Bioenergetic abnormalities in discrete cerebral motor pathways presage spinal cord pathology in the G93A SOD1 mouse model of ALS

Neurobiology of Disease

Volumn 22, Issue 3, 2006, Pages 599-610

  Browne, Susan E ^a   Yang, Lichuan ^a   DiMauro, Jon Paul ^a   Fuller, Sara W ^a   Licata, Stephanie C ^b   Beal, M Flint ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

2 Deoxyglucose; Amyotrophic lateral sclerosis; ATP; Brain; Cerebral glucose metabolism; Corticospinal tract; Creatine; Motor neuron; Motor neuron disease; Spinal cord

Indexed keywords

ADENOSINE TRIPHOSPHATE; COPPER ZINC SUPEROXIDE DISMUTASE; CREATINE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BIOENERGY; BRAIN CORTEX; BULBOSPINAL TRACT; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; EXPERIMENTAL MODEL; GLUCOSE METABOLISM; METABOLIC DISORDER; MOUSE; NERVE TRACT; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PYRAMIDAL TRACT; SPINAL CORD DISEASE; SPINAL CORD MOTONEURON;

ADENOSINE TRIPHOSPHATE; AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AUTORADIOGRAPHY; CARBON RADIOISOTOPES; CEREBRAL CORTEX; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DEOXYGLUCOSE; DISEASE MODELS, ANIMAL; EFFERENT PATHWAYS; ENERGY METABOLISM; GLUCOSE; HUMANS; MICE; MICE, TRANSGENIC; NERVE DEGENERATION; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 33744816535     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.01.001     Document Type: Article

References (63)

