Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits

Journal of Cell Biology

Volumn 214, Issue 1, 2016, Pages 103-119

  Zhou, Bing ^a   Yu, Panpan ^b   Lin, Mei Yao ^a   Sun, Tao ^a   Chen, Yanmin ^a   Sheng, Zu Hang ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b JINAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL PROTEIN; NEUROMODULIN; SYNTAPHILIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE; MICROTUBULE ASSOCIATED PROTEIN; SNPH PROTEIN, MOUSE;

ACUTE STRESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXON; BRAIN CELL; CELL MATURATION; CONTROLLED STUDY; EMBRYO; GENETIC MANIPULATION; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; KNOCKOUT MOUSE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NERVE CELL GROWTH; NERVE CRUSH; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SCIATIC NERVE; SCIATIC NERVE INJURY; ANIMAL; AXOTOMY; C57BL MOUSE; CELL DIFFERENTIATION; ENERGY METABOLISM; GROWTH CONE; METABOLISM; MITOCHONDRION; NERVE FIBER TRANSPORT; NERVE REGENERATION; PHYSIOLOGICAL STRESS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; AXONAL TRANSPORT; AXONS; AXOTOMY; CELL DIFFERENTIATION; ENERGY METABOLISM; GAP-43 PROTEIN; GROWTH CONES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; NERVE REGENERATION; SCIATIC NERVE; STRESS, PHYSIOLOGICAL;

EID: 84979966700     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201605101     Document Type: Article

References (65)

