Brain-derived neurotrophic factor-mediated effects on mitochondrial respiratory coupling and neuroprotection share the same molecular signalling pathways

European Journal of Neuroscience

Volumn 35, Issue 3, 2012, Pages 366-374

  Markham, Anthony ^a   Cameron, Ian ^a   Bains, Rasneer ^a   Franklin, Paul ^a   Kiss, Janos P ^b   Schwendimann, Leslie ^c,d   Gressens, Pierre ^c,d,e   Spedding, Michael ^f  

^a UNIVERSITY OF SUNDERLAND   (United Kingdom)

^b Servier Research Institute for Medicinal Chemistry   (Hungary)

^c INSERM   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HÔPITAL ROBERT DEBRÉ   (France)

^f INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

Author keywords

Brain derived neurotrophic factor; Glial cell line derived neurotrophic factor; Mice; Mitochondria; Neurodegeneration; Oxidative metabolism

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; IBOTENIC ACID; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NERVE GROWTH FACTOR; PROTEIN BCL 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; BRAIN SYNAPTOSOME; CELLULAR PARAMETERS; CONCENTRATION RESPONSE; CONTROLLED STUDY; EXCITOTOXICITY; GRAY MATTER; IN VITRO STUDY; MITOCHONDRIAL RESPIRATION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY CONTROL INDEX; SIGNAL TRANSDUCTION; WHITE MATTER;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL RESPIRATION; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HUMANS; IBOTENIC ACID; INTERLEUKIN-1BETA; MICE; MITOCHONDRIA; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 84856467949     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07965.x     Document Type: Article

References (51)

