PH as a biomarker of neurodegeneration in Huntington's disease: A translational rodent-human MRS study

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 5, 2012, Pages 771-779

  Chaumeil, Myriam M ^a,b   Valette, Julien ^a   Baligand, Céline ^b   Brouillet, Emmanuel ^a   Hantraye, Philippe ^a   Bloch, Gilles ^a   Gaura, Véronique ^a   Rialland, Amandine ^c   Krystkowiak, Pierre ^d   Verny, Christophe ^e   Damier, Philippe ^f   Remy, Philippe ^a,c   Bachoud Levi, Anne Catherine ^c,g,h   Carlier, Pierre ^b   Lebon, Vincent ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b Institut de Myologie   (France)

^c HENRI MONDOR HOSPITAL   (France)

^d LILLE UNIVERSITY HOSPITAL   (France)

^e ANGERS UNIVERSITY HOSPITAL   (France)

^f CHU de Nantes   (France)

^g UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^h ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

3 nitropropionic acid; 31P MR spectroscopy; brain; Huntington's disease; pH

Indexed keywords

3 NITROPROPIONIC ACID; BIOLOGICAL MARKER; PHOSPHORUS 31; SUCCINATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DAMAGE; CENTRAL NERVOUS SYSTEM INFECTION; CEREBRAL PH; CONTROLLED STUDY; CORPUS STRIATUM; CORRELATIONAL STUDY; FEMALE; HUNTINGTON CHOREA; HYPOTHESIS; INTOXICATION; MALE; NERVE DEGENERATION; NONHUMAN; PH; PH MEASUREMENT; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; TRANSLATIONAL RESEARCH; VALIDATION PROCESS;

ADULT; ANIMALS; ANTIHYPERTENSIVE AGENTS; BIOLOGICAL MARKERS; CORPUS STRIATUM; FEMALE; HUMANS; HUNTINGTON DISEASE; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; NITRO COMPOUNDS; PROPIONIC ACIDS; RATS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84860437363     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.15     Document Type: Article

References (54)

