Nortriptyline delays disease onset in models of chronic neurodegeneration

European Journal of Neuroscience

Volumn 26, Issue 3, 2007, Pages 633-641

  Wang, Hongyan ^a   Guan, Yingjun ^a,f   Wang, Xin ^a   Smith, Karen ^b,c   Cormier, Kerry ^b,c   Zhu, Shan ^a   Stavrovskaya, Irina G ^d   Huo, Chunfeng ^a   Ferrante, Robert J ^b,c   Kristal, Bruce S ^d,e   Friedlander, Robert M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f WEIFANG MEDICAL UNIVERSITY   (China)

Author keywords

Amyotrophic lateral sclerosis; Cell death; Huntington's disease; Mitochondrial permeability transition; Rodent

Indexed keywords

CASPASE 3; CYTOCHROME C; NORTRIPTYLINE; PROMETHAZINE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; FEMALE; HUNTINGTON CHOREA; MALE; MITOCHONDRIAL PERMEABILITY; MORTALITY; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; APOPTOSIS; BRAIN; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; HUNTINGTON DISEASE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, TRANSGENIC; MITOCHONDRIA; NEURODEGENERATIVE DISEASES; NEURONS; NEUROPROTECTIVE AGENTS; NORTRIPTYLINE; TIME FACTORS; TREATMENT OUTCOME;

EID: 34547639330     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05663.x     Document Type: Article

References (48)

