Splitting of Pi and other 31P NMR anomalies of skeletal muscle metabolites in canine muscular dystrophy

NMR in Biomedicine

Volumn 25, Issue 10, 2012, Pages 1160-1169

  Wary, Claire ^a,b,c   Naulet, Thibaud ^a,b,c   Thibaud, Jean Laurent ^a,d   Monnet, Aurélien ^a,b,c   Blot, Stéphane ^d   Carlier, Pierre G ^a,b,c  

^a Institute of Myology   (France)

^b SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

DMD; Duchenne Muscular Dystrophy; GRMD; Inorganic phosphate; Magnetisation transfer; Phosphodiesters; Spectroscopy

Indexed keywords

DMD; GRMD; INORGANIC PHOSPHATES; MUSCULAR DYSTROPHY; PHOSPHODIESTERS;

ENZYME ACTIVITY; ESTERS; MAGNETIZATION; MUSCLE; NEUROMUSCULAR REHABILITATION; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; SPECTROSCOPY;

ALKALINITY;

CREATINE PHOSPHATE; DIESTER; ESTER DERIVATIVE; PHOSPHATE; PHOSPHOMONOESTER; UNCLASSIFIED DRUG; PHOSPHORUS;

AGE; ANIMAL EXPERIMENT; ARTICLE; BICEPS BRACHII MUSCLE; CONTROLLED STUDY; DOG DISEASE; DUCHENNE MUSCULAR DYSTROPHY; GOLDEN RETRIEVER MUSCULAR DYSTROPHY; MALE; NONHUMAN; PH; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; TIBIA; ANIMAL; ANIMAL MUSCULAR DYSTROPHY; DOG; MAGNETISM; METABOLISM; METABOLOME; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; REST; SKELETAL MUSCLE;

ANIMALIA; CANIS FAMILIARIS;

ANIMALS; DOGS; MAGNETIC PHENOMENA; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; PHOSPHATES; PHOSPHORUS ISOTOPES; REST;

EID: 84866267986     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2785     Document Type: Article

References (67)

