Cerebrospinal fluid evidence of increased extra-mitochondrial glucose metabolism implicates mitochondrial dysfunction in multiple sclerosis disease progression

Journal of the Neurological Sciences

Volumn 275, Issue 1-2, 2008, Pages 106-112

  Regenold, William T ^a,b   Phatak, Pornima ^a,b   Makley, Michael J ^a   Stone, Roger D ^c   Kling, Mitchel A ^d  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b BALTIMORE VA MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^d Discovery Analytical Chemistry Chemical and Screening Sciences   (United States)

Author keywords

Degeneration; Energy; Glucose; Lactate; Metabolism; Mitochondrial; Multiple sclerosis; Polyol; Progression

Indexed keywords

FRUCTOSE; GLUCOSE; INOSITOL; LACTIC ACID; SORBITOL;

ADULT; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; DISEASE COURSE; EXPANDED DISABILITY STATUS SCALE; FEMALE; GAS CHROMATOGRAPHY; GLUCOSE METABOLISM; HUMAN; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; PATHOGENESIS; PRIORITY JOURNAL;

ADULT; ANALYSIS OF VARIANCE; DISEASE PROGRESSION; FEMALE; FRUCTOSE; GLUCOSE; HUMANS; LACTIC ACID; MALE; MIDDLE AGED; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MULTIPLE SCLEROSIS; PILOT PROJECTS; SORBITOL; YOUNG ADULT;

EID: 55649118665     PISSN: 0022510X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jns.2008.07.032     Document Type: Article

References (46)