1. Albin R.L., and Greenamyre J.T. Alternative excitotoxic hypotheses. Neurology 42 (1992) 733-738
2. Alexander G.M., Deitch J.S., Seeburger J.L., Del Valle L., and Heiman-Patterson T.D. Elevated cortical extracellular fluid glutamate in transgenic mice expressing human mutant (G93A) Cu/Zn superoxide dismutase. J. Neurochem. 74 (2000) 1666-1673
3. Ames III A. CNS energy metabolism as related to function. Brain Res. Rev. 34 (2000) 42-68
4. Andreassen O.A., Jenkins B.G., Dedeoglu A., Ferrante K.L., Bogdanov M.B., Kaddurah-Daouk R., and Beal M.F. Increases in cortical glutamate concentrations in transgenic amyotrophic lateral sclerosis mice are attenuated by creatine supplementation. J. Neurochem. 77 (2001) 383-390
5. Bensimon G., Lacomblez L., Delumeau J.C., Bejuit R., Truffinet P., Meininger V., and Riluzole/ALS Study Group II. A study of riluzole in the treatment of advanced stage or elderly patients with amyotrophic lateral sclerosis. J. Neurol. 249 (2002) 609-615
6. Bernocchi P., Ceconi C., Cargnoni A., Pedersini P., Curello S., and Ferrari R. Extraction and assay of creatine phosphate, purine, and pyridine nucleotides in cardiac tissue by reversed-phase high-performance liquid chromatograph. Anal. Biochem. 222 (1994) 374-379
7. Borthwick G.M., Johnson M.A., Ince P.G., Shaw P.J., and Turnbull D.M. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann. Neurol. 46 (1999) 787-790
8. Bowling A.C., Schulz J.B., Brown R.H., and Beal M.F. Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J. Neurochem. 61 (1993) 2322-2325
9. Browne S.E., Bowling A.C., Baik M.J., Gurney M., Brown Jr. R.H., and Beal M.F. Metabolic dysfunction in familial, but not sporadic, amyotrophic lateral sclerosis. J. Neurochem. 71 (1998) 281-287
10. Browne S.E., Ayata C., Huang P.L., Moskowitz M.A., and Beal M.F. The cerebral metabolic consequences of nitric oxide synthase (NOS) deficiency: glucose utilization in neuronal and endothelial NOS null mice. J. Cereb. Blood Flow Metab. 19 (1999) 144-148
11. + concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Lett. 414 (1997) 365-368
12. Cicirata F., Angaut P., Cioni M., Serapide M.F., and Papale A. Functional organization of thalamic projections to the motor cortex. An anatomical and electrophysiological study in the rat. Neuroscience 19 (1986) 81-99
13. Cicirata F., Angaut P., Serapide M.F., and Panto M.R. Functional organization of the direct and indirect projection via the reticularis thalami nuclear complex from the motor cortex to the thalamic nucleus ventralis lateralis. Exp. Brain Res. 79 (1990) 325-337
14. Dal Canto M.C., and Gurney M.E. Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu, Zn, S.OD., and in mice overexpressing wild type SOD: a model of familial amyotrophic lateral sclerosis (FALS). Brain Res. 676 (1995) 25-40
15. Dupuis L., Oudart H., Rene F., Gonzalez de Aguilar J.L., and Loeffler J.P. Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 11159-11164
16. Eisen A., and Weber M. The motor cortex and amyotrophic lateral sclerosis. Muscle 24 (2001) 564-573
17. Ellis C.M., Suckling J., Amaro Jr. E., Bullmore E.T., Simmons A., Williams S.C., and Leigh P.N. Volumetric analysis reveals corticospinal degeneration and extramotor involvement in ALS. Neurology 9 (2001) 1571-1578
18. Ellis D.Z., Rabe J., and Sweadner K.J. Global loss of Na,K-ATPase and its nitric oxide-mediated regulation in a transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosci. 23 (2003) 43-51
19. Fujita K., Yamauchi M., Shibayama K., Ando M., Honda M., and Nagata Y. Decreased cytochrome c oxidase activity but unchanged superoxide dismutase and glutathione peroxidase activities in the spinal cords of patients with amyotrophic lateral sclerosis. J. Neurosci. Res. 45 (1996) 276-281
20. Gu X., Staines W.A., and Fortier P.A. Quantitative analyses of neurons projecting to primary motor cortex zones controlling limb movements in the rat. Brain Res. 835 (1999) 175-187
21. Gunther M.R., Vangilder R., Fang J., and Beattie D.S. Expression of a familial amyotrophic lateral sclerosis-associated mutant human superoxide dismutase in yeast leads to decreased mitochondrial electron transport. Arch. Biochem. Biophys. 431 (2004) 207-214
22. 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., and Deng H.X. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264 (1994) 1772-1775
23. Hatazawa J., Brooks R.A., Dalakas M.C., Mansi L., and Di Chiro G. Cortical motor-sensory hypo-metabolism in amyotrophic lateral sclerosis: a PET study. J. Comput. Assist. Tomogr. 12 (1988) 630-636
24. Higgins C.M., Jung C., Ding H., and Xu Z. Mutant Cu, Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J. Neurosci. 22 (2002) RC215
25. Higgins C.M., Jung C., and Xu Z. ALS-associated mutant SOD1 G93A causes mitochondrial vacuolation by expansion of the intermembrane space and by involvement of SOD1 aggregation and peroxisomes. BMC Neurosci. 4 (2003) 16
26. Hirano A., Nakano I., Kurland L.T., Mulder D.W., Holley P.W., and Saccomanno G. Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43 (1984) 471-480
27. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., DeGennaro L.J., Cleveland D.W., and Rothstein J.D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. 99 (2002) 1604-1609
28. Jaarsma D., Haasdijk E.D., Grashorn J.A., Hawkins R., van Duijn W., Verspaget H.W., London J., and Holstegem J.C. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol. Dis. 7 (2000) 623-643
29. Jaarsma D., Rognoni F., van Duijn W., Verspaget H.W., Haasdijk E.D., and Holstege J.C. CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. (Berl.) 102 (2001) 293-305
30. Julien J.P. Amyotrophic lateral sclerosis. Unfolding the toxicity of the misfolded. Cell 104 (2001) 581-591
31. Jung C., Higgins C.M., and Xu Z. Mitochondrial electron transport chain complex dysfunction in a transgenic mouse model for amyotrophic lateral sclerosis. J. Neurochem. 83 (2002) 535-545
