Effects of dexpramipexole on brain mitochondrial conductances and cellular bioenergetic efficiency

Brain Research

Volumn 1446, Issue , 2012, Pages 1-11

  Alavian, Kambiz N ^a   Dworetzky, Steven I ^c   Bonanni, Laura ^b   Zhang, Ping ^a   Sacchetti, Silvio ^a,b   Mariggio, Maria A ^b   Onofrj, Marco ^b   Thomas, Astrid ^b   Li, Hongmei ^a   Mangold, Jamie E ^c   Signore, Armando P ^c   Demarco, Ulrike ^c   Demady, Damon R ^c   Nabili, Panah ^a   Lazrove, Emma ^a   Smith, Peter J S ^d   Gribkoff, Valentin K ^c   Jonas, Elizabeth A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHIETI   (Italy)

^c SAB: Knopp Biosciences LLC   (United States)

^d MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Bioenergetics; Leak conductance; Mitochondrion; Neural metabolism; Patch clamp electrophysiology

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CYCLOSPORIN A; DEXPRAMIPEXOLE; PROTEASOME INHIBITOR;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENERGY; BRAIN CELL; BRAIN MITOCHONDRION; BRAIN OXYGEN CONSUMPTION; CELL METABOLISM; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; HUMAN; HUMAN CELL; ION CONDUCTANCE; LIVER MITOCHONDRION; MALE; MEMBRANE CONDUCTANCE; MITOCHONDRIAL PERMEABILITY; NERVE CELL CULTURE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEINASE INHIBITION; RAT;

ADENOSINE TRIPHOSPHATE; ADRENERGIC BETA-ANTAGONISTS; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICAL PROCESSES; BRAIN; CELL SURVIVAL; CELLS, CULTURED; CYCLOSPORINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; ENZYME INHIBITORS; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEUROBLASTOMA; NEURONS; OLIGOPEPTIDES; OXYGEN CONSUMPTION; PATCH-CLAMP TECHNIQUES; PROPRANOLOL; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84862793575     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.01.046     Document Type: Article

References (59)