1. Anneser, J.M., Gmerek, A., Gerkrath, J., Borasio, G.D. Heumann, R. (2001) Immunosuppressant FK506 does not exert beneficial effects in symptomatic G93A superoxide dismutase-1 transgenic mice. Neuroreport, 12, 2663 2665.
2. Baines, C.P., Kaiser, R.A., Purcell, N.H., Blair, N.S., Osinska, H., Hambleton, M.A., Brunskill, E.W., Sayen, M.R., Gottlieb, R.A., Dorn, G.W., Robbins, J. Molkentin, J.D. (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature, 434, 658 662.
3. Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M.A. Bernardi, P. (2005) Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J. Biol. Chem., 280, 18558 18561.
4. Bossy-Wetzel, E., Schwarzenbacher, R. Lipton, S.A. (2004) Molecular pathways to neurodegeneration. Nat. Med., 10 (Suppl. S2 S9.
5. Bouchier-Hayes, L., Lartigue, L. Newmeyer, D.D. (2005) Mitochondria: pharmacological manipulation of cell death. J. Clin. Invest, 115, 2640 2647.
6. Cattaneo, E. Conti, L. (1998) Generation and characterization of embryonic striatal conditionally immortalized ST14A cells. J. Neurosci. Res., 53, 223 234.
7. Chen, M., Ona, V.O., Li, M., Ferrante, R.J., Fink, K.B., Zhu, S., Bian, J., Guo, L., Farrell, L.A., Hersch, S.M., Hobbs, W., Vonsattel, J.P., Cha, J.H. Friedlander, R.M. (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat. Med., 6, 797 801.
8. Damiano, M., Starkov, A.A., Petri, S., Kipiani, K., Kiaei, M., Mattiazzi, M., Flint Beal, M. Manfredi, G. (2006) Neural mitochondrial Ca2+ capacity impairment precedes the onset of motor symptoms in G93A Cu/Zn-superoxide dismutase mutant mice. J. Neurochem., 96, 1349 1361.
9. Ferrante, R.J., Gutekunst, C.A., Persichetti, F., McNeil, S.M., Kowall, N.W., Gusella, J.F., MacDonald, M.E., Beal, M.F. Hersch, S.M. (1997) Heterogeneous topographic and cellular distribution of huntingtin expression in the normal human neostriatum. J. Neurosci., 17, 3052 3063.
10. Friedlander, R.M. (2003) Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med., 348, 1365 1375.
11. Green, D.R. Kroemer, G. (2004) The pathophysiology of mitochondrial cell death. Science, 305, 626 629.
12. Green, D.R. Reed, J.C. (1998) Mitochondria and apoptosis. Science, 281, 1309 1312.
13. Guegan, C., Vila, M., Rosoklija, G., Hays, A.P. Przedborski, S. (2001) Recruitment of the mitochondrial-dependent apoptotic pathway in amyotrophic lateral sclerosis. J. Neurosci., 21, 6569 6576.
14. Gunter, T.E., Gunter, K.K., Sheu, S.S. Gavin, C.E. (1994) Mitochondrial calcium transport: physiological and pathological relevance. Am. J. Physiol., 267, C313 C339.
15. Gurney, M.E. (1994) Transgenic-mouse model of amyotrophic lateral sclerosis. N. Engl. J. Med., 331, 1721 1722.
16. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X.& et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science, 264, 1772 1775.
17. Heemskerk, J., Tobin, A.J. Bain, L.J. (2002a) Teaching old drugs new tricks. Meeting of the Neurodegeneration Drug Screening Consortium, 7-8 April 2002, Washington, DC, USA Trends Neurosci., 25, 494 496.
18. Heemskerk, J., Tobin, A.J. Ravina, B. (2002b) From chemical to drug: neurodegeneration drug screening and the ethics of clinical trials. Nat. Neurosci., 5 (Suppl. 1027 1029.
19. Karlsson, J., Fong, K.S., Hansson, M.J., Elmer, E., Csiszar, K. Keep, M.F. (2004) Life span extension and reduced neuronal death after weekly intraventricular cyclosporin injections in the G93A transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosurg, 101, 128 137.
20. Keep, M., Elmer, E., Fong, K.S. Csiszar, K. (2001) Intrathecal cyclosporin prolongs survival of late-stage ALS mice. Brain Res., 894, 327 331.
21. Kirkinezos, I.G., Hernandez, D., Bradley, W.G. Moraes, C.T. (2004) An ALS mouse model with a permeable blood-brain barrier benefits from systemic cyclosporine A treatment. J. Neurochem., 88, 821 826.
22. Kolla, N., Wei, Z., Richardson, J.S. Li, X.M. (2005) Amitriptyline and fluoxetine protect PC12 cells from cell death induced by hydrogen peroxide. J. Psychiatry Neurosci., 30, 196 201.
23. Kristal, B.S. Dubinsky, J.M. (1997) Mitochondrial permeability transition in the central nervous system: induction by calcium cycling-dependent and - independent pathways. J. Neurochem., 69, 524 538.
24. Kriz, J., Gowing, G. Julien, J.P. (2003) Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Ann. Neurol., 53, 429 436.
25. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell, 91, 479 489.
26. Li, M., Ona, V.O., Guegan, C., Chen, M., Jackson-Lewis, V., Andrews, L.J., Olszewski, A.J., Stieg, P.E., Lee, J.P., Przedborski, S. Friedlander, R.M. (2000) Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science, 288, 335 339.
27. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W. Bates, G.P. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell, 87, 493 506.