1. Albers MJ, Krieger MD, Gonzalez-Gomez I, Gilles FH, McComb JG, Nelson Jr MD, Bluml S (2005) Protondecoupled 31P MRS in untreated pediatric brain tumors. Magn Reson Med 53: 22-9 (Pubitemid 40110473)
2. Beal MF (2005) Mitochondria take center stage in aging and neurodegeneration. Ann Neurol 58: 495-505 (Pubitemid 41377212)
3. Bizat N, Hermel JM, Boyer F, Jacquard C, Creminon C, Ouary S, Escartin C, Hantraye P, Kajewski S, Brouillet E (2003a) Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease. J Neurosci 23: 5020-30 (Pubitemid 36793229)
4. Bizat N, Hermel JM, Humbert S, Jacquard C, Creminon C, Escartin C, Saudou F, Krajewski S, Hantraye P, Brouillet E (2003b) In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase-3. J Biol Chem 278: 43245-53 (Pubitemid 37345944)
5. Boumezbeur F, Besret L, Valette J, Gregoire MC, Delzescaux T, Maroy R, Vaufrey F, Gervais P, Hantraye P, Bloch G, Lebon V (2005) Glycolysis versus TCA cycle in the primate brain as measured by combining 18F-FDG PET and 13C-NMR. J Cereb Blood Flow Metab 25: 1418-23 (Pubitemid 41541952)
6. Boumezbeur F, Besret L, Valette J, Vaufrey F, Henry PG, Slavov V, Giacomini E, Hantraye P, Bloch G, Lebon V (2004) NMR measurement of brain oxidative metabolism in monkeys using 13C-labeled glucose without a 13C radiofrequency channel. Magn Reson Med 52: 33-40 (Pubitemid 39295253)
7. Brouillet E, Conde F, Beal MF, Hantraye P (1999) Replicating Huntington's disease phenotype in experimental animals. Prog Neurobiol 59: 427-68 (Pubitemid 29392967)
8. Brouillet E, Jacquard C, Bizat N, Blum D (2005) 3-Nitropropionic acid: a mitochondrial toxin to uncover physiopathological mechanisms underlying striatal degeneration in Huntington's disease. J Neurochem 95: 1521-40 (Pubitemid 41804051)
9. Chaumeil MM, Valette J, Guillermier M, Brouillet E, Boumezbeur F, Herard AS, Bloch G, Hantraye P, Lebon V (2009) Multimodal neuroimaging provides a highly consistent picture of energy metabolism, validating 31P MRS for measuring brain ATP synthesis. Proc Natl Acad Sci USA 106: 3988-93
10. Chopp M, Vande Linde AM, Chen H, Knight R, Helpern JA, Welch KM (1990) Chronic cerebral intracellular alkalosis following forebrain ischemic insult in rats. Stroke 21: 463-6 (Pubitemid 20089796)
11. Corbett RJ, Nunnally RL, Giovanella BC, Antich PP (1987) Characterization of the 31P nuclear magnetic resonance spectrum from human melanoma tumors implanted in nude mice. Cancer Res 47: 5065-9 (Pubitemid 17146473)
12. Damiano M, Galvan L, Deglon N, Brouillet E (2010) Mitochondria in Huntington's disease. Biochim Biophys Acta 1802: 52-61
13. Dautry C, Vaufrey F, Brouillet E, Bizat N, Henry PG, Conde F, Bloch G, Hantraye P (2000) Early N-acetylaspartate depletion is a marker of neuronal dysfunction in rats and primates chronically treated with the mitochondrial toxin 3-nitropropionic acid. J Cereb Blood Flow Metab 20: 789-99 (Pubitemid 30317053)
14. Garcia M, Vanhoutte P, Pages C, Besson MJ, Brouillet E, Caboche J (2002) Themitochondrial toxin 3-nitropropionic acid induces striatal neurodegeneration via a c-Jun N-terminal kinase/c-Jun module. J Neurosci 22: 2174-84 (Pubitemid 35386517)
15. Gerweck LE, Seetharaman K (1996) Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer Res 56: 1194-8 (Pubitemid 26080953)
16. Govindaraju V, Young K, Maudsley AA (2000) Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13: 129-53 (Pubitemid 30414704)
17. Hamakawa H, Murashita J, Yamada N, Inubushi T, Kato N, Kato T (2004) Reduced intracellular pH in the basal ganglia and whole brain measured by 31P-MRS in bipolar disorder. Psychiatry Clin Neurosci 58: 82-8 (Pubitemid 38200376)
