highlights the design logic of an RNA repair machine. RNA 19, 659-669 (2013).
26. Englert, M., Sheppard, K., Aslanian, A., Yates, J.R. III & Soll, D. Archaeal 3'-phosphate RNA splicing ligase characterization identifies the missing component in tRNA maturation. Proc. Natl. Acad. Sci. USA 108, 1290-1295 (2011).
27. Tanaka, N. & Shuman, S. RtcB is the RNA ligase component of an Escherichia coli RNA repair operon. J. Biol. Chem. 286, 7727-7731 (2011).
28. Tanaka, N., Meineke, B. & Shuman, S. RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J. Biol. Chem. 286, 30253-30257 (2011).
29. Desai, K.K., Cheng, C.L., Bingman, C.A., Phillips, G.N. Jr. & Raines, R.T. A tRNA splicing operon: Archease endows RtcB with dual GTP/ATP cofactor specificity and accelerates RNA ligation. Nucleic Acids Res. 42, 3931-3942 (2014).
30. Popow, J., Jurkin, J., Schleiffer, A. & Martinez, J. Analysis of orthologous groups reveals archease and DDX1 as tRNA splicing factors. Nature 511, 104-107 (2014).
31. Canaves, J.M. Predicted role for the archease protein family based on structural and sequence analysis of TM1083 and MTH1598, two proteins structurally characterized through structural genomics efforts. Proteins 56, 19-27 (2004).
32. Das, U. & Shuman, S. 2'-Phosphate cyclase activity of RtcA: a potential rationale for the operon organization of RtcA with an RNA repair ligase RtcB in Escherichia coli and other bacterial taxa. RNA 19, 1355-1362 (2013).
33. Tanaka, N., Chakravarty, A.K., Maughan, B. & Shuman, S. Novel mechanism of RNA repair by RtcB via sequential 2', 3'-cyclic phosphodiesterase and 3'-phosphate/5'-hydroxyl ligation reactions. J. Biol. Chem. 286, 43134-43143 (2011).
34. Chakravarty, A.K. & Shuman, S. The sequential 2', 3'-cyclic phosphodiesterase and 3'-phosphate/5'-OH ligation steps of the RtcB RNA splicing pathway are GTP-dependent. Nucleic Acids Res. 40, 8558-8567 (2012).
35. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529 (2007).
36. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. & Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891 (2001).
37. Jurkin, J. et al. The mammalian tRNA ligase complex mediates splicing of XBP1 mRNA and controls antibody secretion in plasma cells. EMBO J. 33, 2922-2936 (2014).
38. Ryoo, H.D., Domingos, P.M., Kang, M.J. & Steller, H. Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J. 26, 242-252 (2007).
39. Ramon y Cajal, S. Degeneration and Regeneration of the Nervous System (Oxford University Press, London, 1928).
40. Liu, X., Hawkes, E., Ishimaru, T., Tran, T. & Sretavan, D.W. EphB3: an endogenous mediator of adult axonal plasticity and regrowth after CNS injury. J. Neurosci. 26, 3087-3101 (2006).
41. Lu, Y., Belin, S. & He, Z. Signaling regulations of neuronal regenerative ability. Curr. Opin. Neurobiol. 27, 135-142 (2014).
42. Hu, Y. et al. Differential effects of unfolded protein response pathways on axon injury-induced death of retinal ganglion cells. Neuron 73, 445-452 (2012).
43. Han, C., Jan, L.Y. & Jan, Y.N. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc. Natl. Acad. Sci. USA 108, 9673-9678 (2011).
44. Grueber, W.B., Jan, L.Y. & Jan, Y.N. Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112, 805-818 (2003).
45. Sepp, K.J., Schulte, J. & Auld, V.J. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev. Biol. 238, 47-63 (2001).
46. Xiang, Y. et al. Light-Avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468, 921-926 (2010).
47. Awasaki, T., Lai, S.L., Ito, K. & Lee, T. Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J. Neurosci. 28, 13742-13753 (2008).
48. Song, W., Onishi, M., Jan, L.Y. & Jan, Y.N. Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proc. Natl. Acad. Sci. USA 104, 5199-5204 (2007).
49. Grueber, W.B. et al. Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development 134, 55-64 (2007).
50. Huang, H. et al. PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126, 5365-5372 (1999).
51. Ritzenthaler, S., Suzuki, E. & Chiba, A. Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat. Neurosci. 3, 1012-1017 (2000).
52. Emoto, K., Parrish, J.Z., Jan, L.Y. & Jan, Y.N. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443, 210-213 (2006).
53. Parrish, J.Z., Emoto, K., Kim, M.D. & Jan, Y.N. Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30, 399-423 (2007).
54. Xiong, X. et al. Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J. Cell Biol. 191, 211-223 (2010).
55. Ultanir, S.K. et al. Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 Uncovers their roles in dendrite arborization and spine development. Neuron 73, 1127-1142 (2012).