1. Pichavant C, Aartsma-Rus A, Clemens PR, Davies KE, Dickson G, Takeda S, Wilton SD, Wolff JA, Wooddell CI, Xiao X, Tremblay JP. Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol. Ther. 2011; 19: 830-840.
2. Edwards RH, Dawson MJ, Wilkie DR, Gordon RE, Shaw D. Clinical use of nuclear magnetic resonance in the investigation of myopathy. Lancet 1982; 1: 725-731.
3. Newman RJ, Bore PJ, Chan L, Gadian DG, Styles P, Taylor D, Radda GK. Nuclear magnetic resonance studies of forearm muscle in Duchenne dystrophy. Br. Med. J. (Clin. Res. Ed.). 1982; 284: 1072-1074.
4. Argov Z, Maris J, Damico L. In vivo phosphorus nuclear magnetic resonance (31P-NMR) study of dystrophic hamster muscle. J. Neurol. Sci. 1988; 86: 185-193.
5. Cole MA, Rafael JA, Taylor DJ, Lodi R, Davies KE, Styles P. A quantitative study of bioenergetics in skeletal muscle lacking utrophin and dystrophin. Neuromuscul. Disord. 2002; 12: 247-257.
6. Dunn JF, Bannister N, Kemp GJ, Publicover SJ. Sodium is elevated in mdx muscles: ionic interactions in dystrophic cells. J. Neurol. Sci. 1993; 114: 76-80.
7. McCully K, Giger U, Argov Z, Valentine B, Cooper B, Chance B, Bank W. Canine X-linked muscular dystrophy studied with in vivo phosphorus magnetic resonance spectroscopy. Muscle Nerve 1991; 14: 1091-1098.
8. Griffiths RD, Cady EB, Edwards RH, Wilkie DR. Muscle energy metabolism in Duchenne dystrophy studied by 31P-NMR: controlled trials show no effect of allopurinol or ribose. Muscle Nerve 1985; 8: 760-767.
9. Younkin DP, Berman P, Sladky J, Chee C, Bank W, Chance B. 31P NMR studies in Duchenne muscular dystrophy: age-related metabolic changes. Neurology 1987; 37: 165-169.
10. Banerjee B, Sharma U, Balasubramanian K, Kalaivani M, Kalra V, Jagannathan NR. Effect of creatine monohydrate in improving cellular energetics and muscle strength in ambulatory Duchenne muscular dystrophy patients: a randomized, placebo-controlled 31P MRS study. Magn. Reson. Imaging 2010; 28: 698-707.
11. Barbiroli B, Funicello R, Iotti S, Montagna P, Ferlini A, Zaniol P. 31P-NMR spectroscopy of skeletal muscle in Becker dystrophy and DMD/BMD carriers. Altered rate of phosphate transport. J. Neurol. Sci. 1992; 109: 188-195.
12. Barbiroli B, McCully KK, Iotti S, Lodi R, Zaniol P, Chance B. Further impairment of muscle phosphate kinetics by lengthening exercise in DMD/BMD carriers. An in vivo 31P-NMR spectroscopy study. J. Neurol. Sci. 1993; 119: 65-73.
13. Kemp GJ, Taylor DJ, Dunn JF, Frostick SP, Radda GK. Cellular energetics of dystrophic muscle. J. Neurol. Sci. 1993; 116: 201-206.
14. Argov Z, Lofberg M, Arnold DL. Insights into muscle diseases gained by phosphorus magnetic resonance spectroscopy. Muscle Nerve 2000; 23: 1316-1334.
15. Valentine BA, Cooper BJ, de Lahunta A, O'Quinn R, Blue JT. Canine X-linked muscular dystrophy. An animal model of Duchenne muscular dystrophy: clinical studies. J. Neurol. Sci. 1988; 88: 69-81.
16. Willmann R, Possekel S, Dubach-Powell J, Meier T, Ruegg MA. Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul. Disord. 2009;19:241-249.
17. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993;29:804-811.
18. Forsen S, Hoffman RA. Study of Moderately Rapid Chemical Exchange Reactions by Means of Nuclear Magnetic Double Resonance. J. Chem. Phys. 1963; 39: 2892-2901.
19. Horska A, Spencer GS. Correctly accounting for radiofrequency spillover in saturation transfer experiments: application to measurement of the creatine kinase reaction rate in human forearm muscle. MAGMA 1997; 5: 159-163.
20. Cerdan S, Subramanian VH, Hilberman M, Cone J, Egan J, Chance B, Williamson JR. 31P NMR detection of mobile dog brain phospholipids. Magn. Reson. Med. 1986; 3: 432-439.
21. Murphy EJ, Rajagopalan B, Brindle KM, Radda GK. Phospholipid bilayer contribution to 31P NMR spectra in vivo. Magn. Reson. Med. 1989; 12: 282-289.
22. McNamara R, Arias-Mendoza F, Brown TR. Investigation of broad resonances in 31P NMR spectra of the human brain in vivo. NMR Biomed. 1994; 7: 237-242.
23. Taylor DJ, Bore PJ, Styles P, Gadian DG, Radda GK. Bioenergetics of intact human muscle. A 31P nuclear magnetic resonance study. Mol. Biol. Med. 1983; 1: 77-94.
24. Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J. Magn. Reson. 1997; 129: 35-43.