18. Hamilton G, Mathur R, Allsop JM, Forton DM, Dhanjal NS, Shaw RJ, Taylor-Robinson SD (2003) Changes in brain intracellular pH and membrane phospholipids on oxygen therapy in hypoxic patients with chronic obstructive pulmonary disease. Metab Brain Dis 18: 95-109 (Pubitemid 36207340)
19. Harper PS (1991) Huntington's Disease. Saunders: London
20. Henry PG, Lebon V, Vaufrey F, Brouillet E, Hantraye P, Bloch G (2002) Decreased TCA cycle rate in the rat brain after acute 3-NP treatment measured by in vivo 1H-[13C] NMR spectroscopy. J Neurochem 82: 857-66.
21. Hoang TQ, Bluml S, Dubowitz DJ, Moats R, Kopyov O, Jacques D, Ross BD (1998) Quantitative proton-decoupled 31P MRS and 1H MRS in the evaluation of Huntington's and Parkinson's diseases. Neurology 50: 1033-40 (Pubitemid 28212834)
22. Hugg JW, Duijn JH, Matson GB, Maudsley AA, Tsuruda JS, Gelinas DF, Weiner MW (1992) Elevated lactate and alkalosis in chronic human brain infarction observed by 1H and 31P MR spectroscopic imaging. J Cereb Blood Flow Metab 12: 734-44
23. Jenkins BG, Koroshetz WJ, Beal MF, Rosen BR (1993) Evidence for impairment of energy metabolism in vivo in Huntington's disease using localized 1H NMR spectroscopy. Neurology 43: 2689-95 (Pubitemid 24004570)
24. Jenkins BG, Rosas HD, Chen YC, Makabe T, Myers R, MacDonald M, Rosen BR, Beal MF, Koroshetz WJ (1998) 1H NMR spectroscopy studies of Huntington's disease: correlations with CAG repeat numbers. Neurology 50: 1357-65 (Pubitemid 28240352)
25. Jensen JE, Daniels M, Haws C, Bolo NR, Lyoo IK, Yoon SJ, Cohen BM, Stoll AL, Rusche JR, Renshaw PF (2008) Triacetyluridine (TAU) decreases depressive symptoms and increases brain pH in bipolar patients. Exp Clin Psychopharmacol 16: 199-206 (Pubitemid 351822563)
26. Jensen JE Drost DJ, Menon RS, Williamson PC (2002) In vivo brain (31)P-MRS: measuring the phospholipid resonances at 4 Tesla from small voxels. NMR Biomed 15: 338-47 (Pubitemid 34960101)
27. Kaila KR, Bruce R (1998) pH and Brain Function.Wiley-Liss: England
28. Kato T, Shioiri T, Murashita J, Hamakawa H, Inubushi T, Takahashi S (1994) Phosphorus-31 magnetic resonance spectroscopy and ventricular enlargement in bipolar disorder. Psychiatry Res 55: 41-50 (Pubitemid 24119048)
29. Kogure K, Busto R, Schwartzman RJ, Scheinberg P (1980) The dissociation of cerebral blood flow, metabolism, and function in the early stages of developing cerebral infarction. Ann Neurol 8: 278-90 (Pubitemid 10018377)
30. Kuhl DE, Phelps ME, Markham CH, Metter EJ, Riege WH, Winter J (1982) Cerebral metabolism and atrophy in Huntington's disease determined by 18FDG and computed tomographic scan. Ann Neurol 12: 425-34 (Pubitemid 12006877)
31. Lei H, Ugurbil K, Chen W (2003) Measurement of unidirectional Pi to ATP flux in human visual cortex at 7 T by using in vivo 31P magnetic resonance spectroscopy. Proc Natl Acad Sci USA 100: 14409-14 (Pubitemid 37499250)
32. Luyten PR, Bruntink G, Sloff FM, Vermeulen JW, van der Heijden JI, den Hollander JA, Heerschap A (1989) Broadband proton decoupling in human 31P NMR spectroscopy. NMR Biomed 1: 177-83
33. Mabe H, Blomqvist P, Siesjo BK (1983) Intracellular pH in the brain following transient ischemia. J Cereb Blood Flow Metab 3: 109-14 (Pubitemid 13129642)
34. Mascalchi M, Lolli F, Della Nave R, Tessa C, Petralli R, Gavazzi C, Politi LS, Macucci M, Filippi M, Piacentini S (2004) Huntington disease: volumetric, diffusionweighted, and magnetization transfer MR imaging of brain. Radiology 232: 867-73 (Pubitemid 39100275)
35. McNamara R, Arias-Mendoza F, Brown TR (1994) Investigation of broad resonances in 31P NMR spectra of the human brain in vivo. NMR Biomed 7: 237-42 (Pubitemid 2144157)
