Impact of genetic reduction of NMNAT2 on chemotherapy-induced losses in cell viability in vitro and peripheral neuropathy in vivo

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Slivicki, Richard A ^a   Ali, Yousuf O ^a,b,c   Lu, Hui Chen ^a,b,c   Hohmann, Andrea G ^a  

^a INDIANA UNIVERSITY   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; ISOPROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROFILAMENT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; PACLITAXEL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; VINCRISTINE; ANTINEOPLASTIC AGENT; NICOTINAMIDE MONONUCLEOTIDE ADENYLYLTRANSFERASE 3, MOUSE; NMNAT1 PROTEIN, MOUSE;

ADULT; ADULTHOOD; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIRTH; BRAIN CELL CULTURE; CANCER CHEMOTHERAPY; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; DEATH; DRUG HYPERSENSITIVITY; DRUG INDUCED DISEASE; DRUG RESPONSE; DRUG SENSITIVITY; EMBRYO; ENZYME ACTIVITY; FEMALE; GENE FUNCTION; GENE KNOCKDOWN; GENOTYPE; HETEROZYGOTE; IN VITRO STUDY; IN VIVO STUDY; LOCOMOTION; MALE; MOUSE; NERVE CELL DEGENERATION; NMNAT2 GENE; NOCICEPTION; NONHUMAN; NULL ALLELE; PERIPHERAL NEUROPATHY; ROTAROD TEST; SPINAL GANGLION; SURVIVAL; WILD TYPE; ANIMAL; CELL SURVIVAL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; PREGNANCY;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL SURVIVAL; FEMALE; MICE; MICE, MUTANT STRAINS; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; PACLITAXEL; PERIPHERAL NERVOUS SYSTEM DISEASES; PREGNANCY; VINCRISTINE;

EID: 85013788593     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147620     Document Type: Article

References (35)