25. Stefan D, Di Cesare F, Andrasescu A, Popa E, Lazariev A, Vescovo E, Strbak O, Williams S, Starcuk Z, Cabanas M, van Ormondt D, Graveron-Demilly D. Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Measurement Sci. Technol. 2009; 20: 1-9.
26. Kan HE, Klomp DW, Wong CS, Boer VO, Webb AG, Luijten PR, Jeneson JA. In vivo 31P MRS detection of an alkaline inorganic phosphate pool with short T1 in human resting skeletal muscle. NMR Biomed. 2010; 23: 995-1000.
27. Samaha FJ, Davis B, Nagy B. Duchenne muscular dystrophy: adenosine triphosphate and creatine phosphate content in muscle. Neurology 1981; 31: 916-919.
28. Harris RC, Hultman E, Nordesjo LO. Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand. J. Clin. Lab. Invest. 1974; 33: 109-120.
29. Buchthal SD, Thoma WJ, Taylor JS, Nelson SJ, Brown TR. In vivo T1 values of phosphorus metabolites in human liver and muscle determined at 1.5T by chemical shift imaging. NMR Biomed. 1989; 2: 298-304.
30. Goudemant JF, Francaux M, Mottet I, Demeure R, Sibomana M, Sturbois X. 31P NMR saturation transfer study of the creatine kinase reaction in human skeletal muscle at rest and during exercise. Magn. Reson. Med. 1997; 37: 744-753.
31. van den Broek NM, Ciapaite J, Nicolay K, Prompers JJ. Comparison of in vivo postexercise phosphocreatine recovery and resting ATP synthesis flux for the assessment of skeletal muscle mitochondrial function. Am. J. Physiol. Cell Physiol. 2010; 299: C1136-C1143.
32. De Levie R. Advanced Excel for scientific data analysis. Oxford University Press: New-York; 2004.
33. Heerschap A, Bergman AH, van Vaals JJ, Wirtz P, Loermans HM, Veerkamp JH. Alterations in relative phosphocreatine concentrations in preclinical mouse muscular dystrophy revealed by in vivo NMR. NMR Biomed. 1988; 1: 27-31.
34. Ruiz-Cabello J, Cohen JS. Phospholipid metabolites as indicators of cancer cell function. NMR Biomed. 1992; 5: 226-233.
35. Lowry M, Porter DA, Twelves CJ, Heasley PE, Smith MA, Richards MA. Visibility of phospholipids in 31P NMR spectra of human breast tumours in vivo. NMR Biomed. 1992; 5: 37-42.
36. Kilby PM, Bolas NM, Radda GK. 31P-NMR study of brain phospholipid structures in vivo. Biochim. Biophys. Acta 1991; 1085: 257-264.
37. Satrustegui J, Berkowitz H, Boden B, Donlon E, McLaughlin A, Maris J, Warnell R, Chance B. An in vivo phosphorus nuclear magnetic resonance study of the variations with age in the phosphodiester content of human muscle. Mech. Ageing Dev. 1988; 42: 105-114.
38. Chalovich JM, Burt CT, Danon MJ, Glonek T, Barany M. Phosphodiesters in muscular dystrophies. Ann. N. Y. Acad. Sci. 1979; 317: 649-669.
39. Ozawa E, Hagiwara Y, Yoshida M. Creatine kinase, cell membrane and Duchenne muscular dystrophy. Mol. Cell. Biochem. 1999; 190: 143-151.
40. Bates TE, Williams SR, Gadian DG. Phosphodiesters in the liver: the effect of field strength on the 31P signal. Magn. Reson. Med. 1989; 12: 145-150.
41. Burt CT, Glonek T, Barany M. Phosphorus-31 nuclear magnetic resonance detection of unexpected phosphodiesters in muscle. Biochemistry 1976; 15: 4850-4853.
42. Burt CT, Pluskal MG, Sreter FA. Generation of phosphodiesters during fast-to-slow muscle transformation. A 31P-NMR study. Biochim. Biophys. Acta 1982; 721: 492-494.
43. Bernus G, Gonzalez de Suso JM, Alonso J, Martin PA, Prat JA, Arus C. 31P-MRS of quadriceps reveals quantitative differences between sprinters and long-distance runners. Med. Sci. Sports Exerc. 1993; 25: 479-484.
44. Hug F, Grelot L, Le Fur Y, Cozzone PJ, Bendahan D. Recovery kinetics throughout successive bouts of various exercises in elite cyclists. Med. Sci. Sports Exerc. 2006; 38: 2151-2158.
45. Argov Z, Renshaw PF, Boden B, Winokur A, Bank WJ. Effects of thyroid hormones on skeletal muscle bioenergetics. In vivo phosphorus-31 magnetic resonance spectroscopy study of humans and rats. J. Clin. Invest. 1988; 81: 1695-1701.
46. Khushu S, Rana P, Sekhri T, Sripathy G, Tripathi RP. Bio-energetic impairment in human calf muscle in thyroid disorders: a 31P MRS study. Magn. Reson. Imaging 2010; 28: 683-689.
47. Webster C, Silberstein L, Hays AP, Blau HM. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 1988; 52: 503-513.