1. Adlard, P.A., Perreau, V.M. & Cotman, C.W. (2005) The exercise-induced expression of BDNF within the hippocampus varies across life-span. Neurobiol. Aging, 26, 511-520.
2. Agid, Y., Buzsaki, G., Diamond, D.M., Frackowiak, R., Giedd, J., Girault, J.A., Grace, A., Lambert, J.J., Manji, H., Mayberg, H., Popoli, M., Prochiantz, A., Richter-Levin, G., Somogyi, P., Spedding, M., Svenningsson, P. & Weinberger, D. (2007) How can drug discovery for psychiatric disorders be improved? Nat. Rev. Drug Discov., 6, 189-201.
3. Bachmann, R.F., Wang, Y., Yuan, P., Zhou, R., Li, X., Alesci, S., Du, J. & Manji, H.K. (2009) Common effects of lithium and valproate on mitochondrial functions: protection against methamphetamine-induced mitochondrial damage 38. Int. J. Neuropsychopharmacol., 12, 805-822.
4. Betarbet, R., Sherer, T.B., Mackenzie, G., Garcia-Osuna, M., Panov, A.V. & Greenamyre, J.T. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci., 3, 1301-1309.
5. Brunoni, A.R., Lopes, M. & Fregni, F. (2008) A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression. Int. J. Neuropsychopharmacol., 11, 1169-1180.
6. Chance, B. & Williams, G.R. (1956) The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subj. Biochem., 17, 65-134.
7. Chauhan, D., Velankar, M., Brahmandam, M., Hideshima, T., Podar, K., Richardson, P., Schlossman, R., Ghobrial, I., Raje, N., Munshi, N. & Anderson, K.C. (2007) A novel Bcl-2/Bcl-X(L)/Bcl-w inhibitor ABT-737 as therapy in multiple myeloma. Oncogene, 26, 2374-2380.
8. Chen, Z.X. & Pervaiz, S. (2007) Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ., 14, 1617-1627.
9. Chen, Z.X. & Pervaiz, S. (2009) BCL-2: pro-or anti-oxidant? Front. Biosci. (Elite Ed.), 1, 263-268.
10. Cotman, C.W., Berchtold, N.C. & Christie, L.A. (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci., 30, 464-472.
11. Dantzer, R., Wollman, E.E., Vitkovic, L. & Yirmiya, R. (1999) Cytokines, stress, and depression. Conclusions and perspectives. Adv. Exp. Med. Biol., 461, 317-329.
12. Dechant, G. & Barde, Y.A. (2002) The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat. Neurosci., 5, 1131-1136.
13. Dicou, E., Rangon, C.M., Guimiot, F., Spedding, M. & Gressens, P. (2003) Positive allosteric modulators of AMPA receptors are neuroprotective against lesions induced by an NMDA agonist in neonatal mouse brain. Brain Res., 970, 221-225.
14. Du, J., Wang, Y., Hunter, R., Wie, Y., Blumenthal, R., Fanke, C., Khairova, R., Zhou, R., Yuan, P., Machado-Vieira, R., McEwen, B.S. & Manji, H.K. (2009) Dynamic regulation of mitochondrial function by glucocorticoids. Proc. Natl. Acad. Sci. USA, 06, 3543-3548.
15. Ernster, L., Dallner, G. & Azzone, G.F. (1963) Differential effects of rotenone and amytal on mitochondrial electron and energy transfer. J. Biol. Chem., 238, 1124-1131.
16. Gavillet, M., Allaman, I. & Magistretti, P.J. (2008) Modulation of astrocytic metabolic phenotype by proinflammatory cytokines. Glia, 56, 975-989.
17. Gomez-Pinilla, F., Vaynman, S. & Ying, Z. (2008) Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur. J. Neurosci., 28, 2278-2287.
18. Gornall, A.G., Bardawill, C.J. & David, M.M. (1949) Determination of serum proteins by means of the biuret reaction. J. Biol. Chem., 177, 751-766.
19. Gressens, P., Marret, S., Hill, J.M., Brenneman, D.E., Gozes, I., Fridkin, M. & Evrard, P. (1997) Vasoactive intestinal peptide prevents excitotoxic cell death in the murine developing brain. J. Clin. Invest., 100, 390-397.
20. Gupta, S.K., Mishra, R., Kusum, S., Spedding, M., Meiri, K.F., Gressens, P. & Mani, S. (2009) GAP-43 is essential for the neurotrophic effects of BDNF and positive AMPA receptor modulator S18986. Cell Death Differ., 16, 624-637.
21. Gutman, M., Singer, T.P. & Casida, J.E. (1970) Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase: XVII. Reaction sites of piericidin A and rotenone. J. Biol. Chem., 245, 1992-1997.
22. Han, B.H. & Holtzman, D.M. (2000) BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J. Neurosci., 20, 5775-5781.
23. Hetman, M., Kanning, K., Cavanaugh, J.E. & 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. Hickman, J.A., Hardwick, J.M., Kaczmarek, L.K. & Jonas, E.A. (2008) Bcl-xL inhibitor ABT-737 reveals a dual role for Bcl-xL in synaptic transmission. J. Neurophysiol., 99, 1515-1522.
25. Husson, I., Mesples, B., Bac, P., Vamecq, J., Evrard, P. & Gressens, P. (2002) Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge. Ann. Neurol., 51, 82-92.
26. Ibanez, C.F. (1998) Emerging themes in structural biology of neurotrophic factors. Trends Neurosci., 21, 438-444.