1. N.A. Abramova, D.S. Cassarino, S.M. Khan, T.W. Painter, and J.P. Bennett Jr. Inhibition by R(+) or S(-) pramipexole of caspase activation and cell death induced by methylpyridinium ion or beta amyloid peptide in SH-SY5Y neuroblastoma J. Neurosci. Res. 67 2002 494 500 (Pubitemid 34117119)
2. K.N. Alavian, H. Li, L. Collis, L. Bonanni, L. Zeng, S. Sacchetti, E. Lazrove, P. Nabili, B. Flaherty, M. Graham, Y. Chen, S.M. Messerli, M.A. Mariggio, C. Rahner, E. McNay, G.C. Shore, P.J. Smith, J.M. Hardwick, and E.A. Jonas Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase Nat. Cell Biol. 13 2011 1224 1233
3. Z.B. Andrews, S. Diano, and T.L. Horvath Mitochondrial uncoupling proteins in the CNS: in support of function and survival Nat. Rev. Neurosci. 6 2005 829 840 (Pubitemid 41568725)
4. Azzolin, L.; von Stockum, S.; Basso, E.; Petronilli, V.; Forte, M.A.; Bernardi, P.; 2010. The mitochondrial permeability transition from yeast to mammals. FEBS Lett. 584, 2504-2509.
5. R. Bandopadhyay, and J. de Belleroche Pathogenesis of Parkinson's disease: emerging role of molecular chaperones Trends Mol. Med. 16 2010 27 36
6. M. Baron, A.P. Kudin, and W.S. Kunz Mitochondrial dysfunction in neurodegenerative disorders Biochem. Soc. Trans. 35 2007 1228 1231 (Pubitemid 350206468)
7. M.F. Beal Mitochondria and neurodegeneration Novartis Foundation Symposium 287 2007 183 192 discussion 192-6
8. P. Bernardi Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization J. Biol. Chem. 267 1992 8834 8839
9. P. Bernardi, and A. Rasola Calcium and cell death: the mitochondrial connection Subcell. Biochem. 45 2007 481 506
10. L. Bonanni, M. Chachar, T. Jover-Mengual, H. Li, A. Jones, H. Yokota, D. Ofengeim, R.J. Flannery, T. Miyawaki, C.H. Cho, B.M. Polster, M. Pypaert, J.M. Hardwick, S.L. Sensi, R.S. Zukin, and E.A. Jonas Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain J. Neurosci. 26 2006 6851 6862 (Pubitemid 44315246)
11. M.E. Bozik, E.W. Ingersoll, L. Volles, J.M. Mather, C.A. Amburgey, J.M. Moritz, D.G. Archibald, M. Sullivan, V.K. Gribkoff, R. Miller, H. Mitsumoto, D. Moore, D. Schoenfeld, J. Shefner, and M. Cudkowicz KNS-760704-CL201, part 1: a 12-week phase 2 study of the safety, tolerability, and clinical effects of KNS-760704 in ALS subjects abstract Amyotroph. Lateral Scler. 10 2009 28 29
12. Bozik, M.E.; Mather, J.L.; Kramer, W.G.; Gribkoff, V.K.; Ingersoll, E.W.; 2011. Safety, Tolerability, and Pharmacokinetics of KNS-760704 (Dexpramipexole) in Healthy Adult Subjects. J. Clin. Pharmacol. 51, 1177-1185.
13. M.D. Brand The efficiency and plasticity of mitochondrial energy transduction Biochem. Soc. Trans. 33 2005 897 904
14. M.R. Brown, P.G. Sullivan, K.A. Dorenbos, E.A. Modafferi, J.W. Geddes, and O. Steward Nitrogen disruption of synaptoneurosomes: an alternative method to isolate brain mitochondria J. Neurosci. Meth. 137 2004 299 303 (Pubitemid 38942894)
15. D.S. Cassarino, C.P. Fall, T.S. Smith, and J.P. Bennett Jr. Pramipexole reduces reactive oxygen species production in vivo and in vitro and inhibits the mitochondrial permeability transition produced by the parkinsonian neurotoxin methylpyridinium ion J. Neurochem. 71 1998 295 301 (Pubitemid 28292562)
16. Y.B. Chen, M.A. Aon, Y.T. Hsu, L. Soane, X. Teng, J.M. McCaffery, W.C. Cheng, B. Qi, H. Li, K.N. Alavian, M. Dayhoff-Brannigan, S. Zou, F.J. Pineda, B. O'Rourke, Y.H. Ko, P.L. Pedersen, L.K. Kaczmarek, E.A. Jonas, and J.M. Hardwick Bcl-xL regulates mitochondrial energetics by stabilizing the inner membrane potential J. Cell Biol. 195 2011 263 276
17. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem. J. 341 1999 233 249 (Pubitemid 29373645)
18. M. Cudkowicz, M.E. Bozik, E.W. Ingersoll, R. Miller, H. Mitsumoto, J. Shefner, D.H. Moore, D. Schoenfeld, J.L. Mather, D. Archibald, M. Sullivan, C. Amburgey, J. Moritz, and V.K. Gribkoff The effects of dexpramipexole (KNS-760704)in individuals withamyotrophic lateral sclerosis Nat. Med. 17 2011 1652 1656
19. R. Danzeisen, B. Schwalenstoecker, F. Gillardon, E. Buerger, V. Krzykalla, K. Klinder, L. Schild, B. Hengerer, A.C. Ludolph, C. Dorner-Ciossek, and L. Kussmaul Targeted antioxidative and neuroprotective properties of the dopamine agonist pramipexole and its nondopaminergic enantiomer SND919CL2x [(+)2-amino-4,5,6,7-tetrahydro-6-Lpropylamino-benzathiazole dihydrochloride] J. Pharmacol. Exp. Ther. 316 2006 189 199 (Pubitemid 41832596)
