Early and progressive impairment of spinal blood flow-glucose metabolism coupling in motor neuron degeneration of ALS model mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 3, 2012, Pages 456-467

  Miyazaki, Kazunori ^a   Masamoto, Kazuto ^b,c   Morimoto, Nobutoshi ^a   Kurata, Tomoko ^a   Mimoto, Takahumi ^a   Obata, Takayuki ^b   Kanno, Iwao ^b   Abe, Koji ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF ELECTRO COMMUNICATIONS   (Japan)

Author keywords

ALS; flow metabolism uncoupling (FMU); G93A; local spinal glucose utilization (LSGU); spinal blood flow (SBF)

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CAPILLARY; CAPILLARY DENSITY; CONTROLLED STUDY; DISEASE COURSE; ERYTHROCYTE; EXPERIMENTAL MODEL; FEMALE; GLUCOSE METABOLISM; GLUCOSE UTILIZATION; GRAY MATTER; IMAGING; MALE; MOTOR NEURON DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD BLOOD FLOW; WILD TYPE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CAPILLARIES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GLUCOSE; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MOTOR NEURONS; NERVE DEGENERATION; REGIONAL BLOOD FLOW; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84857790779     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.155     Document Type: Article

References (46)

1. Abe K, Fujimura H, Toyooka K, Sakoda S, Yorifuji S, Yanagihara T (1997) Cognitive function in amyotrophic lateral sclerosis. J Neurol Sci 148:95-100
2. Aoki M, Ogasawara M, Matsubara Y, Narisawa K, Nakamura S, Itoyama Y, Abe K (1993) Mild ALS in Japan associated with novel SOD mutation. Nat Genet 5:323-4
3. Autio J, Kawaguchi H, Saito S, Aoki I, Obata T, Masamoto K, Kanno I (2011) Spatial frequency-based analysis of mean red blood cell speed in single microvessels: investigation of microvascular perfusion in rat cerebral cortex. PLoS One 6:e24056
4. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-92
5. Browne SE, Yang L, DiMauro JP, Fuller SW, Licata SC, Beal MF (2006) Bioenergetic abnormalities in discrete cerebral motor pathways presage spinal cord pathology in the G93A SOD1 mouse model of ALS. Neurobiol Dis 22:599-610
6. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown Jr RH, Julien JP, Goldstein LS, Cleveland DW (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-7
7. Dalakas MC, Hatazawa J, Brooks RA, Di Chiro G (1987) Lowered cerebral glucose utilization in amyotrophic lateral sclerosis. Ann Neurol 22:580-6
8. Davalos D, Lee JK, Smith WB, Brinkman B, Ellisman MH, Zheng B, Akassoglou K (2008) Stable in vivo imaging of densely populated glia, axons and blood vessels in the mouse spinal cord using two-photon microscopy. J Neurosci Methods 169:1-7
9. del Zoppo GJ (2010) The neurovascular unit, matrix proteases, and innate inflammation. Ann NY Acad Sci 1207:46-9
10. Dirnagl U (1997) Metabolic aspects of neurovascular coupling. Adv Exp Med Biol 413:155-9
11. Dupuis L, Pradat PF, Ludolph AC, Loeffler JP (2011) Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol 10:75-82
12. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, Sanberg PR (2007) Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS One 2:e1205
13. Gordon T, Tyreman N, Li S, Putman CT, Hegedus J (2010) Functional over-load saves motor units in the SOD1-G93A transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 37:412-22
14. Guo Z, Kindy MS, Kruman I, Mattson MP (2000) ALSlinked Cu/Zn-SOD mutation impairs cerebral synaptic glucose and glutamate transport and exacerbates ischemic brain injury. J Cereb Blood Flow Metab 20:463-8
15. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, Chen W, Zhai P, Sufit RL, Siddique T (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:1772-5
16. Harder DR, Alkayed NJ, Lange AR, Gebremedhin D, Roman RJ (1998) Functional hyperemia in the brain: hypothesis for astrocyte-derived vasodilator metabolites. Stroke 29:229-34
17. Hatazawa J, Brooks RA, Dalakas MC, Mansi L, Di Chiro G (1988) Cortical motor-sensory hypometabolism in amyotrophic lateral sclerosis: a PET study. J Comput Assist Tomogr 12:630-6
18. Henkel JS, Beers DR, Wen S, Bowser R, Appel SH (2009) Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS. Neurology 72:1614-6
19. Ishikawa T, Morita M, Nakano I (2007) Constant blood flow reduction in premotor frontal lobe regions in ALS with dementia-a SPECT study with 3D-SSP. Acta Neurol Scand 116:340-4
20. Jay TM, Lucignani G, Crane AM, Jehle J, Sokoloff L (1988) Measurement of local cerebral blood flow with [14C]iodoantipyrine in the mouse. J Cereb Blood Flow Metab 8:121-9