1. Confavreux C., Vukusic S., Moreau T., and Adeleine P. Relapses and progression of disability in multiple sclerosis. N Engl J Med 343 (2000) 1430-1438
2. McDonald W.I. Relapse, remission, and progression in multiple sclerosis. N Engl J Med 343 (2000) 1486-1487
3. Dutta R., McDonough J., Yin X., Peterson J., Chang A., Torres T., et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59 (2006) 478-489
4. Kalman B., and Leist T.P. A mitochondrial component of neurodegeneration in multiple sclerosis. Neuromolecular Med 3 (2003) 147-158
5. Lu F., Selak M., O'Connor J., Croul S., Lorenzana C., Butunoi C., et al. Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis. J Neurol Sci 177 (2000) 95-103
6. Waxman S.G. Ions, energy and axonal injury: towards a molecular neurology of multiple sclerosis. Trends Mol Med 12 (2006) 192-195
7. Kalman B., Lublin F.D., and Alder H. Mitochondrial DNA mutations in multiple sclerosis. Mult Scler 1 (1995) 32-36
8. Lees F., Macdonald A.M., and Turner J.W. Leber's disease with symptoms resembling disseminated sclerosis. J Neurol Neurosurg Psychiatry 27 (1964) 415-421
9. Lutz N.W., Viola A., Malikova I., Confort-Gouny S., Audoin B., Ranjeva J.P., et al. Inflammatory multiple-sclerosis plaques generate characteristic metabolic profiles in cerebrospinal fluid. PLoS ONE 2 (2007) e595
10. Nicoli F., Vion-Dury J., Confort-Gouny S., Maillet S., Gastaut J.L., and Cozzone P.J. Cerebrospinal fluid metabolic profiles in multiple sclerosis and degenerative dementias obtained by high resolution proton magnetic resonance spectroscopy. C R Acad Sci III 319 (1996) 623-631
11. Smith S.L., Novotny M., and Karmen A. Elevation of certain polyols in the cerebrospinal fluid of patients with multiple sclerosis. J Chromatogr 336 (1984) 351-355
12. Berry G.T., Hunter J.V., Wang Z., Dreha S., Mazur A., Brooks D.G., et al. In vivo evidence of brain galactitol accumulation in an infant with galactosemia and encephalopathy. J Pediatr 138 (2001) 260-262
13. Gabbay K.H. Hyperglycemia, polyol metabolism, and complications of diabetes mellitus. Annu Rev Med 26 (1975) 521-536
14. van der Knaap M.S., Wevers R.A., Struys E.A., Verhoeven N.M., Pouwels P.J., Engelke U.F., et al. Leukoencephalopathy associated with a disturbance in the metabolism of polyols. Ann Neurol 46 (1999) 925-928
15. Stevens M.J., Feldman E.L., and Greene D.A. The aetiology of diabetic neuropathy: the combined roles of metabolic and vascular defects. Diabet Med 12 (1995) 566-579
16. Finsterer J. Cerebrospinal-fluid lactate in adult mitochondriopathy with and without encephalopathy. Acta Med Austriaca 28 (2001) 152-155
17. Seyama K., Suzuki K., Mizuno Y., Yoshida M., Tanaka M., and Ozawa T. Mitochondrial encephalomyopathy with lactic acidosis and stroke-like episodes with special reference to the mechanism of cerebral manifestations. Acta Neurol Scand 80 (1989) 561-568
18. Kalman B., Laitinen K., and Komoly S. The involvement of mitochondria in the pathogenesis of multiple sclerosis. J Neuroimmunol 188 (2007) 1-12
19. Qi X., Lewin A.S., Sun L., Hauswirth W.W., and Guy J. Mitochondrial protein nitration primes neurodegeneration in experimental autoimmune encephalomyelitis. J Biol Chem 281 (2006) 31950-31962
20. Rose A.S., Kuzma J.W., Kurtzke J.F., Namerow N.S., Sibley W.A., and Tourtellotte W.W. Cooperative study in the evaluation of therapy in multiple sclerosis. ACTH vs. placebo-final report. Neurology 20 (1970) 1-59
21. Regenold W.T., Kling M.A., and Hauser P. Elevated sorbitol concentration in the cerebrospinal fluid of patients with mood disorders. Psychoneuroendocrinology 25 (2000) 593-606
22. Davson H., Welch K., and Segal M.B. Physiology and pathophysiology of the cerebrospinal fluid (1987), Churchill Livingstone, Edinburgh
23. Shetty H.U., Holloway H.W., and Rapoport S.I. Capillary gas chromatography combined with ion trap detection for quantitative profiling of polyols in cerebrospinal fluid and plasma. Anal Biochem 224 (1995) 279-285
24. Shetty H.U., Holloway H.W., and Schapiro M.B. Cerebrospinal fluid and plasma distribution of myo-inositol and other polyols in Alzheimer disease. Clin Chem 42 (1996) 298-302
25. Wray H.L., and Winegrad A.I. Free fructose in human cerebrospinal fluid. Diabetologia 2 (1966) 82-85
26. Watson M.A., and Scott M.G. Clinical utility of biochemical analysis of cerebrospinal fluid. Clin Chem 41 (1995) 343-360
27. Shetty H.U., Schapiro M.B., Holloway H.W., and Rapoport S.I. Polyol profiles in Down syndrome. myo-Inositol, specifically, is elevated in the cerebrospinal fluid. J Clin Invest 95 (1995) 542-546
28. Berry G.T. The role of polyols in the pathophysiology of hypergalactosemia. Eur J Pediatr 154 (1995) S53-64
29. Regenold W.T., Hisley K.C., Obuchowski A., Lefkowitz D.M., Marano C., and Hauser P. Relationship of white matter hyperintensities to cerebrospinal fluid glucose polyol pathway metabolites-a pilot study in treatment-resistant affective disorder patients. J Affect Disord 85 (2005) 341-350
30. Servo C. Sorbitol and myoinositol levels in the cerebrospinal fluid of diabetic patients. Acta Endocrinol Suppl 238 (1980) 133-137
31. Servo C., Palo J., and Pitkanen E. Gas chromatographic separation and mass spectrometric identification of polyols in human cerebrospinal fluid and plasma. Acta Neurol Scand 56 (1977) 104-110
32. Watanabe S., Kamiyama J., Chigasaki H., and Yoshioka S. Polyol content of cerebrospinal fluid in brain-tumor patients. J Neurosurg 70 (1989) 183-189
33. Yamamoto M., Ujike H., Wada K., and Tsuji T. Cerebrospinal fluid lactate and pyruvate concentrations in patients with Parkinson's disease and mitochondrial encephalomyopathy, lactic acidosis, and stroke-like episodes (MELAS). J Neurol Neurosurg Psychiatry 62 (1997) 290
34. Aasly J., Garseth M., Sonnewald U., Zwart J.A., White L.R., and Unsgard G. Cerebrospinal fluid lactate and glutamine are reduced in multiple sclerosis. Acta Neurol Scand 95 (1997) 9-12
35. Lynch J., Peeling J., Auty A., and Sutherland G.R. Nuclear magnetic resonance study of cerebrospinal fluid from patients with multiple sclerosis. Can J Neurol Sci 20 (1993) 194-198
36. Jongen P.J., Lamers K.J., Doesburg W.H., Lemmens W.A., and Hommes O.R. Cerebrospinal fluid analysis differentiates between relapsing-remitting and secondary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 63 (1997) 446-451
37. Simone I.L., Federico F., Trojano M., Tortorella C., Liguori M., Giannini P., et al. High resolution proton MR spectroscopy of cerebrospinal fluid in MS patients. Comparison with biochemical changes in demyelinating plaques. J Neurol Sci 144 (1996) 182-190
38. Magistretti P.J., and Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 354 (1999) 1155-1163
39. Frackowiak R.S., Herold S., Petty R.K., and Morgan-Hughes J.A. The cerebral metabolism of glucose and oxygen measured with positron tomography in patients with mitochondrial diseases. Brain 111 Pt 5 (1988) 1009-1024
40. Danielson S.R., Carelli V., Tan G., Martinuzzi A., Schapira A.H., Savontaus M.L., et al. Isolation of transcriptomal changes attributable to LHON mutations and the cybridization process. Brain 128 (2005) 1026-1037
41. Rango M., Bozzali M., Prelle A., Scarlato G., and Bresolin N. Brain activation in normal subjects and in patients affected by mitochondrial disease without clinical central nervous system involvement: a phosphorus magnetic resonance spectroscopy study. J Cereb Blood Flow Metab 21 (2001) 85-91
42. Mihailova S.M., Ivanova M.I., Quin L.M., and Naumova E.J. Mitochondrial DNA variants in Bulgarian patients affected by multiple sclerosis. Eur J Neurol 14 (2007) 44-47
43. Olsen N.K., Hansen A.W., Norby S., Edal A.L., Jorgensen J.R., and Rosenberg T. Leber's hereditary optic neuropathy associated with a disorder indistinguishable from multiple sclerosis in a male harbouring the mitochondrial DNA 11778 mutation. Acta Neurol Scand 91 (1995) 326-329
44. Kalman B., and Alder H. Is the mitochondrial DNA involved in determining susceptibility to multiple sclerosis?. Acta Neurol Scand 98 (1998) 232-237
45. Kaufmann P., Shungu D.C., Sano M.C., Jhung S., Engelstad K., Mitsis E., et al. Cerebral lactic acidosis correlates with neurological impairment in MELAS. Neurology 62 (2004) 1297-1302
46. Friese M.A., Craner M.J., Etzensperger R., Vergo S., Wemmie J.A., Welsh M.J., et al. Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 13 (2007) 1483-1489