Olesoxime protects embryonic cortical neurons from camptothecin intoxication by a mechanism distinct from BDNF

British Journal of Pharmacology

Volumn 168, Issue 8, 2013, Pages 1975-1988

  Gouarné, Caroline ^a   Giraudon Paoli, Marc ^a   Seimandi, Mathieu ^a,b   Biscarrat, Clotilde ^a,c   Tardif, Gwenaëlle ^a   Pruss, Rebecca M ^a   Bordet, Thierry ^a  

^a Trophos   (France)

^b Neuroservice   (France)

^c ICDD ^*  (France)

Author keywords

apoptosis; BDNF; camptothecin; MAPK ERK; mitochondria; neurodegenerative diseases; neurotrophic factors; olesoxime; PI3K Akt; TRO19622

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CAMPTOTHECIN; CASPASE; CYTOCHROME C; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OLESOXIME; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53; 1,3 BUTADIENE DERIVATIVE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CHOLEST 4 EN 3 ONE; NITRILE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; CELL CULTURE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; EMBRYO; ENZYME ACTIVATION; FEMALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; BRAIN CORTEX; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; METABOLISM; MITOCHONDRION; NERVE CELL; PHYSIOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BUTADIENES; CAMPTOTHECIN; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CHOLESTENONES; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION; MAP KINASE SIGNALING SYSTEM; MITOCHONDRIA; NEURONS; NITRILES; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84875433073     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12094     Document Type: Article

References (66)