21. Krafft P, Frietsch T, Lenz C, Piepgras A, Kuschinsky W, Waschke KF (2000) Mild and moderate hypothermia (alpha-stat) do not impair the coupling between local cerebral blood flow and metabolism in rats. Stroke 31:1393-400; discussion 401
22. Kuschinsky W (1997) Neuronal-vascular coupling. A unifying hypothesis. Adv Exp Med Biol 413:167-76
23. Lenz C, Frietsch T, Futterer C, Rebel A, van Ackern K, Kuschinsky W, Waschke KF (1999) Local coupling of cerebral blood flow to cerebral glucose metabolism during inhalational anesthesia in rats: desflurane versus isoflurane. Anesthesiology 91:1720-3
24. Leybaert L (2005) Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 25:2-16
25. Leybaert L, De Bock M, Van Moorhem M, Decrock E, De Vuyst E (2007) Neurobarrier coupling in the brain: adjusting glucose entry with demand. J Neurosci Res 85:3213-20
26. Llinas RR, Sugimori M, Moran KA, Moreira JE, Fukuda M (2004) Vesicular reuptake inhibition by a synaptotagmin I C2B domain antibody at the squid giant synapse. Proc Natl Acad Sci USA 101:17855-60
27. Lo EH, Rosenberg GA (2009) The neurovascular unit in health and disease: introduction. Stroke 40:S2-3
28. Ludolph AC, Langen KJ, Regard M, Herzog H, Kemper B, Kuwert T, Bottger IG, Feinendegen L (1992) Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol Scand 85:81-9
29. Miyazaki K, Ohta Y, Nagai M, Morimoto N, Kurata T, Takehisa Y, Ikeda Y, Matsuura T, Abe K (2011) Disruption of neurovascular unit prior to motor neuron degeneration in amyotrophic lateral sclerosis. J Neurosci Res 89:718-28
30. Murakami T, Ilieva H, Shiote M, Nagata T, Nagano I, Shoji M, Abe K (2003) Hypoxic induction of vascular endothelial growth factor is selectively impaired in mice carrying the mutant SOD1 gene. Brain Res 989:231-7
31. Murakami T, Nagai M, Miyazaki K, Morimoto N, Ohta Y, Kurata T, Takehisa Y, Kamiya T, Abe K (2007) Early decrease of mitochondrial DNA repair enzymes in spinal motor neurons of presymptomatic transgenic mice carrying a mutant SOD1 gene. Brain Res 1150: 182-9
32. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-22
33. Ohta Y, Nagai M, Miyazaki K, Tanaka T, Kawai H, Morimoto N, Kurata T, Ikeda Y, Matsuura T, Abe K. Neuroprotective and angiogenic effects of bone marrow transplantation combined with granulocyte colonystimulating factor in a mouse model of amyotrophic lateral sclerosis. Cell Transplantation (in press)
34. Pramatarova A, Laganiere J, Roussel J, Brisebois K, Rouleau GA (2001) Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 21:3369-74
35. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, Hung WY, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, Gusella JS, Horvitz HR, Brown RH (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62
36. Sakurada O, Kennedy C, Jehle J, Brown JD, Carbin GL, Sokoloff L (1978) Measurement of local cerebral blood flow with iodo [14C] antipyrine. Am J Physiol 234:H59-66
37. Sasaki S, Warita H, Murakami T, Abe K, Iwata M (2004) Ultrastructural study of mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol 107:461-74
38. Sokoloff L (1977) Relation between physiological function and energy metabolism in the central nervous system. J Neurochem 29:13-26
39. Waldemar G, Vorstrup S, Jensen TS, Johnsen A, Boysen G (1992) Focal reductions of cerebral blood flow in amyotrophic lateral sclerosis: a [99mTc]-d,l-HMPAO SPECT study. J Neurol Sci 107:19-28
40. Wang J, Xu G, Slunt HH, Gonzales V, Coonfield M, Fromholt D, Copeland NG, Jenkins NA, Borchelt DR (2005) Coincident thresholds of mutant protein for paralytic disease and protein aggregation caused by restrictively expressed superoxide dismutase cDNA. Neurobiol Dis 20:943-52
41. Weir CJ, Zivin JA, Lyden PD (2002) Inter-relationships between spinal cord blood flow, neuronal death and neurological function in rabbit spinal cord ischemia. Brain Res 946:43-51
42. Xu R, Wu C, Zhang X, Zhang Q, Yang Y, Yi J, Yang R, Tao Y (2011) Linking hypoxic and oxidative insults to cell death mechanisms in models of ALS. Brain Res 1372:133-44
43. Yamashita T, Kamiya T, Deguchi K, Inaba T, Zhang H, Shang J, Miyazaki K, Ohtsuka A, Katayama Y, Abe K (2009) Dissociation and protection of the neurovascular unit after thrombolysis and reperfusion in ischemic rat brain. J Cereb Blood Flow Metab 29:715-25
44. Zhong Z, Deane R, Ali Z, Parisi M, Shapovalov Y, O'Banion MK, Stojanovic K, Sagare A, Boillee S, Cleveland DW, Zlokovic BV (2008) ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 11:420-2
45. Zivin JA, DeGirolami U, Hurwitz EL (1982) Spectrum of neurological deficits in experimental CNS ischemia. A quantitative study. Arch Neurol 39:408-12
46. Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201