1. Abe, N., and V. Cavalli. 2008. Nerve injury signaling. Curr. Opin. Neurobiol. 18:276-283. http ://dx.doi.org/10.1016/j.conb.2008.06.005
2. Abe, N., S.H. Borson, M.J. Gambello, F. Wang, and V. Cavalli. 2010. Mammalian target of rapamycin (mTOR) activation increases axonal growth capacity of injured peripheral nerves. J. Biol. Chem. 285:28034-28043. http ://dx.doi.org/10.1074/jbc.M110.125336
3. Ackermann, P.W., M. Ahmed, and A. Kreicbergs. 2002. Early nerve regeneration after achilles tendon rupture-a prerequisite for healing? A study in the rat. J. Orthop. Res. 20:849-856. http ://dx.doi.org/10.1016/S0736-0266(01)00159-0
4. Afshari, F.T., S. Kappagantula, and J.W. Fawcett. 2009. Extrinsic and intrinsic factors controlling axonal regeneration after spinal cord injury. Expert Rev. Mol. Med. 11:e37. http ://dx.doi.org/10.1017/S1462399409001288
5. Alvarez, S., M. Moldovan, and C. Krarup. 2008. Acute energy restriction triggers Wallerian degeneration in mouse. Exp. Neurol. 212:166-178. http ://dx.doi.org/10.1016/j.expneurol.2008.03.022
6. Avery, M.A., T.M. Rooney, J.D. Pandya, T.M. Wishart, T.H. Gillingwater, J.W. Geddes, P.G. Sullivan, and M.R. Freeman. 2012. WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca2+ buffering. Curr. Biol. 22:596-600. http ://dx.doi.org/10.1016/j.cub.2012.02.043
7. Berg, J., Y.P. Hung, and G. Yellen. 2009. A genetically encoded fluorescent reporter of ATP :ADP ratio. Nat. Methods. 6:161-166. http ://dx.doi.org/10.1038/nmeth.1288
8. Bradke, F., J.W. Fawcett, and M.E. Spira. 2012. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 13:183-193. http ://dx.doi.org/10.1038/nrn3176
9. Cai, Q., H.M. Zakaria, A. Simone, and Z.H. Sheng. 2012. Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr. Biol. 22:545-552. http ://dx.doi.org/10.1016/j.cub.2012.02.005
10. Case, L.C., and M. Tessier-Lavigne. 2005. Regeneration of the adult central nervous system. Curr. Biol. 15:R749-R753. http ://dx.doi.org/10.1016/j.cub.2005.09.008
11. Cavallucci, V., E. Bisicchia, M.T. Cencioni, A. Ferri, L. Latini, A. Nobili, F. Biamonte, F. Nazio, F. Fanelli, S. Moreno, et al. 2014. Acute focal brain damage alters mitochondrial dynamics and autophagy in axotomized neurons. Cell Death Dis. 5:e1545. http ://dx.doi.org/10.1038/cddis.2014.511
12. Chandran, V., G. Coppola, H. Nawabi, T. Omura, R. Versano, E.A. Huebner, A. Zhang, M. Costigan, A. Yekkirala, L. Barrett, et al. 2016. A systemslevel analysis of the peripheral nerve intrinsic axonal growth program. Neuron. 89:956-970. http ://dx.doi.org/10.1016/j.neuron.2016.01.034
13. Chang, D.T., and I.J. Reynolds. 2006. Mitochondrial trafficking and morphology in healthy and injured neurons. Prog. Neurobiol. 80:241-268. http ://dx.doi.org/10.1016/j.pneurobio.2006.09.003
14. Chen, H., and D.C. Chan. 2009. Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18:R169-R176. http ://dx.doi.org/10.1093/hmg/ddp326
15. Chen, Y., and Z.H. Sheng. 2013. Kinesin-1-syntaphilin coupling mediates activity-dependent regulation of axonal mitochondrial transport. J. Cell Biol. 202:351-364. http ://dx.doi.org/10.1083/jcb.201302040
16. Cho, Y., and V. Cavalli. 2014. HDAC signaling in neuronal development and axon regeneration. Curr. Opin. Neurobiol. 27:118-126. http ://dx.doi.org/10.1016/j.conb.2014.03.008
17. Cho, Y., R. Sloutsky, K.M. Naegle, and V. Cavalli. 2013. Injury-induced HDAC5 nuclear export is essential for axon regeneration. Cell. 155:894-908. (published erratum appears in Cell. 2015. 161:691) http ://dx.doi.org/10.1016/j.cell.2013.10.004
18. Coleman, M.P., and M.R. Freeman. 2010. Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci. 33:245-267. http ://dx.doi.org/10.1146/annurev-neuro-060909-153248
19. Conforti, L., A. Tarlton, T.G. Mack, W. Mi, E.A. Buckmaster, D. Wagner, V.H. Perry, and M.P. Coleman. 2000. A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc. Natl. Acad. Sci. USA. 97:11377-11382. http ://dx.doi.org/10.1073/pnas.97.21.11377
20. Courchet, J., T.L. Lewis Jr., S. Lee, V. Courchet, D.Y. Liou, S. Aizawa, and F. Polleux. 2013. Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell. 153:1510-1525. http ://dx.doi.org/10.1016/j.cell.2013.05.021
21. Court, F.A., and M.P. Coleman. 2012. Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci. 35:364-372. http ://dx.doi.org/10.1016/j.tins.2012.04.001