20. L.M. Dejean, S. Martinez-Caballero, L. Guo, C. Hughes, O. Teijido, T. Ducret, F. Ichas, S.J. Korsmeyer, B. Antonsson, E.A. Jonas, and K.W. Kinnally Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel Mol. Biol. Cell 16 2005 2424 2432 (Pubitemid 40632223)
21. M.W. Dodson, and M. Guo Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease Curr. Opin. Neurobiol. 17 2007 331 337 (Pubitemid 46880329)
22. L. Dupuis, J.L. Gonzalez de Aguilar, H. Oudart, M. de Tapia, L. Barbeito, and J.P. Loeffler Mitochondria in amyotrophic lateral sclerosis: a trigger and a target Neurodegener. Dis. 1 2004 245 254 (Pubitemid 40960427)
23. G. Ferrari-Toninelli, G. Maccarinelli, D. Uberti, E. Buerger, and M. Memo Mitochondria-targeted antioxidant effects of S(-) and R(+) pramipexole BMC Pharmacol. 10 2010 2
24. A.A. Gerencser, A. Neilson, S.W. Choi, U. Edman, N. Yadava, R.J. Oh, D.A. Ferrick, D.G. Nicholls, and M.D. Brand Quantitative microplate-based respirometry with correction for oxygen diffusion Anal. Chem. 81 2009 6868 6878
25. M. Gleichmann, L.P. Collis, P.J. Smith, and M.P. Mattson Simultaneous single neuron recording of O2 consumption, [Ca2 +]i and mitochondrial membrane potential in glutamate toxicity J. Neurochem. 109 2009 644 655
26. V.K. Gribkoff, and M.E. Bozik KNS-760704 [(6R)-4,5,6,7-tetrahydro-N6- propyl-2, 6-benzothiazole-diamine dihydrochloride monohydrate] for the treatment of amyotrophic lateral sclerosis CNS Neurosci. Ther. 14 2008 215 226
27. D.P. Hanger, A. Seereeram, and W. Noble Mediators of tau phosphorylation in the pathogenesis of Alzheimer's disease Expert. Rev. Neurother. 9 2009 1647 1666
28. D. Hinerfeld, M.D. Traini, R.P. Weinberger, B. Cochran, S.R. Doctrow, J. Harry, and S. Melov Endogenous mitochondrial oxidative stress: neurodegeneration, proteomic analysis, specific respiratory chain defects, and efficacious antioxidant therapy in superoxide dismutase 2 null mice J. Neurochem. 88 2004 657 667 (Pubitemid 38140210)
29. M.M. Iravani, C.O. Haddon, J.M. Cooper, P. Jenner, and A.H. Schapira Pramipexole protects against MPTP toxicity in non-human primates J. Neurochem. 96 2006 1315 1321
30. E.A. Jonas Molecular participants in mitochondrial cell death channel formation during neuronal ischemia Exp. Neurol. 218 2009 203 212
31. E.A. Jonas, R.J. Knox, and L.K. Kaczmarek Giga-ohm seals on intracellular membranes: a technique for studying intracellular ion channels in intact cells Neuron 19 1997 7 13 (Pubitemid 27332989)
32. J. Jordan, V. Cena, and J.H. Prehn Mitochondrial control of neuron death and its role in neurodegenerative disorders J. Physiol. Biochem. 59 2003 129 141
33. H. Kawamata, and G. Manfredi Mitochondrial dysfunction and intracellular calcium dysregulation in ALS Mech. Ageing Dev. 131 2010 517 526
34. K.W. Kinnally, H. Tedeschi, and C.A. Mannella Evidence for a novel voltage-activated channel in the outer mitochondrial membrane FEBS Lett. 226 1987 83 87
35. K.W. Kinnally, S. Martinez-Caballero, and L.M. Dejean Detection of the mitochondrial apoptosis-induced channel (MAC) and its regulation by Bcl-2 family proteins. Current Protocols in Toxicology 2006 Chapter 2, Unit2 12
36. S.C. Land, D.M. Porterfield, R.H. Sanger, and P.J. Smith The self-referencing oxygen-selective microelectrode: detection of transmembrane oxygen flux from single cells J. Exp. Biol. 202 1999 211 218 (Pubitemid 29083815)
37. W.D. Le, J. Jankovic, W. Xie, and S.H. Appel Antioxidant property of pramipexole independent of dopamine receptor activation in neuroprotection J. Neural Transm. 107 2000 1165 1173
38. J.J. Lemasters Modulation of mitochondrial membrane permeability in pathogenesis, autophagy and control of metabolism J. Gastroenterol. Hepatol. 22 Suppl. 1 2007 S31 S37
39. H. Li, Y. Chen, A.F. Jones, R.H. Sanger, L.P. Collis, R. Flannery, E.C. McNay, T. Yu, R. Schwarzenbacher, B. Bossy, E. Bossy-Wetzel, M.V. Bennett, M. Pypaert, J.A. Hickman, P.J. Smith, J.M. Hardwick, and E.A. Jonas Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons Proc. Natl. Acad. Sci. U. S. A. 105 2008 2169 2174 (Pubitemid 351439483)