1. Ali YO, Li-Kroeger D, Bellen HJ, Zhai RG, Lu HC (2013) NMNATs, evolutionarily conserved neuronal maintenance factors. Trends Neurosci 36: 632-640. doi: 10.1016/j.tins.2013.07.002 PMID: 23968695
2. Berger F, Lau C, Dahlmann M, Ziegler M (2005) Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem 280: 36334-36341. PMID: 16118205
3. Meyer zu Horste G, Miesbach TA, Muller JI, Fledrich R, Stassart RM, et al. (2011) The Wlds transgene reduces axon loss in a Charcot-Marie-Tooth disease 1A rat model and nicotinamide delays post-traumatic axonal degeneration. Neurobiol Dis 42: 1-8. doi: 10.1016/j.nbd.2010.12.006 PMID: 21168501
4. Gilley J, Coleman MP (2010) Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 8: e1000300. doi: 10.1371/journal.pbio.1000300 PMID: 20126265
5. Yan T, Feng Y, Zheng J, Ge X, Zhang Y, et al. (2010) Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem Int 56: 101-106. doi: 10.1016/j. neuint.2009.09.007 PMID: 19778564
6. Gilley J, Adalbert R, Yu G, Coleman MP (2013) Rescue of peripheral and CNS axon defects in mice lacking NMNAT2. J Neurosci 33: 13410-13424. doi: 10.1523/JNEUROSCI.1534-13.2013 PMID: 23946398
7. Fang Y, Soares L, Teng X, Geary M, Bonini NM (2012) A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr Biol 22: 590-595. doi: 10.1016/j.cub. 2012.01.065 PMID: 22425156
8. Mayer PR, Huang N, Dewey CM, Dries DR, Zhang H, et al. (2010) Expression, localization, and biochemical characterization of nicotinamide mononucleotide adenylyltransferase 2. J Biol Chem 285: 40387-40396. doi: 10.1074/jbc.M110.178913 PMID: 20943658
9. Moulin D, Boulanger A, Clark AJ, Clarke H, Dao T, et al. (2014) Pharmacological management of chronic neuropathic pain: Revised consensus statement from the Canadian Pain Society. Pain Res Manag 19: 328-335. PMID: 25479151
10. Topp KS, Tanner KD, Levine JD (2000) Damage to the cytoskeleton of large diameter sensory neurons and myelinated axons in vincristine-induced painful peripheral neuropathy in the rat. J Comp Neurol 424: 563-576. PMID: 10931481
11. Tanner KD, Levine JD, Topp KS (1998) Microtubule disorientation and axonal swelling in unmyelinated sensory axons during vincristine-induced painful neuropathy in rat. J Comp Neurol 395: 481-492. PMID: 9619501
12. Rahn EJ, Makriyannis A, Hohmann AG (2007) Activation of cannabinoid CB1 and CB2 receptors suppresses neuropathic nociception evoked by the chemotherapeutic agent vincristine in rats. Br J Pharmacol 152: 765-777. PMID: 17572696
13. Carozzi VA, Canta A, Chiorazzi A, Cavaletti G (2014) Chemotherapy-induced peripheral neuropathy: What do we know about mechanisms? Neurosci Lett.
14. Crowe MS, Leishman E, Banks ML, Gujjar R, Mahadevan A, et al. (2014) Dual inhibition of monoacylglycerol lipase and cyclooxygenases synergistically reduces neuropathic pain in mice. Br J Pharmacol.
15. Deng L, Guindon J, Vemuri VK, Thakur GA, White FA, et al. (2012) The maintenance of cisplatin- and paclitaxel-induced mechanical and cold allodynia is suppressed by cannabinoid CB(2) receptor activation and independent of CXCR4 signaling in models of chemotherapy-induced peripheral neuropathy. Mol Pain 8: 71. doi: 10.1186/1744-8069-8-71 PMID: 22998838
16. Deng L, Guindon J, Cornett BL, Makriyannis A, Mackie K, et al. (2015) Chronic cannabinoid receptor 2 activation reverses paclitaxel neuropathy without tolerance or cannabinoid receptor 1-dependent withdrawal. Biol Psychiatry 77: 475-487. doi: 10.1016/j.biopsych.2014.04.009 PMID: 24853387
17. Hicks AN, Lorenzetti D, Gilley J, Lu B, Andersson KE, et al. (2012) Nicotinamide mononucleotide adenylyltransferase 2 (Nmnat2) regulates axon integrity in the mouse embryo. PLoS One 7: e47869. doi: 10.1371/journal.pone.0047869 PMID: 23082226
18. Bellamy WT (1992) Prediction of response to drug therapy of cancer. A review of in vitro assays. Drugs 44: 690-708. PMID: 1280562
19. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110. PMID: 6877845
20. Rahn EJ, Thakur GA, Wood JA, Zvonok AM, Makriyannis A, et al. (2011) Pharmacological characterization of AM1710, a putative cannabinoid CB2 agonist from the cannabilactone class: antinociception without central nervous system side-effects. Pharmacol Biochem Behav 98: 493-502. doi: 10.1016/j. pbb.2011.02.024 PMID: 21382397
21. Bourke JL, Coleman HA, Pham V, Forsythe JS, Parkington HC (2014) Neuronal electrophysiological function and control of neurite outgrowth on electrospun polymer nanofibers are cell type dependent. Tissue Eng Part A 20: 1089-1095. doi: 10.1089/ten.TEA.2013.0295 PMID: 24147808
22. Scuteri A, Nicolini G, Miloso M, Bossi M, Cavaletti G, et al. (2006) Paclitaxel toxicity in post-mitotic dorsal root ganglion (DRG) cells. Anticancer Res 26: 1065-1070. PMID: 16619507
23. Cashman CR, Hoke A (2015) Mechanisms of distal axonal degeneration in peripheral neuropathies. Neurosci Lett.
24. Brunden KR, Trojanowski JQ, Smith AB, Lee VMY, Ballatore C (2014) Microtubule-stabilizing agents as potential therapeutics for neurodegenerative disease. Bioorganic & Medicinal Chemistry 22: 5040-5049.
25. Milde S, Gilley J, Coleman MP (2013) Axonal trafficking of NMNAT2 and its roles in axon growth and survival in vivo. Bioarchitecture 3: 133-140. doi: 10.4161/bioa.27049 PMID: 24284888
26. Schiff PB, Horwitz SB (1980) Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci U S A 77: 1561-1565. PMID: 6103535
27. Xiao WH, Bennett GJ (2008) Chemotherapy-evoked neuropathic pain: Abnormal spontaneous discharge in A-fiber and C-fiber primary afferent neurons and its suppression by acetyl-L-carnitine. Pain 135: 262-270. PMID: 17659836
28. Conforti L, Fang G, Beirowski B, Wang MS, Sorci L, et al. (2007) NAD(+) and axon degeneration revisited: Nmnat1 cannot substitute for Wld(S) to delay Wallerian degeneration. Cell Death Differ 14: 116-127. PMID: 16645633
29. Watanabe M, Tsukiyama T, Hatakeyama S (2007) Protection of vincristine-induced neuropathy by WldS expression and the independence of the activity of Nmnat1. Neurosci Lett 411: 228-232. PMID: 17113230
30. Sahenk Z, Barohn R, New P, Mendell JR (1994) Taxol neuropathy. Electrodiagnostic and sural nerve biopsy findings. Arch Neurol 51: 726-729. PMID: 7912506
31. Avery MA, Rooney TM, Pandya JD, Wishart TM, Gillingwater TH, et al. (2012) WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca2+ buffering. Curr Biol 22: 596-600. doi: 10.1016/j.cub.2012.02.043 PMID: 22425157
32. Ljungberg MC, Ali YO, Zhu J, Wu CS, Oka K, et al. (2012) CREB-activity and nmnat2 transcription are down-regulated prior to neurodegeneration, while NMNAT2 over-expression is neuroprotective, in a mouse model of human tauopathy. Hum Mol Genet 21: 251-267. doi: 10.1093/hmg/ddr492 PMID: 22027994
33. Spradley JM, Guindon J, Hohmann AG (2010) Inhibitors of monoacylglycerol lipase, fatty-acid amide hydrolase and endocannabinoid transport differentially suppress capsaicin-induced behavioral sensitization through peripheral endocannabinoid mechanisms. Pharmacol Res 62: 249-258. doi: 10.1016/j. phrs.2010.03.007 PMID: 20416378
34. Gilchrist HD, Allard BL, Simone DA (1996) Enhanced withdrawal responses to heat and mechanical stimuli following intraplantar injection of capsaicin in rats. Pain 67: 179-188. PMID: 8895246
35. Chiang H, Ohno N, Hsieh YL, Mahad DJ, Kikuchi S, et al. (2015) Mitochondrial fission augments capsaicin- induced axonal degeneration. Acta Neuropathol 129: 81-96. doi: 10.1007/s00401-014-1354-3 PMID: 25322817