28. McCaslin, P.P.YuX.Z., Ho, I.K. Smith, T.G. (1992) Amitriptyline prevents N-methyl-D-aspartate (NMDA) -induced toxicity, does not prevent NMDA-induced elevations of extracellular glutamate, but augments kainate-induced elevations of glutamate. J. Neurochem., 59, 401 405.
29. Murphy, A.N., Fiskum, G. Beal, M.F. (1999) Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J. Cereb. Blood Flow Metab., 19, 231 245.
30. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T. Tsujimoto, Y. (2005) Cyclophilin d-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature, 434, 652 658.
31. Newmeyer, D.D. Ferguson-Miller, S. (2003) Mitochondria: releasing power for life and unleashing the machineries of death. Cell, 112, 481 490.
32. Nicotera, P. (2003) Molecular switches deciding the death of injured neurons. Toxicol. Sci., 74, 4 9.
33. Ona, V.O., Li, M., Vonsattel, J.P., Andrews, L.J., Khan, S.Q., Chung, W.M., Frey, A.S., Menon, A.S., Li, X.J., Stieg, P.E., Yuan, J., Penney, J.B., Young, A.B., Cha, J.H. Friedlander, R.M. (1999) Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease. Nature, 399, 263 267.
34. Petronilli, V., Costantini, P., Scorrano, L., Colonna, R., Passamonti, S. Bernardi, P. (1994) The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J. Biol. Chem., 269, 16638 16642.
35. Rigamonti, D., Bauer, J.H., De-Fraja, C., Conti, L., Sipione, S., Sciorati, C., Clementi, E., Hackam, A., Hayden, M.R., Li, Y., Cooper, J.K., Ross, C.A., Govoni, S., Vincenz, C. Cattaneo, E. (2000) Wild-type huntingtin protects from apoptosis upstream of caspase-3. J. Neurosci., 20, 3705 3713.
36. Ripps, M.E., Huntley, G.W., Hof, P.R., Morrison, J.H. Gordon, J.W. (1995) Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA, 92, 689 693.
37. Ryu, H., Smith, K., Camelo, S.I., Carreras, I., Lee, J., Iglesias, A.H., Dangond, F., Cormier, K.A., Cudkowicz, M.E., Brown, R.H. Jr. Ferrante, R.J. (2005) Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J. Neurochem., 93, 1087 1098.
38. Schinzel, A.C., Takeuchi, O., Huang, Z., Fisher, J.K., Zhou, Z., Rubens, J., Hetz, C., Danial, N.N., Moskowitz, M.A. Korsmeyer, S.J. (2005) Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc. Natl Acad. Sci. USA, 102, 12005 12010.
39. Stack, E.C., Smith, K.M., Ryu, H., Cormier, K., Chen, M., Hagerty, S.W., Del Signore, S.J., Cudkowicz, M.E., Friedlander, R.M. Ferrante, R.J. (2006) Combination therapy using minocycline and coenzyme Q (10) in R6/2 transgenic Huntington's disease mice. Biochim. Biophys. Acta., 1762, 373 380.
40. Stavrovskaya, I.G., Narayanan, M.V., Zhang, W., Krasnikov, B.F., Heemskerk, J., Young, S.S., Blass, J.P., Brown, A.M., Beal, M.F., Friedlander, R.M. Kristal, B.S. (2004) Clinically approved heterocyclics act on a mitochondrial target and reduce stroke-induced pathology. J. Exp. Med., 200, 211 222.
41. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Snow, B.E., Brothers, G.M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D.R., Aebersold, R., Siderovski, D.P., Penninger, J.M. Kroemer, G. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 397, 441 446.
42. Takahashi, T., Kobayashi, T., Ozaki, M., Takamatsu, Y., Ogai, Y., Ohta, M., Yamamoto, H. Ikeda, K. (2006) G protein-activated inwardly rectifying K+ channel inhibition and rescue of weaver mouse motor functions by antidepressants. Neurosci. Res., 54, 104 111.
43. Tang, T.S., Slow, E., Lupu, V., Stavrovskaya, I.G., Sugimori, M., Llinas, R., Kristal, B.S., Hayden, M.R. Bezprozvanny, I. (2005) Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc. Natl Acad. Sci. USA, 102, 2602 2607.
44. Wang, X., Wang, H., Figueroa, B.E., Zhang, W.H., Huo, C., Guan, Y., Zhang, Y., Bruey, J.M., Reed, J.C. Friedlander, R.M. (2005) Dysregulation of receptor interacting protein-2 and caspase recruitment domain only protein mediates aberrant caspase-1 activation in Huntington's disease. J. Neurosci., 25, 11645 11654.
45. Wang, X., Zhu, S., Drozda, M., Zhang, W., Stavrovskaya, I.G., Cattaneo, E., Ferrante, R.J., Kristal, B.S. Friedlander, R.M. (2003) Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc. Natl Acad. Sci. USA, 100, 10483 10487.
46. Zhang, W., Narayanan, M. Friedlander, R.M. (2003) Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann. Neurol., 53, 267 270.
47. Zhu, S., Stavrovskaya, I.G., Drozda, M., Kim, B.Y., Ona, V., Li, M., Sarang, S., Liu, A.S., Hartley, D.M., Wu du, C., Gullans, S., Ferrante, R.J., Przedborski, S., Kristal, B.S. Friedlander, R.M. (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature, 417, 74 78.
48. Zoratti, M. Szabo, I. (1995) The mitochondrial permeability transition. Biochim. Biophys. Acta, 1241, 139 176.