Poly(ADP-ribose) polymerase 1 is a novel target to promote axonal regeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 49, 2015, Pages 15220-15225

  Brochier, Camille ^a,b   Jones, James I ^a   Willis, Dianna E ^a,b   Langley, Brett ^a,b  

^a BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Axon; PAR; PARP1; Poly(ADP ribose) polymerase; Regeneration

Indexed keywords

GENOMIC DNA; GLYCOPROTEIN; HISTONE H2AX; MYELIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PROTEIN NOGO A; RHO KINASE; RHO KINASE INHIBITOR; ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; AXONAL INJURY; BRAIN CELL; BRAIN CELL CULTURE; CELL BODY; CELL SHAPE; CHO CELL LINE; CONTROL; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SYNTHESIS; FEMALE; GENE DELETION; GROWTH INHIBITION; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MICROENVIRONMENT; MOUSE; NERVE CELL NECROSIS; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; AXON; DRUG EFFECTS; HUMAN; METABOLISM;

AXONS; ENZYME INHIBITORS; HUMANS; NERVE REGENERATION; POLY (ADP-RIBOSE) POLYMERASE-1; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84949267031     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509754112     Document Type: Article

References (57)

1. Anderson DK, Hall ED (1993) Pathophysiology of spinal cord trauma. Ann Emerg Med 22(6):987-992.
2. Stam FJ, et al. (2007) Identification of candidate transcriptional modulators involved in successful regeneration after nerve injury. Eur J Neurosci 25(12):3629-3637.
3. Park KK, Liu K, Hu Y, Kanter JL, He Z (2010) PTEN/mTOR and axon regeneration. Exp Neurol 223(1):45-50.
4. Hannila SS, Filbin MT (2008) The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209(2):321-332.
5. McKerracher L, et al. (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13(4):805-811.
6. Domeniconi M, et al. (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35(2):283-290.
7. Wang KC, et al. (2002) Oligodendrocyte-myelin glycoprotein is a Nogo receptor li-gand that inhibits neurite outgrowth. Nature 417(6892):941-944.
8. Atwal JK, et al. (2008) PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322(5903):967-970.
9. Shen Y, et al. (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326(5952):592-596.
10. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420(6911):74-78.
11. Fisher D, et al. (2011) Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 31(40):14051-14066.
12. Dickendesher TL, et al. (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15(5):703-712.
13. Sandvig A, Berry M, Barrett LB, Butt A, Logan A (2004) Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 46(3):225-251.
14. Prinjha R, et al. (2000) Inhibitor of neurite outgrowth in humans. Nature 403(6768): 383-384.
15. Mimura F, et al. (2006) Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J Biol Chem 281(23):15970-15979.
16. Bradbury EJ, et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416(6881):636-640.
17. Lee JK, et al. (2009) Reassessment of corticospinal tract regeneration in Nogo-deficient mice. J Neurosci 29(27):8649-8654.
18. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): Novel functions for an old molecule. Nat Rev Mol Cell Biol 7(7):517-528.
19. Wang M, et al. (2006) PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 34(21):6170-6182.
20. Wang Y, Dawson VL, Dawson TM (2009) Poly(ADP-ribose) signals to mitochondrial AIF: A key event in parthanatos. Exp Neurol 218(2):193-202.
21. Jagtap P, Szabó C (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 4(5):421-440.
22. Sasaki Y, Vohra BP, Lund FE, Milbrandt J (2009) Nicotinamide mononucleotide ad-enylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J Neurosci 29(17): 5525-5535.
23. Chada SR, Hollenbeck PJ (2003) Mitochondrial movement and positioning in axons: The role of growth factor signaling. J Exp Biol 206(Pt 12):1985-1992.
24. Rivieccio MA, et al. (2009) HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci USA 106(46):19599-19604.
25. Tang S, et al. (1997) Soluble myelin-associated glycoprotein (MAG) found in vivo inhibits axonal regeneration. Mol Cell Neurosci 9(5-6):333-346.
26. Sun X, Zhou Z, Fink DJ, Mata M (2013) HspB1 silences translation of PDZ-RhoGEF by enhancing miR-20a and miR-128 expression to promote neurite extension. Mol Cell Neurosci 57:111-119.
27. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7(8): 617-627.
28. Monnier PP, Sierra A, Schwab JM, Henke-Fahle S, Mueller BK (2003) The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 22(3):319-330.
29. Sharma K, Selzer ME, Li S (2012) Scar-mediated inhibition and CSPG receptors in the CNS. Exp Neurol 237(2):370-378.
30. Brochier C, Langley B (2013) Chromatin modifications associated with DNA double-strand breaks repair as potential targets for neurological diseases. Neurotherapeutics 10(4):817-830.
31. Brochier C, et al. (2013) Specific acetylation of p53 by HDAC inhibition prevents DNA damage-induced apoptosis in neurons. J Neurosci 33(20):8621-8632.
32. Lingor P, et al. (2007) Inhibition of Rho kinase (ROCK) increases neurite outgrowth on chondroitin sulphate proteoglycan in vitro and axonal regeneration in the adult optic nerve in vivo. J Neurochem 103(1):181-189.
33. Messner S, et al. (2010) PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res 38(19):6350-6362.
34. Taylor AM, et al. (2005) A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2(8):599-605.
35. Kurimoto T, et al. (2010) Long-distance axon regeneration in the mature optic nerve: Contributions of oncomodulin, cAMP, and pten gene deletion. J Neurosci 30(46): 15654-15663.
36. Cafferty WB, Duffy P, Huebner E, Strittmatter SM (2010) MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J Neurosci 30(20):6825-6837.
37. Wang Y, et al. (2011) Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 4(167): ra20.
38. Andrabi SA, et al. (2014) Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis. Proc Natl Acad Sci USA 111(28):10209-10214.
39. Fouquerel E, et al. (2014) ARTD1/PARP1 negatively regulates glycolysis by inhibiting hexokinase 1 independent of NAD+ depletion. Cell Reports 8(6):1819-1831.
40. Robey RB, Hay N (2006) Mitochondrial hexokinases, novel mediators of the anti-apoptotic effects of growth factors and Akt. Oncogene 25(34):4683-4696.
41. David KK, Andrabi SA, Dawson TM, Dawson VL (2009) Parthanatos, a messenger of death. Front Biosci (Landmark Ed) 14:1116-1128.
42. Cheng A, Hou Y, Mattson MP (2010) Mitochondria and neuroplasticity. ASN Neuro 2(5):e00045.
43. Lathrop KL, Steketee MB (2013) Mitochondrial dynamics in retinal ganglion cell axon regeneration and growth cone guidance. J Ocular Biol 1(2):9.
44. Estrada-Bernal A, et al. (2012) Functional complexity of the axonal growth cone: A proteomic analysis. PLoS One 7(2):e31858.
45. Wang Z, Gardiner NJ, Fernyhough P (2008) Blockade of hexokinase activity and binding to mitochondria inhibits neurite outgrowth in cultured adult rat sensory neurons. Neurosci Lett 434(1):6-11.
46. Berger NA (1985) Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res 101(1):4-15.
47. Ruggieri S, Orsomando G, Sorci L, Raffaelli N (2015) Regulation of NAD biosynthetic enzymes modulates NAD-sensing processes to shape mammalian cell physiology under varying biological cues. Biochim Biophys Acta 1854(9):1138-1149.
48. Langley B, Sauve A (2013) Sirtuin deacetylases as therapeutic targets in the nervous system. Neurotherapeutics 10(4):605-620.
49. Liu CM, et al. (2013) MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev 27(13):1473-1483.
50. Guo W, et al. (2011) Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling. J Neurosci Res 89(11): 1723-1736.
51. Sugino T, et al. (2010) Protein deacetylase SIRT1 in the cytoplasm promotes nerve growth factor-induced neurite outgrowth in PC12 cells. FEBS Lett 584(13):2821-2826.
52. Araki T, Sasaki Y, Milbrandt J (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305(5686):1010-1013.
53. Harkcom WT, et al. (2014) NAD+ and SIRT3 control microtubule dynamics and reduce susceptibility to antimicrotubule agents. Proc Natl Acad Sci USA 111(24):E2443-E2452.
54. Yahata N, Yuasa S, Araki T (2009) Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J Neurosci 29(19): 6276-6284.
55. Yan T, et al. (2010) Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem Int 56(1):101-106.
56. Tangutoori S, Baldwin P, Sridhar S (2015) PARP inhibitors: A new era of targeted therapy. Maturitas 81(1):5-9.
57. Willis DE, et al. (2007) Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 178(6):965-980.