48. Lanfossi M, Cozzi F, Bugini D, Colombo S, Scarpa P, Morandi L, Galbiati S, Cornelio F, Pozza O, Mora M. Development of muscle pathology in canine X-linked muscular dystrophy. I. Delayed postnatal maturation of affected and normal muscle as revealed by myosin isoform analysis and utrophin expression. Acta Neuropathol. 1999; 97: 127-138.
49. Schunk K, Pitton M, Duber C, Kersjes W, Schadmand-Fischer S, Thelen M. Dynamic phosphorus-31 magnetic resonance spectroscopy of the quadriceps muscle: effects of age and sex on spectroscopic results. Invest. Radiol. 1999; 34: 116-125.
50. Taylor DJ, Kemp GJ, Thompson CH, Radda GK. Ageing: effects on oxidative function of skeletal muscle in vivo. Mol. Cell. Biochem. 1997; 174: 321-324.
51. Burt CT, Ribolow HJ. A hypothesis: noncyclic phosphodiesters may play a role in membrane control. Biochem. Med. 1984; 31: 21-30.
52. Fallbrook A, Turenne SD, Mamalias N, Kish SJ, Ross BM. Phosphatidylcholine and phosphatidylethanolamine metabolites may regulate brain phospholipid catabolism via inhibition of lysophospholipase activity. Brain Res. 1999; 834: 207-210.
53. Takahashi H, Kuno SY, Katsuta S, Shimojo H, Masuda K, Yoshioka H, Anno I, Itai Y. Relationships between fiber composition and NMR measurements in human skeletal muscle. NMR Biomed. 1996; 9: 8-12.
54. Dunn JF, Frostick S, Brown G, Radda GK. Energy status of cells lacking dystrophin: an in vivo/in vitro study of mdx mouse skeletal muscle. Biochim. Biophys. Acta 1991; 1096: 115-120.
55. Lodi R, Kemp GJ, Muntoni F, Thompson CH, Rae C, Taylor J, Styles P, Taylor DJ. Reduced cytosolic acidification during exercise suggests defective glycolytic activity in skeletal muscle of patients with Becker muscular dystrophy. An in vivo 31P magnetic resonance spectroscopy study. Brain 1999; 122 (Pt 1): 121-130.
56. Kemp GJ. The interpretation of abnormal 31P magnetic resonance saturation transfer measurements of Pi/ATP exchange in insulin-resistant skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2008; 294: E640-E642; author reply E643-644.
57. Sharma U, Atri S, Sharma MC, Sarkar C, Jagannathan NR. Skeletal muscle metabolism in Duchenne muscular dystrophy (DMD): an in-vitro proton NMR spectroscopy study. Magn. Reson. Imaging 2003; 21: 145-153.
58. Wehling-Henricks M, Oltmann M, Rinaldi C, Myung KH, Tidball JG. Loss of positive allosteric interactions between neuronal nitric oxide synthase and phosphofructokinase contributes to defects in glycolysis and increased fatigability in muscular dystrophy. Hum. Mol. Genet. 2009; 18: 3439-3451.
59. Newcomer BR, Boska MD. T1 measurements of 31P metabolites in resting and exercising human gastrocnemius/soleus muscle at 1.5 Tesla. Magn. Reson. Med. 1999; 41: 486-494.
60. Kushmerick MJ, Moerland TS, Wiseman RW. Mammalian skeletal muscle fibers distinguished by contents of phosphocreatine, ATP, and Pi. Proc Natl. Acad. Sc. U. S. A. 1992; 89: 7521-7525.
61. Dufour S, Thiaudiere E, Vidal G, Gallis JL, Rousse N, Canioni P. Temperature dependence of NMR relaxation times of nucleoside triphosphates and inorganic phosphate in the isolated perfused rat liver. Effect on Pi compartmentation. J. Magn. Reson. B 1996; 113: 125-135.
62. Garlick PB, Brown TR, Sullivan RH, Ugurbil K. Observation of a second phosphate pool in the perfused heart by 31P NMR; is this the mitochondrial phosphate? J. Mol. Cell. Cardiol. 1983; 15: 855-858.
63. Schmidt O, Bunse M, Dietze GJ, Lutz O, Jung WI. Unveiling extracellular inorganic phosphate signals from blood in human cardiac 31P NMR spectra. J. Cardiovasc. Magn. Reson. 2001; 3: 325-329.
64. Matsuda R, Nishikawa A, Tanaka H. Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem. 1995; 118: 959-964.
65. Lotz BP, Engel AG. Are hypercontracted muscle fibers artifacts and do they cause rupture of the plasma membrane? Neurology 1987; 37: 1466-1475.
66. Roth SM, Martel GF, Rogers MA. Muscle biopsy and muscle fiber hypercontraction: a brief review. Eur. J. Appl. Physiol. 2000; 83: 239-245.
67. Thibaud JL, Monnet A, Bertoldi D, Barthelemy I, Blot S, Carlier PG. Characterization of dystrophic muscle in golden retriever muscular dystrophy dogs by nuclear magnetic resonance imaging. Neuromuscul. Disord. 2007; 17: 575-584.