40. T.A. Lohret, R.E. Jensen, and K.W. Kinnally Tim23, a protein import component of the mitochondrial inner membrane, is required for normal activity of the multiple conductance channel, MCC J. Cell Biol. 137 1997 377 386 (Pubitemid 27181291)
41. C.A. Mannella, and K.W. Kinnally Reflections on VDAC as a voltage-gated channel and a mitochondrial regulator J. Bioenerg. Biomembr. 40 2008 149 155
42. K.S. McNaught, D.P. Perl, A.L. Brownell, and C.W. Olanow Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease. [see comment] Ann. Neurol. 56 2004 149 162 (Pubitemid 38857373)
43. T. Miyawaki, T. Mashiko, D. Ofengeim, R.J. Flannery, K.M. Noh, S. Fujisawa, L. Bonanni, M.V. Bennett, R.S. Zukin, and E.A. Jonas Ischemic preconditioning blocks BAD translocation, Bcl-xL cleavage, and large channel activity in mitochondria of postischemic hippocampal neurons Proc. Natl. Acad. Sci. U. S. A. 105 2008 4892 4897 (Pubitemid 351753842)
44. H. Naiki, and Y. Nagai Molecular pathogenesis of protein misfolding diseases: pathological molecular environments versus quality control systems against misfolded proteins J. Biochem. 146 2009 751 756
45. D.G. Nicholls Oxidative stress and energy crises in neuronal dysfunction Ann. N. Y. Acad. Sci. 1147 2008 53 60
46. D.G. Nicholls, and S. Chalmers The integration of mitochondrial calcium transport and storage J. Bioenerg. Biomembr. 36 2004 277 281 (Pubitemid 39619826)
47. K. Nowikovsky, R.J. Schweyen, and P. Bernardi Pathophysiology of mitochondrial volume homeostasis: potassium transport and permeability transition Biochim. Biophys. Acta 1787 2009 345 350
48. E.V. Pavlov, M. Priault, D. Pietkiewicz, E.H. Cheng, B. Antonsson, S. Manon, S.J. Korsmeyer, C.A. Mannella, and K.W. Kinnally A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast J. Cell Biol. 155 2001 725 731 (Pubitemid 34286224)
49. S. Pedrini, D. Sau, S. Guareschi, M. Bogush, R.H. Brown Jr.; N. Naniche, A. Kia, D. Trotti, and P. Pasinelli ALS-linked mutant SOD1 damages mitochondria by promoting conformational changes in Bcl-2 Hum. Mol. Genet. 19 2010 2974 2986
50. J.J. Perry, D.S. Shin, and J.A. Tainer Amyotrophic lateral sclerosis Adv. Exp. Med. Biol. 685 2010 9 20
51. S. Sasaki, and M. Iwata Ultrastructural study of the synapses of central chromatolytic anterior horn cells in motor neuron disease J. Neuropathol. Exp. Neurol. 55 1996 932 939 (Pubitemid 26287010)
52. I. Sayeed, S. Parvez, K. Winkler-Stuck, G. Seitz, I. Trieu, C.W. Wallesch, P. Schonfeld, and D. Siemen Patch clamp reveals powerful blockade of the mitochondrial permeability transition pore by the D2-receptor agonist pramipexole FASEB J. 20 2006 556 558 (Pubitemid 46671248)
53. N. Shalbuyeva, T. Brustovetsky, and N. Brustovetsky Lithium desensitizes brain mitochondria to calcium, antagonizes permeability transition, and diminishes cytochrome C release J. Biol. Chem. 282 2007 18057 18068 (Pubitemid 47100223)
54. B.F. Shaw, and J.S. Valentine How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem. Sci. 32 2007 78 85 (Pubitemid 46199198)
55. R.H. Swerdlow, J.K. Parks, D.S. Cassarino, P.A. Trimmer, S.W. Miller, D.J. Maguire, J.P. Sheehan, R.S. Maguire, G. Pattee, V.C. Juel, L.H. Phillips, J.B. Tuttle, J.P. Bennett Jr.; R.E. Davis, and W.D. Parker Jr. Mitochondria in sporadic amyotrophic lateral sclerosis Exp. Neurol. 153 1998 135 142 (Pubitemid 28452305)
56. I. Szabo, and M. Zoratti The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A J. Biol. Chem. 266 1991 3376 3379 (Pubitemid 21909221)
57. I. Szabo, P. Bernardi, and M. Zoratti Modulation of the mitochondrial megachannel by divalent cations and protons J. Biol. Chem. 267 1992 2940 2946
58. H. Wang, K.S. Larriviere, K.E. Keller, K.A. Ware, T.M. Burns, M.A. Conaway, D. Lacomis, G.L. Pattee, L.H. Phillips II, N.J. Solenski, S.A. Zivkovic, and J.P. Bennett Jr. R + pramipexole as a mitochondrially focused neuroprotectant: initial early phase studies in ALS Amyotroph. Lateral Scler. 9 2008 50 58 (Pubitemid 351260373)
59. S. Wang, Z. Xing, P.S. Vosler, H. Yin, W. Li, F. Zhang, A.P. Signore, R.A. Stetler, Y. Gao, and J. Chen Cellular NAD replenishment confers marked neuroprotection against ischemic cell death: role of enhanced DNA repair Stroke 39 2008 2587 2595