22. Das, S., J. Boczan, C. Gerwin, P.B. Zald, and Z.H. Sheng. 2003. Regional and developmental regulation of syntaphilin expression in the brain: a candidate molecular element of synaptic functional differentiation. Brain Res. Mol. Brain Res. 116:38-49. http ://dx.doi.org/10.1016/S0169-328X(03)00212-2
23. Di Giovanni, J., and Z.H. Sheng. 2015. Regulation of synaptic activity by snapinmediated endolysosomal transport and sorting. EMBO J. 34:2059-2077. http ://dx.doi.org/10.15252/embj.201591125
24. Fang, Y., L. Soares, X. Teng, M. Geary, and N.M. Bonini. 2012. A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr. Biol. 22:590-595. http ://dx.doi.org/10.1016/j.cub.2012.01.065
25. Filbin, M.T. 2006. Recapitulate development to promote axonal regeneration: good or bad approach? Philos. Trans. R. Soc. Lond. B Biol. Sci. 361:1565-1574. http ://dx.doi.org/10.1098/rstb.2006.1885
26. Fitch, M.T., and J. Silver. 2008. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 209:294-301. http ://dx.doi.org/10.1016/j.expneurol.2007.05.014
27. Fu, S.Y., and T. Gordon. 1997. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 14:67-116. http ://dx.doi.org/10.1007/BF02740621
28. Giger, R.J., E.R. Hollis II, and M.H. Tuszynski. 2010. Guidance molecules in axon regeneration. Cold Spring Harb. Perspect. Biol. 2:a001867. http ://dx.doi.org/10.1101/cshperspect.a001867
29. Gilley, J., and M.P. Coleman. 2010. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 8:e1000300. http ://dx.doi.org/10.1371/journal.pbio.1000300
30. Goslin, K., D.J. Schreyer, J.H. Skene, and G. Banker. 1988. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature. 336:672-674. http ://dx.doi.org/10.1038/336672a0
31. Harel, N.Y., and S.M. Strittmatter. 2006. Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci. 7:603-616. http ://dx.doi.org/10.1038/nrn1957
32. Hill, C.E., M.S. Beattie, and J.C. Bresnahan. 2001. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp. Neurol. 171:153-169. http ://dx.doi.org/10.1006/exnr.2001.7734
33. Hoffman, P.N. 2010. A conditioning lesion induces changes in gene expression and axonal transport that enhance regeneration by increasing the intrinsic growth state of axons. Exp. Neurol. 223:11-18. http ://dx.doi.org/10.1016/j.expneurol.2009.09.006
34. Hu, Y., K.K. Park, L. Yang, X. Wei, Q. Yang, K.S. Cho, P. Thielen, A.H. Lee, R. Cartoni, L.H. Glimcher, et al. 2012. Differential effects of unfolded protein response pathways on axon injury-induced death of retinal ganglion cells. Neuron. 73:445-452. http ://dx.doi.org/10.1016/j.neuron.2011.11.026
35. Kang, J.S., J.H. Tian, P.Y. Pan, P. Zald, C. Li, C. Deng, and Z.H. Sheng. 2008. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell. 132:137-148. http ://dx.doi.org/10.1016/j.cell.2007.11.024
36. Koeberle, P.D., and A.K. Ball. 1999. Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp. Neurol. 158:366-381. http ://dx.doi.org/10.1006/exnr.1999.7113
37. Li, Y., and G. Raisman. 1995. Sprouts from cut corticospinal axons persist in the presence of astrocytic scarring in long-term lesions of the adult rat spinal cord. Exp. Neurol. 134:102-111. http ://dx.doi.org/10.1006/exnr.1995.1041
38. Liu, K., A. Tedeschi, K.K. Park, and Z. He. 2011. Neuronal intrinsic mechanisms of axon regeneration. Annu. Rev. Neurosci. 34:131-152. http ://dx.doi.org/10.1146/annurev-neuro-061010-113723
39. Lucius, R., and J. Sievers. 1996. Postnatal retinal ganglion cells in vitro: protection against reactive oxygen species (ROS)-induced axonal degeneration by cocultured astrocytes. Brain Res. 743:56-62. http ://dx.doi.org/10.1016/S0006-8993(96)01029-3
40. MacAskill, A.F., and J.T. Kittler. 2010. Control of mitochondrial transport and localization in neurons. Trends Cell Biol. 20:102-112. http ://dx.doi.org/10.1016/j.tcb.2009.11.002
41. Miller, K.E., and M.P. Sheetz. 2004. Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 117:2791-2804. http ://dx.doi.org/10.1242/jcs.01130
42. Misgeld, T., M. Kerschensteiner, F.M. Bareyre, R.W. Burgess, and J.W. Lichtman. 2007. Imaging axonal transport of mitochondria in vivo. Nat. Methods. 4:559-561. http ://dx.doi.org/10.1038/nmeth1055
43. Morris, R.L., and P.J. Hollenbeck. 1993. The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci. 104:917-927.