1. Allsopp TE, Wyatt S, Paterson HF, Davies AM, (1993). The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell 73: 295-307.
2. Allsopp TE, Kiselev S, Wyatt S, Davies AM, (1995). Role of Bcl-2 in the brain-derived neurotrophic factor survival response. Eur J Neurosci 7: 1266-1272.
3. Almeida RD, Manadas BJ, Melo CV, Gomes JR, Mendes CS, Graos MM, et al. (2005). Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 12: 1329-1343.
4. Apfel SC, (2001). Neurotrophic factor therapy-prospects and problems. Clin Chem Lab Med 39: 351-355.
5. Arbel N, Shoshan-Barmatz V, (2010). Voltage-dependent anion channel 1-based peptides interact with Bcl-2 to prevent antiapoptotic activity. J Biol Chem 285: 6053-6062.
6. Bazan-Peregrino M, Seymour LW, Harris AL, (2007). Gene therapy targeting to tumor endothelium. Cancer Gene Ther 14: 117-127.
7. Bordet T, Lesbordes JC, Rouhani S, Castelnau-Ptakhine L, Schmalbruch H, Haase G, et al. (2001). Protective effects of cardiotrophin-1 adenoviral gene transfer on neuromuscular degeneration in transgenic ALS mice. Hum Mol Genet 10: 1925-1933.
8. Bordet T, Buisson B, Michaud M, Drouot C, Galea P, Delaage P, et al. (2007). Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J Pharmacol Exp Ther 322: 709-720.
9. Bordet T, Buisson B, Michaud M, Abitbol JL, Marchand F, Grist J, et al. (2008). Specific antinociceptive activity of cholest-4-en-3-one, oxime (TRO19622) in experimental models of painful diabetic and chemotherapy-induced neuropathy. J Pharmacol Exp Ther 326: 623-632.
10. Bordet T, Berna P, Abitbol JL, Pruss RM, (2010). Olesoxime (TRO19622): a novel mitochondrial-targeted neuroprotective compound. Pharmaceuticals 3: 345-368.
11. Caleo M, Medini P, von, Bartheld CS, Maffei L, (2003). Provision of brain-derived neurotrophic factor via anterograde transport from the eye preserves the physiological responses of axotomized geniculate neurons. J Neurosci 23: 287-296.
12. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ, (2003). VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513-517.
13. Cheung EC, Melanson-Drapeau L, Cregan SP, Vanderluit JL, Ferguson KL, McIntosh WC, et al. (2005). Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. J Neurosci 25: 1324-1334.
14. Connor B, Young D, Lawlor P, Gai W, Waldvogel H, Faull RL, et al. (1996). Trk receptor alterations in Alzheimer's disease. Brain Res Mol Brain Res 42: 1-17.
15. Cregan SP, Fortin A, MacLaurin JG, Callaghan SM, Cecconi F, Yu SW, et al. (2002). Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 158: 507-517.
16. Friedman WJ, Ibanez CF, Hallbook F, Persson H, Cain LD, Dreyfus CF, et al. (1993). Differential actions of neurotrophins in the locus coeruleus and basal forebrain. Exp Neurol 119: 72-78.
17. Gatliff J, Campanella M, (2012). The 18Kda translocator protein (TSPO): a new perspective in mitochondrial biology. Curr Mol Med 12: 356-358.
18. Ghahremani MH, Keramaris E, Shree T, Xia Z, Davis RJ, Flavell R, et al. (2002). Interaction of the c-Jun/JNK pathway and cyclin-dependent kinases in death of embryonic cortical neurons evoked by DNA damage. J Biol Chem 277: 35586-35596.
19. Gonzalez-Aparicio R, Flores JA, Fernandez-Espejo E, (2010). Anti-Parkinsonian trophic action of glial cell line-derived neurotrophic factor and transforming growth factor beta1 is enhanced after co-infusion in rats. Exp Neurol 226: 136-147.
20. Haase G, Kennel P, Pettmann B, Vigne E, Akli S, Revah F, et al. (1997). Gene therapy of murine motor neuron disease using adenoviral vectors for neurotrophic factors. Nat Med 3: 429-436.
21. Han BH, Holtzman DM, (2000). BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J Neurosci 20: 5775-5781.
22. Henderson CE, Camu W, Mettling C, Gouin A, Poulsen K, Karihaloo M, et al. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363: 266-270.
23. Hetman M, Kanning K, Cavanaugh JE, Xia Z, (1999). Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. J Biol Chem 274: 22569-22580.
24. Keramaris E, Stefanis L, MacLaurin J, Harada N, Takaku K, Ishikawa T, et al. (2000). Involvement of caspase 3 in apoptotic death of cortical neurons evoked by DNA damage. Mol Cell Neurosci 15: 368-379.
25. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
26. Kubo T, Nonomura T, Enokido Y, Hatanaka H, (1995). Brain-derived neurotrophic factor (BDNF) can prevent apoptosis of rat cerebellar granule neurons in culture. Brain Res Dev Brain Res 85: 249-258.
27. Lang AE, Gill S, Patel NK, Lozano A, Nutt JG, Penn R, et al. (2006). Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann Neurol 59: 459-466.
28. Lang-Rollin IC, Rideout HJ, Noticewala M, Stefanis L, (2003). Mechanisms of caspase-independent neuronal death: energy depletion and free radical generation. J Neurosci 23: 11015-11025.
29. Lim JY, Park SI, Oh JH, Kim SM, Jeong CH, Jun JA, et al. (2008). Brain-derived neurotrophic factor stimulates the neural differentiation of human umbilical cord blood-derived mesenchymal stem cells and survival of differentiated cells through MAPK/ERK and PI3K/Akt-dependent signaling pathways. J Neurosci Res 86: 2168-2178.
30. Madeddu F, Naska S, Bozzi Y, (2004). BDNF down-regulates the caspase 3 pathway in injured geniculo-cortical neurones. Neuroreport 15: 2045-2049.
31. Markham A, Cameron I, Bains R, Franklin P, Kiss JP, Schwendimann L, et al. (2012). Brain-derived neurotrophic factor-mediated effects on mitochondrial respiratory coupling and neuroprotection share the same molecular signalling pathways. Eur J Neurosci 35: 366-374.
32. Martin LJ, Adams NA, Pan Y, Price A, Wong M, (2011). The mitochondrial permeability transition pore regulates nitric oxide-mediated apoptosis of neurons induced by target deprivation. J Neurosci 31: 359-370.
33. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
34. Miller RG, Bryan WW, Dietz MA, Munsat TL, Petajan JH, Smith SA, et al. (1996). Toxicity and tolerability of recombinant human ciliary neurotrophic factor in patients with amyotrophic lateral sclerosis. Neurology 47: 1329-1331.