27. Kalb, R. (2005) The protean actions of neurotrophins and their receptors on the life and death of neurons. Trends Neurosci., 28, 5-11.
28. Kernie, S.G., Liebl, D.J. & Parada, L.F. (2000) BDNF regulates eating behavior and locomotor activity in mice. EMBO J., 19, 1290-1300.
29. Koo, J.W. & Duman, R.S. (2008) IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA, 105, 751-756.
30. Leadsham, J.E. & Gourley, C.W. (2010) cAMP/PKA signalling balances respiratory activity with mitochondria dependent apoptosis via transcriptional regulation. BMC Cell Biol., 11, 92-105.
31. Li, H., Chen, Y., Jones, A.F., Sanger, R.H., Collis, L.P., Flannery, R., McNay, E.C., Yu, T., Schwarzenbacher, R., Bossy, B., Bossy-Wetzel, E., Bennett, M.V., Pypaert, M., Hickman, J.A., Smith, P.J., Hardwick, J.M. & Jonas, E.A. (2008) Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA, 105, 2169-2174.
32. Markham, A., Cameron, I., Franklin, P. & Spedding, M. (2004) BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II. Eur. J. Neurosci., 20, 1189-1196.
33. Mattson, M.P. (2005) Energy intake, meal frequency, and health: a neurobiological perspective. Annu. Rev. Nutr., 25, 237-260.
34. Nonomura, T., Tsuchida, A., Ono-Kishino, M., Nakagawa, T., Taiji, M. & Noguchi, H. (2001) Brain-derived neurotrophic factor regulates energy expenditure through the central nervous system in obese diabetic mice. Int. J. Exp. Diabetes Res., 2, 201-209.
35. Nykjaer, A., Willnow, T.E. & Petersen, C.M. (2005) p75NTR - live or let die. Curr. Opin. Neurobiol., 15, 49-57.
36. Papa, S., Sardinelli, A.M., Scacco, S. & Technikova-Dodrova, Z. (1999) cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of cAMP-mediated transduction. FEBS Lett., 444, 245-249.
37. Perera, T.D., Coplan, J.D., Lisanby, S.H., Lipira, C.M., Arif, M., Carpio, C., Spitzer, G., Santarelli, L., Scharf, B., Hen, R., Rosoklija, G., Sackeim, H.A. & Dwork, A.J. (2007) Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J. Neurosci., 27, 4894-4901.
38. Pittenger, C. & Duman, R.S. (2008) Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology, 33, 88-109.
39. Plaisant, F., Clippe, A., Vander, S.D., Knoops, B. & Gressens, P. (2003a) Recombinant peroxiredoxin 5 protects against excitotoxic brain lesions in newborn mice. Free Radic. Biol. Med., 34, 862-872.
40. Plaisant, F., Dommergues, M.A., Spedding, M., Cecchelli, R., Brillault, J., Kato, G., Munoz, C. & Gressens, P. (2003b) Neuroprotective properties of tianeptine: interactions with cytokines. Neuropharmacology, 44, 801-809.
41. Qi, H., Mailliet, F., Spedding, M., Rocher, C., Zhang, X., Delagrange, P., McEwen, B., Jay, T.M. & Svenningsson, P. (2009) Antidepressants reverse the attenuation of the neurotrophic MEK/MAPK cascade in frontal cortex by elevated platform stress; reversal of effects on LTP is associated with GluA1 phosphorylation. Neuropharmacology, 56, 37-46.
42. Rocher, C., Spedding, M., Munoz, C. & Jay, T.M. (2004) Acute stress-induced changes in hippocampal/prefrontal circuits in rats: effects of antidepressants. Cereb. Cortex, 14, 224-229.
43. Schinder, A.F. & Poo, M. (2000) The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci., 23, 639-645.
44. Sherer, T.B., Kim, J.H., Betarbet, R. & Greenamyre, J.T. (2003) Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp. Neurol., 179, 9-16.
45. Shoshan-Barmatz, V., Keinan, N. & Zaid, H. (2008) Uncovering the role of VDAC in the regulation of cell life and death. J. Bioenerg. Biomembr., 40, 183-191.
46. Spedding, M. & Gressens, P. (2008) Neurotrophins and cytokines in neuronal plasticity. Novartis Found. Symp., 289, 222-233.
47. Spedding, M. & Spedding, C. (2008) Drugs in sport: a scientist-athlete's perspective: from ambition to neurochemistry. Br. J. Pharmacol., 154, 496-501.
48. Sweetman, A.J. & Weetman, D.F. (1972) The oxidation of biologically important monoamines by monoamine oxidase. Exp. Physiol. Biochem., 5, 302-328.
49. Tagscherer, K.E., Fassl, A., Campos, B., Farhadi, M., Kraemer, A., Bock, B.C., Macher-Goeppinger, S., Radlwimmer, B., Wiestler, O.D., Herold-Mende, C. & Roth, W. (2008) Apoptosis-based treatment of glioblastomas with ABT-737, a novel small molecule inhibitor of Bcl-2 family proteins. Oncogene, 27, 6646-6656.
50. Tong, I., Balazs, R., Soiampornkul, R., Thengnipon, W. & Cotman, C.W. (2008) Interleukin-1 Beta impairs derived neurotrophic factor-induced signal transduction. Neurobiol. Aging, 29, 1380-1393.
51. Wiedemann, F.R., Siemen, D., Mawrin, C., Horn, T.F. & Dietzmann, K. (2006) The neurotrophin receptor TrkB is colocalized to mitochondrial membranes. Int. J. Biochem. Cell Biol., 38, 610-620.