44. Nakano, M., H. Imamura, T. Nagai, and H. Noji. 2011. Ca2+ regulation of mitochondrial ATP synthesis visualized at the single cell level. ACS Chem. Biol. 6:709-715. http ://dx.doi.org/10.1021/cb100313n
45. Nicholls, D.G., and S.L. Budd. 2000. Mitochondria and neuronal survival. Physiol. Rev. 80:315-360.
46. O'Donnell, K.C., M.E. Vargas, and A. Sagasti. 2013. WldS and PGC-1a regulate mitochondrial transport and oxidation state after axonal injury. J. Neurosci. 33:14778-14790. http ://dx.doi.org/10.1523/JNE URO SCI.1331-13.2013
47. Park, K.K., K. Liu, Y. Hu, P.D. Smith, C. Wang, B. Cai, B. Xu, L. Connolly, I. Kramvis, M. Sahin, and Z. He. 2008. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science. 322:963-966. http ://dx.doi.org/10.1126/science.1161566
48. Perlson, E., G.B. Jeong, J.L. Ross, R. Dixit, K.E. Wallace, R.G. Kalb, and E.L. Holzbaur. 2009. A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. J. Neurosci. 29:9903-9917. http ://dx.doi.org/10.1523/JNE URO SCI.0813-09.2009
49. Rawson, R.L., L. Yam, R.M. Weimer, E.G. Bend, E. Hartwieg, H.R. Horvitz, S.G. Clark, and E.M. Jorgensen. 2014. Axons degenerate in the absence of mitochondria in C. elegans. Curr. Biol. 24:760-765. http ://dx.doi.org/10.1016/j.cub.2014.02.025
50. Ruthel, G., and P.J. Hollenbeck. 2003. Response of mitochondrial traffic to axon determination and differential branch growth. J. Neurosci. 23:8618-8624.
51. Saxton, W.M., and P.J. Hollenbeck. 2012. The axonal transport of mitochondria. J. Cell Sci. 125:2095-2104. http ://dx.doi.org/10.1242/jcs.053850
52. Schwab, M.E., and D. Bartholdi. 1996. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76:319-370.
53. Sheng, Z.H. 2014. Mitochondrial trafficking and anchoring in neurons: New insight and implications. J. Cell Biol. 204:1087-1098. http ://dx.doi.org/10.1083/jcb.201312123
54. Sheng, Z.H., and Q. Cai. 2012. Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 13:77-93. http ://dx.doi.org/10.1038/nrn3156
55. Spillane, M., A. Ketschek, T.T. Merianda, J.L. Twiss, and G. Gallo. 2013. Mitochondria coordinate sites of axon branching through localized intraaxonal protein synthesis. Cell Reports. 5:1564-1575. http ://dx.doi.org/10.1016/j.celrep.2013.11.022
56. Sun, F., K.K. Park, S. Belin, D. Wang, T. Lu, G. Chen, K. Zhang, C. Yeung, G. Feng, B.A. Yankner, and Z. He. 2011. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature. 480:372-375. http ://dx.doi.org/10.1038/nature10594
57. Sun, T., H. Qiao, P.Y. Pan, Y. Chen, and Z.H. Sheng. 2013. Motile axonal mitochondria contribute to the variability of presynaptic strength. Cell Reports. 4:413-419. http ://dx.doi.org/10.1016/j.celrep.2013.06.040
58. Tantama, M., J.R. Martínez-François, R. Mongeon, and G. Yellen. 2013. Imaging energy status in live cells with a fluorescent biosensor of the intracellular ATP-to-ADP ratio. Nat. Commun. 4:2550. http ://dx.doi.org/10.1038/ncomms3550
59. Tao, K., N. Matsuki, and R. Koyama. 2014. AMP-activated protein kinase mediates activity-dependent axon branching by recruiting mitochondria to axon. Dev. Neurobiol. 74:557-573. http ://dx.doi.org/10.1002/dneu.22149
60. Tessier-Lavigne, M., and C.S. Goodman. 1996. The molecular biology of axon guidance. Science. 274:1123-1133. http ://dx.doi.org/10.1126/science.274.5290.1123
61. Yanik, M.F., H. Cinar, H.N. Cinar, A.D. Chisholm, Y. Jin, and A. Ben-Yakar. 2004. Neurosurgery: functional regeneration after laser axotomy. Nature. 432:822. http ://dx.doi.org/10.1038/432822a
62. Yiu, G., and Z. He. 2006. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7:617-627. http ://dx.doi.org/10.1038/nrn1956
63. Yu, T.W., and C.I. Bargmann. 2001. Dynamic regulation of axon guidance. Nat. Neurosci. 4:1169-1176. http ://dx.doi.org/10.1038/nn748
64. Zhao, Y., S. Araki, J. Wu, T. Teramoto, Y.F. Chang, M. Nakano, A.S. Abdelfattah, M. Fujiwara, T. Ishihara, T. Nagai, and R.E. Campbell. 2011. An expanded palette of genetically encoded Ca2+ indicators. Science. 333:1888-1891. http ://dx.doi.org/10.1126/science.1208592
65. Zhou, B., Q. Cai, Y. Xie, and Z.H. Sheng. 2012. Snapin recruits dynein to BDNFTrkB signaling endosomes for retrograde axonal transport and is essential for dendrite growth of cortical neurons. Cell Reports. 2:42-51. http ://dx.doi.org/10.1016/j.celrep.2012.06.010