32. Kaal E.C., Vlug A.S., Versleijen M.W., Kuilman M., Joosten E.A., and Bar P.R. Chronic mitochondrial inhibition induces selective motoneuron death in vitro: a new model for amyotrophic lateral sclerosis. J. Neurochem. 74 (2000) 1158-1165
33. Killackey H.P., and Sherman S.M. Corticothalamic projections from the rat primary somatosensory cortex. J. Neurosci. 23 (2003) 7381-7384
34. Kirkinezos I.G., Bacman S.R., Hernandez D., Oca-Cossio J., Arias L.J., Perez-Pinzon M.A., Bradley W.G., and Moraes C.T. Cytochrome c association with the inner mitochondrial membrane is impaired in the CNS of G93A-SOD1 mice. J. Neurosci. 25 (2005) 164-172
35. Klivenyi P., Ferrante R.J., Matthews R.T., Bogdanov M.B., Klein A.M., Andreassen O.A., Meuller G., Wermer M., Kaddurah-Daouk R., and Beal M.F. Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis. Nat. Med. 5 (1999) 347-350
36. Klivenyi P., Calingasan N.Y., Starkov A., Stavrovskaya I.G., Kristal B.S., Yang L., Wieringa B., and Beal M.F. Neuroprotective mechanisms of creatine occur in the absence of mitochondrial creatine kinase. Neurobiol. Dis. 15 (2004) 610-617
37. Kong J., and Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 18 (1998) 3241-3250
38. Lino M.M., Schneider C., and Caroni P. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci. 22 (2002) 4825-4832
39. Liu J., Lillo C., Jonsson P.A., Vande Velde C., Ward C.M., Miller T.M., Subramaniam J.R., Rothstein J.D., Marklund S., Andersen P.M., Brannstrom T., Gredal O., Wong P.C., Williams D.S., and Cleveland D.W. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43 (2004) 5-17
40. 10 administration increases brain mitochondrial concentrations and exerts neuroprotective effects. Proc. Natl. Acad. Sci. 95 (1998) 8892-8897
41. Mattiazzi M., D'Aurelio M., Gajewski C.D., Martushova K., Kiaei M., Beal M.F., and Manfredi G. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. ChemL. 277 (2002) 29626-29633
42. Menzies F.M., Cookson M.R., Taylor R.W., Turnbull D.M., Chrzanowska-Lightowlers Z.M., Dong L., Figlewicz D.A., and Shaw P.J. Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 125 (2002) 1522-1533
43. Mulder D.W., Kurland L.T., Offord K.P., and Beard C.M. Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 36 (1986) 511-517
44. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates (2001), Academic Press, San Diego CA
45. Ratovitski T., Corson L.B., Strain J., Wong P., Cleveland D.W., Culotta V.C., and Borchelt D.R. Variation in the biochemical/biophysical properties of mutant superoxide dismutase 1 enzymes and the rate of disease progression in familial amyotrophic lateral sclerosis kindreds. Hum. Mol. Genet. 8 (1999) 1451-1460
46. Rothstein J.D., Jin L., Dykes-Hoberg M., and Kuncl R.W. Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl. Acad. Sci. 90 (1993) 6591-6595
47. Sasaki S., and Iwata M. Ultrastructural study of synapses in the anterior horn neurons of patients with amyotrophic lateral sclerosis. Neurosci. Lett. 204 (1996) 53-56
48. Sasaki S., Warita H., Murakami T., Abe K., and Iwata M. Ultrastructural study of mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol. (Berl.) 107 (2004) 461-474
49. Siklos L., Engelhardt J., Harati Y., Smith R.G., Joo F., and Appel S.H. Ultrastructural evidence for altered calcium in motor nerve terminals in amyotropic lateral sclerosis. Ann. Neurol. 39 (1996) 203-216
50. 14C]2-deoxyglucose method for the measurement of local cerebral glucose utilization. Theory, procedure, and normal values in the conscious and anaesthetized rat. J. Neurochem. 28 (1977) 897-916
51. Spreux-Varoquaux O., Bensimon G., Lacomblez L., Salachas F., Pradat P.F., Le Forestier N., Marouan A., Dib M., and Meininger V. Glutamate levels in cerebrospinal fluid in amyotrophic lateral sclerosis: a reappraisal using a new HPLC method with coulometric detection in a large cohort of patients. J. Neurol. Sci. 193 (2002) 73-78
52. Strong M.J. The basic aspects of therapeutics in amyotrophic lateral sclerosis. Pharmacol. Ther. 98 (2003) 379-414
53. Takeuchi H., Kobayashi Y., Ishigaki S., Doyu M., and Sobue G. Mitochondrial localization of mutant superoxide dismutase 1 triggers caspase-dependent cell death in a cellular model of familial amyotrophic lateral sclerosis. J. Biol. Chem. 227 (2002) 50966-50972
54. Tandan R., and Bradley W.G. Amyotrophic lateral sclerosis: Part 1. Clinical features, pathology, and ethical issues in management. Ann. Neurol. 184 (1985) 271-280
55. Tarnopolsky M.A., and Beal M.F. Potential for creatine and other therapies targeting cellular energy dysfunction in neurological disorders. Ann. Neurol. 49 (2001) 561-567
56. Tracey J., and Waite P.M.E. Somatosensory system. In: Paxinos G. (Ed). The Rat Nervous System (1995), Academic Press, San Diego CA 689-704
57. Van Westerlaak M.G., Joosten E.A., Gribnau A.A., Cools A.R., and Bar P.R. Chronic mitochondrial inhibition induces glutamate-mediated corticomotoneuron death in an organotypic culture model. Exp. Neurol. 167 (2001) 393-400
58. Vijayvergiya C., Beal M.F., Buck J., and Manfredi G. Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J. Neurosci. 25 (2005) 2463-2470
59. Wallimann T., Dolder M., Schlattner U., Eder M., Hornemann T., O'Gorman E., Ruck A., and Brdiczka D. Some new aspects of creatine kinase (CK): compartmentation, structure, function and regulation for cellular and mitochondrial bioenergetics and physiology. Biofactors 8 (1998) 229-234
60. Wendt S., Dedeoglu A., Speer O., Wallimann T., Beal M.F., and Andreassen O.A. Reduced creatine kinase activity in transgenic amyotrophic lateral sclerosis mice. Free Radical Biol. Med. 32 (2002) 920-926
61. Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Copeland N.G., Jenkins N.A., Sisodia S.S., Cleveland D.W., and Price D.L. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14 (1995) 1105-1116
62. G93A G1H transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci. Lett. 332 (2002) 99-102
63. Zilles K., and Wree A. Cortex: areal and laminar structure. In: Paxinos G. (Ed). The Rat Nervous System (1995), Academic Press, San Diego CA 649-685