36. Mitsufuji N, Yoshioka H, Tominaga M, Okano S, Nishiki T, Sawada T (1995) Intracellular alkalosis during hypoxia in newborn mouse brain in the presence of systemic acidosis: a phosphorus magnetic resonance spectroscopic study. Brain Dev 17: 256-60
37. Mittoux V, Ouary S, Monville C, Lisovoski F, Poyot T, Conde F, Escartin C, Robichon R, Brouillet E, Peschanski M, Hantraye P (2002) Corticostriatopallidal neuroprotection by adenovirus-mediated ciliary neurotrophic factor gene transfer in a rat model of progressive striatal degeneration. J Neurosci 22: 4478-86 (Pubitemid 37465664)
38. Mochel F, Haller RG (2011) Energy deficit in Huntington disease: why it matters. J Clin Invest 121: 493-9
39. Naressi A, Couturier C, Castang I, de Beer R, Graveron-Demilly D (2001) Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput Biol Med 31: 269-86 (Pubitemid 32378728)
40. Ouary S, Bizat N, Altairac S, Menetrat H, Mittoux V, Conde F, Hantraye P, Brouillet E (2000) Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: implications for neuroprotection studies. Neuroscience 97: 521-30 (Pubitemid 30320758)
41. Petroff OA, Prichard JW (1983) Cerebral pH by NMR. Lancet 2: 105-6
42. Petroff OA, Prichard JW, Behar KL, Alger JR, den Hollander JA, Shulman RG (1985) Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35: 781-8 (Pubitemid 15025280)
43. Powers WJ, Videen TO, Markham J, McGee-Minnich L, Antenor-Dorsey JV, Hershey T, Perlmutter JS (2007) Selective defect of in vivo glycolysis in early Huntington's disease striatum. Proc Natl Acad Sci USA 104: 2945-9 (Pubitemid 46327983)
44. Rango M, Bonifati C, Bresolin N (2006) Parkinson's disease and brain mitochondrial dysfunction: a functional phosphorus magnetic resonance spectroscopy study. J Cereb Blood Flow Metab 26: 283-90 (Pubitemid 43151583)
45. Robertson NJ, Cowan FM, Cox IJ, Edwards AD (2002) Brain alkaline intracellular pH after neonatal encephalopathy. Ann Neurol 52: 732-42 (Pubitemid 35403182)
46. Sappey-Marinier D, Hubesch B, Matson GB, Weiner MW (1992) Decreased phosphorus metabolite concentrations and alkalosis in chronic cerebral infarction. Radiology 182: 29-34
47. Thibaud JL, Wary C, Naulet T, Duteil S, Monnet A, Blot S, Carlier PG (2010) Two pools of inorganic phosphate in canine model of DMD evidenced by phosphorus NMR spectroscopy. In: XII ICNMD, Naples. Acta Myologica 29: 225
48. Huntington Study Group (1996) Unified Huntington's disease rating scale: reliability and consistency. Mov Disord 11: 136-42
49. Van der Grond J, Gerson JR, Laxer KD, Hugg JW, Matson GB, Weiner MW (1998) Regional distribution of interictal 31P metabolic changes in patients with temporal lobe epilepsy. Epilepsia 39: 527-36 (Pubitemid 28221810)
50. Vanhamme L, van den Boogaart A, Van Huffel S (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129: 35-43 (Pubitemid 127454051)
51. Veech RL, Lawson JW, Cornell NW, Krebs HA (1979) Cytosolic phosphorylation potential. J Biol Chem 254: 6538-47
52. Vymazal J, Klempir J, Jech R, Zidovska J, Syka M, Ruzicka E, Roth J (2007) MR relaxometry in Huntington's disease: correlation between imaging, genetic and clinical parameters. J Neurol Sci 263: 20-5 (Pubitemid 350029821)
53. Welch KM, Levine SR, Martin G, Ordidge R, Vande Linde AM, Helpern JA (1992) Magnetic resonance spectroscopy in cerebral ischemia. Neurol Clin 10: 1-29
54. Williams GD, Smith MB (1995) Application of the accurate assessment of intracellular magnesium and pH from the 31P shifts of ATP to cerebral hypoxia-ischemia in neonatal rat. Magn Reson Med 33: 853-7