Inhibiting poly(ADP-ribosylation) improves axon regeneration

eLife

Volumn 5, Issue OCTOBER2016, 2016, Pages

  Byrne, Alexandra B ^a,d   McWhirter, Rebecca D ^b,c   Sekine, Yuichi ^a   Strittmatter, Stephen M ^a   Miller, David M ^b,c   Hammarlund, Marc ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; GLYCOSIDASE; POLY ADP-RIBOSE GLYCOHYDROLASE;

ARTICLE; AXONAL INJURY; AXOTOMY; CAENORHABDITIS ELEGANS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DOWN REGULATION; FRAMESHIFT MUTATION; NERVE FIBER REGENERATION; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; AXON; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; POLY(ADENOSINE DIPHOSPHATE) RIBOSYLATION; REGENERATION;

ADP RIBOSE TRANSFERASES; ANIMALS; AXONS; CAENORHABDITIS ELEGANS; GLYCOSIDE HYDROLASES; POLY ADP RIBOSYLATION; REGENERATION;

EID: 84990209386     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12734     Document Type: Article

References (39)

1. Althaus FR, Richter C. 1987. ADP-ribosylation of proteins. Enzymology and biological significance. Molecular Biology, Biochemistry, and Biophysics 37:1–237. doi: 10.1002/abio.370090614
2. Anwar M, Aslam HM, Anwar S. 2015. PARP inhibitors. Hereditary Cancer in Clinical Practice 13:4. doi: 10.1186/s13053-014-0024-8
3. Bai P. 2015. Biology of poly(ADP-Ribose) polymerases: The factotums of cell maintenance. Molecular Cell 58: 947–958. doi: 10.1016/j.molcel.2015.01.034
4. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94
5. Brochier C, Jones JI, Willis DE, Langley B. 2015. Poly(ADP-ribose) polymerase 1 is a novel target to promote axonal regeneration. PNAS 112:15220–15225. doi: 10.1073/pnas.1509754112
6. Byrne AB, Edwards TJ, Hammarlund M. 2011. In vivo laser axotomy in C. elegans. Journal of Visualized Experiments 51:e2707. doi: 10.3791/2707
7. Byrne AB, Walradt T, Gardner KE, Hubbert A, Reinke V, Hammarlund M. 2014. Insulin/IGF1 signaling inhibits age-dependent axon regeneration. Neuron 81:561–573. doi: 10.1016/j.neuron.2013.11.019
8. Ford AL, Lee JM. 2011. Climbing STAIRs towards clinical trials with a novel PARP-1 inhibitor for the treatment of ischemic stroke. Brain Research 1410:120–121. doi: 10.1016/j.brainres.2011.07.001
9. Fournier AE, GrandPre T, Strittmatter SM. 2001. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409:341–346. doi: 10.1038/35053072
10. Friedland AE, Tzur YB, Esvelt KM, Colaiácovo MP, Church GM, Calarco JA. 2013. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nature Methods 10:741–743. doi: 10.1038/nmeth.2532
11. Gagnon SN, Hengartner MO, Desnoyers S. 2002. The genes pme-1 and pme-2 encode two poly(ADP-ribose) polymerases in Caenorhabditis elegans. Biochemical Journal 368:263–271. doi: 10.1042/bj20020669
12. Gibson BA, Kraus WL. 2012. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nature Reviews Molecular Cell Biology 13:411–424. doi: 10.1038/nrm3376
13. GrandPré T, Nakamura F, Vartanian T, Strittmatter SM. 2000. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 403:439–444. doi: 10.1038/35000226
14. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M. 2009. Axon regeneration requires a conserved MAP kinase pathway. Science 323:802–806. doi: 10.1126/science.1165527
15. Huebner EA, Kim BG, Duffy PJ, Brown RH, Strittmatter SM. 2011. A multi-domain fragment of Nogo-A protein is a potent inhibitor of cortical axon regeneration via Nogo receptor 1. Journal of Biological Chemistry 286: 18026–18036. doi: 10.1074/jbc.M110.208108
16. Miwa M, Sugimura T. 1971. Splitting of the ribose-ribose linkage of poly(adenosine diphosphate-robose) by a calf thymus extract. The Journal of Biological Chemistry 246:6362–6364
17. Nakata K, Abrams B, Grill B, Goncharov A, Huang X, Chisholm AD, Jin Y. 2005. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120:407–420. doi: 10.1016/j.cell.2004.12.017
18. Neumann S, Woolf CJ. 1999. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23:83–91. doi: 10.1016/S0896-6273(00)80755-2
19. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L, Kramvis I, Sahin M, He Z. 2008. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322:963–966. doi: 10.1126/science.1161566
20. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT. 2002. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895–903. doi: 10.1016/S0896-6273(02)00730-4
21. Richardson PM, McGuinness UM, Aguayo AJ. 1980. Axons from CNS neurons regenerate into PNS grafts. Nature 284:264–265. doi: 10.1038/284264a0
22. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi: 10.1093/bioinformatics/btp616
23. Schreiber V, Dantzer F, Ame JC, de Murcia G. 2006. Poly(ADP-ribose): novel functions for an old molecule. Nature Reviews Molecular Cell Biology 7:517–528. doi: 10.1038/nrm1963
24. Shin JE, Cho Y, Beirowski B, Milbrandt J, Cavalli V, DiAntonio A. 2012. Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 74:1015–1022. doi: 10.1016/j.neuron.2012.04.028
25. Smith PD, Sun F, Park KK, Cai B, Wang C, Kuwako K, Martinez-Carrasco I, Connolly L, He Z. 2009. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 64:617–623. doi: 10.1016/j.neuron.2009.11.021
26. Song J, Keppler BD, Wise RR, Bent AF. 2015. PARP2 is the predominant poly(ADP-Ribose) polymerase in arabidopsis DNA damage and immune responses. PLOS Genetics 11:e1005200. doi: 10.1371/journal.pgen.1005200
27. Spencer WC, McWhirter R, Miller T, Strasbourger P, Thompson O, Hillier LW, Waterston RH, Miller DM. 2014. Isolation of specific neurons from C. elegans larvae for gene expression profiling. PLoS ONE 9:e112102. doi: 10.1371/journal.pone.0112102
28. St-Laurent JF, Gagnon SN, Dequen F, Hardy I, Desnoyers S. 2007. Altered DNA damage response in Caenorhabditis elegans with impaired poly(ADP-ribose) glycohydrolases genes expression. DNA Repair 6:329–343. doi: 10.1016/j.dnarep.2006.10.027
29. Stone MC, Albertson RM, Chen L, Rolls MM. 2014. Dendrite injury triggers DLK-independent regeneration. Cell Reports 6:247–253. doi: 10.1016/j.celrep.2013.12.022
30. Wang X, Duffy P, McGee AW, Hasan O, Gould G, Tu N, Harel NY, Huang Y, Carson RE, Weinzimmer D, Ropchan J, Benowitz LI, Cafferty WB, Strittmatter SM. 2011. Recovery from chronic spinal cord contusion after Nogo receptor intervention. Annals of Neurology 70:805–821. doi: 10.1002/ana.22527
31. Wang X, Kim JH, Bazzi M, Robinson S, Collins CA, Ye B. 2013. Bimodal control of dendritic and axonal growth by the dual leucine zipper kinase pathway. PLoS Biology 11:e1001572. doi: 10.1371/journal.pbio.1001572
32. Watkins TA, Wang B, Huntwork-Rodriguez S, Yang J, Jiang Z, Eastham-Anderson J, Modrusan Z, Kaminker JS, Tessier-Lavigne M, Lewcock JW. 2013. DLK initiates a transcriptional program that couples apoptotic and regenerative responses to axonal injury. PNAS 110:4039–4044. doi: 10.1073/pnas.1211074110
33. Xiong X, Wang X, Ewanek R, Bhat P, Diantonio A, Collins CA. 2010. Protein turnover of the wallenda/DLK kinase regulates a retrograde response to axonal injury. The Journal of Cell Biology 191:211–223. doi: 10.1083/jcb.201006039
34. Yan D, Jin Y. 2012. Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76:534–548. doi: 10.1016/j.neuron.2012.08.043
35. Yan D, Wu Z, Chisholm AD, Jin Y. 2009. The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138:1005–1018. doi: 10.1016/j.cell.2009.06.023
36. Yeh E, Kawano T, Weimer RM, Bessereau JL, Zhen M. 2005. Identification of genes involved in synaptogenesis using a fluorescent active zone marker in Caenorhabditis elegans. Journal of Neuroscience 25:3833–3841. doi: 10.1523/JNEUROSCI.4978-04.2005
37. Yiu G, He Z. 2006. Glial inhibition of CNS axon regeneration. Nature Reviews Neuroscience 7:617–627. doi: 10. 1038/nrn1956
38. Zhen M, Jin Y. 1999. The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371–375. doi: 10.1038/43886
39. Zou Y, Stagi M, Wang X, Yigitkanli K, Siegel CS, Nakatsu F, Cafferty WB, Strittmatter SM. 2015. Gene-silencing screen for mammalian axon regeneration identifies inpp5f (Sac2) as an endogenous suppressor of repair after spinal cord injury. Journal of Neuroscience 35:10429–10439. doi: 10.1523/JNEUROSCI.1718-15.2015