35. Molina-Holgado F, Doherty P, Williams G, (2008). Tandem repeat peptide strategy for the design of neurotrophic factor mimetics. CNS Neurol Disord Drug Targets 7: 110-119.
36. Morris EJ, Geller HM, (1996). Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. J Cell Biol 134: 757-770.
37. Morris EJ, Keramaris E, Rideout HJ, Slack RS, Dyson NJ, Stefanis L, et al. (2001). Cyclin-dependent kinases and P53 pathways are activated independently and mediate Bax activation in neurons after DNA damage. J Neurosci 21: 5017-5026.
38. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, Shaked GM, et al. (2009). Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med 15: 331-337.
39. Oppenheim RW, Yin QW, Prevette D, Yan Q, (1992). Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360: 755-757.
40. Park DS, Morris EJ, Greene LA, Geller HM, (1997). G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J Neurosci 17: 1256-1270.
41. Park DS, Morris EJ, Padmanabhan J, Shelanski ML, Geller HM, Greene LA, (1998). Cyclin-dependent kinases participate in death of neurons evoked by DNA-damaging agents. J Cell Biol 143: 457-467.
42. Perez-Navarro E, Gavalda N, Gratacos E, Alberch J, (2005). Brain-derived neurotrophic factor prevents changes in Bcl-2 family members and caspase-3 activation induced by excitotoxicity in the striatum. J Neurochem 92: 678-691.
43. Pollack SJ, Harper SJ, (2002). Small molecule Trk receptor agonists and other neurotrophic factor mimetics. Curr Drug Targets CNS Neurol Disord 1: 59-80.
44. Price RD, Milne SA, Sharkey J, Matsuoka N, (2007). Advances in small molecules promoting neurotrophic function. Pharmacol Ther 115: 292-306.
45. Rovini A, Carre M, Bordet T, Pruss RM, Braguer D, (2010). Olesoxime prevents microtubule-targeting drug neurotoxicity: selective preservation of EB comets in differentiated neuronal cells. Biochem Pharmacol 15: 884-894.
46. Sagot Y, Tan SA, Baetge E, Schmalbruch H, Kato AC, Aebischer P, (1995). Polymer encapsulated cell lines genetically engineered to release ciliary neurotrophic factor can slow down progressive motor neuronopathy in the mouse. Eur J Neurosci 7: 1313-1322.
47. Sedarous M, Keramaris E, O'Hare M, Melloni E, Slack RS, Elce JS, et al. (2003). Calpains mediate p53 activation and neuronal death evoked by DNA damage. J Biol Chem 278: 26031-26038.
48. Sendtner M, Holtmann B, Kolbeck R, Thoenen H, Barde YA, (1992a). Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 360: 757-759.
49. Sendtner M, Schmalbruch H, Stockli KA, Carroll P, Kreutzberg GW, Thoenen H, (1992b). Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358: 502-504.
50. Shimizu S, Narita M, Tsujimoto Y, (1999). Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487.
51. Shimoke K, Kubo T, Numakawa T, Abiru Y, Enokido Y, Takei N, et al. (1997). Involvement of phosphatidylinositol-3 kinase in prevention of low K(+)-induced apoptosis of cerebellar granule neurons. Brain Res Dev Brain Res 101: 197-206.
52. Shimoke K, Yamagishi S, Yamada M, Ikeuchi T, Hatanaka H, (1999). Inhibition of phosphatidylinositol 3-kinase activity elevates c-Jun N-terminal kinase activity in apoptosis of cultured cerebellar granule neurons. Brain Res Dev Brain Res 112: 245-253.
53. Shoshan-Barmatz V, Ben-Hail D, (2012). VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12: 24-34.
54. Skaper SD, (2008). The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol Disord Drug Targets 7: 46-62.
55. Stefanis L, Park DS, Friedman WJ, Greene LA, (1999). Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J Neurosci 19: 6235-6247.
56. Sunyach C, Michaud M, Arnoux T, Bernard-Marissal N, Aebischer J, Latyszenok V, et al. (2012). Olesoxime delays muscle denervation, astrogliosis, microglial activation and motoneuron death in an ALS mouse model. Neuropharmacology 62: 2346-2352.
57. The BDNF Study Group (Phase III) (1999). A controlled trial of recombinant methionyl human BDNF in ALS: the BDNF Study Group (Phase III). Neurology 52: 1427-1433.
58. Tomac A, Lindqvist E, Lin LF, Ogren SO, Young D, Hoffer BJ, et al. (1995). Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373: 335-339.
59. Uo T, Kinoshita Y, Morrison RS, (2007). Apoptotic actions of p53 require transcriptional activation of PUMA and do not involve a direct mitochondrial/cytoplasmic site of action in postnatal cortical neurons. J Neurosci 27: 12198-12210.
60. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS, (1998). Bax involvement in p53-mediated neuronal cell death. J Neurosci 18: 1363-1373.
61. Xiao WH, Zheng FY, Bennett GJ, Bordet T, Pruss RM, (2009). Olesoxime (cholest-4-en-3-one, oxime): analgesic and neuroprotective effects in a rat model of painful peripheral neuropathy produced by the chemotherapeutic agent, paclitaxel. Pain 147: 202-209.
62. Yamagishi S, Matsumoto T, Yokomaku D, Hatanaka H, Shimoke K, Yamada M, et al. (2003). Comparison of inhibitory effects of brain-derived neurotrophic factor and insulin-like growth factor on low potassium-induced apoptosis and activation of p38 MAPK and c-Jun in cultured cerebellar granule neurons. Brain Res Mol Brain Res 119: 184-191.
63. Yao J, Irwin RW, Zhao L, Nilsen J, Hamilton RT, Brinton RD, (2009). Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 106: 14670-14675.
64. Zhang Y, Qu D, Morris EJ, O'Hare MJ, Callaghan SM, Slack RS, et al. (2006). The Chk1/Cdc25A pathway as activators of the cell cycle in neuronal death induced by camptothecin. J Neurosci 26: 8819-8828.
65. Zhu D, Wu X, Strauss KI, Lipsky RH, Qureshi Z, Terhakopian A, et al. (2005). N-methyl-D-aspartate and TrkB receptors protect neurons against glutamate excitotoxicity through an extracellular signal-regulated kinase pathway. J Neurosci Res 80: 104-113.
66. Zuccato C, Cattaneo E, (2009). Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 5: 311-322.