Chronic hypoxia impairs muscle function in the drosophila model of duchenne's muscular dystrophy (DMD)

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Mosqueira, Matias ^a,c   Willmann, Gabriel ^a,d   Ruohola Baker, Hannele ^b   Khurana, Tejvir S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; HEAT SHOCK PROTEIN;

ALTITUDE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLIMBING; CONTROLLED STUDY; DROSOPHILA; DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION PROFILING; HYPOXIA; IN VIVO STUDY; MUSCLE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEFICIENCY; SIMULATION; STRESS; WILD TYPE; ANIMAL; ANOXIA; CHRONIC DISEASE; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY; POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; VALIDATION STUDY;

ANIMALS; ANOXIA; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DROSOPHILA; GENE EXPRESSION PROFILING; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; POLYMERASE CHAIN REACTION;

EID: 78149433910     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013450     Document Type: Article

References (82)

1. Engel AG, Franzini-Armstrong C (1994) Myology. New York: McGraw-Hill.
2. Hoffman EP, Brown RH, Kunkel LM (1987) Dystrophin: the protein product of the Duchene muscular dystrophy locus. Cell 51: 919-928.
3. Koenig M, Monaco AP, Kunkel LM (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53: 219-226.
4. Bach JR, Ishikawa Y, Kim H (1997) Prevention of pulmonary morbidity for patients with Duchenne muscular dystrophy. Chest 112: 1024-1028.
5. Inkley SR, Oldenburg FC, Vignos PJ, Jr. (1974) Pulmonary function in Duchenne muscular dystrophy related to stage of disease. Am J Med 56: 297-306.
6. Mukoyama M, Kondo K, Hizawa K, Nishitani H (1987) Life spans of Duchenne muscular dystrophy patients in the hospital care program in Japan. J Neurol Sci 81: 155-158.
7. Rideau Y, Gatin G, Bach J, Gines G (1983) Prolongation of life in Duchenne's muscular dystrophy. Acta Neurol (Napoli) 5: 118-124.
8. Beck J, Weinberg J, Hamnegard C-H, Spahija J, Olofson J, et al. (2006) Diaphragmatic function in advanced Duchenne muscular dystrophy. Neuromuscular Disorders 16: 161-167.
9. De Bruin PF, Ueki J, Bush A, Khan Y, Watson A, et al. (1997) Diaphragm thickness and inspiratory strength in patients with Duchenne muscular dystrophy. Thorax 52: 472-475.
10. Liu M, Mineo K, Hanayama K, Fujiwara T, Chino N (2003) Practical problems and management of seating through the clinical stages of Duchenne's muscular dystrophy. Archives of Physical Medicine and Rehabilitation 84: 818-824.
11. De Bruin PF, Ueki J, Bush A, Y Manzur A, Watson A, et al. (2001) Inspiratory flow reserve in boys with Duchenne muscular dystrophy. Pediatric Pulmonology 31: 451-457.
12. Phillips MF, Quinlivan RC, Edwards RH, Calverley PM (2001) Changes in spirometry over time as a prognostic marker in patients with Duchenne muscular dystrophy. Am J Respir Crit Care Med 164: 2191-2194.
13. Chakkalakal JV, Thompson J, Parks RJ, Jasmin BJ (2005) Molecular, cellular, and pharmacological therapies for Duchenne/Becker muscular dystrophies. FASEB J 19: 880-891.
14. Huang X, Poy F, Zhang R, Joachimiak A, Sudol M, et al. (2000) Structure of a WW domain containing fragment of dystrophin in complex with betadystroglycan. Nat Struct Biol 7: 634-638.
15. Greener MJ, Roberts RG (2000) Conservation of components of the dystrophin complex in Drosophila. FEBS Letters 482: 13-18.
16. Apel ED, Roberds SL, Campbell KP, Merlie JP (1995) Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophinassociated glycoprotein complex. Neuron 15: 115-126.
17. Yamada H, Chiba A, Endo T, Kobata A, Anderson LV, et al. (1996) Characterization of dystroglycan-laminin interaction in peripheral nerve. Journal of Neurochemistry 66: 1518-1524.
18. Gee SH, Madhavan R, Levinson SR, Caldwell JH, Sealock R, et al. (1998) Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J Neurosci 18: 128-137.
19. Schultz J, Hoffmuller U, Krause G, Ashurst J, Macias MJ, et al. (1998) Specific interactions between the syntrophin PDZ domain and voltage-gated sodium channels. Nat Struct Biol 5: 19-24.
20. Bredt DS (1999) Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 31: 577-596.
21. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, et al. (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84: 757-767.
22. Grady RM, Grange RW, Lau KS, Maimone MM, Nichol MC, et al. (1999) Role for [alpha]-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies. Nat Cell Biol 1: 215-220.
23. Haycock JW, MacNeil S, Jones P, Harris JB, Mantle D (1996) Oxidative damage to muscle protein in Duchenne muscular dystrophy. Neuroreport 8: 357-361.
24. Sander M, Chavoshan B, Harris SA, Iannaccone ST, Stull JT, et al. (2000) Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. pp 13818-13823.
25. Thomas GD, Sander M, Lau KS, Huang PL, Stull JT, et al. (1998) Impaired metabolic modulation of α-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. pp 15090-15095.
26. Mendell JR, Engel WK, Derrer EC (1971) Duchenne muscular dystrophy: functional ischemia reproduces its characteristic lesions. Science 172: 1143-1145.
27. Parker JM, Mendell JR (1974) Proximal myopathy induced by 5-HTimipramine simulates Duchenne dystrophy. Nature 247: 103-104.
28. Barbe F, Quera-Salva MA, McCann C, Gajdos P, Raphael JC, et al. (1994) Sleep-related respiratory disturbances in patients with Duchenne muscular dystrophy. Eur Respir J 7: 1403-1408.
29. Smith PE, Calverley PM, Edwards RH (1988) Hypoxemia during sleep in Duchenne muscular dystrophy. Am Rev Respir Dis 137: 884-888.
30. Farkas GA, McCormick KM, G LE (2007) Episodic hypoxia exacerbates respiratory muscle dysfunction in DMD(mdx) mice. Muscle & Nerve 36: 708-710.
31. Gosselin LE, Barkley JE, Spencer MJ, McCormick KM, Farkas GA (2003) Ventilatory dysfunction in mdx mice: impact of tumor necrosis factor-alpha deletion. Muscle Nerve 28: 336-343.
32. Ishizaki M, Suga T, Kimura E, Shiota T, Kawano R, et al. (2008) Mdx respiratory impairment following fibrosis of the diaphragm. Neuromuscular Disorders 18: 342-348.
33. Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci U S A 81: 1189-1192.
34. Ryder-Cook AS, Sicinski P, Thomas K, Davies KE, Worton RG, Barnard EA, Darlison MG, Barnard PJ (1988) Localization of the mdx mutation within the mouse dystrophin gene. EMBO J 7: 3017-3021.
35. Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, et al. (1988) The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 334: 154-156.
36. Bassett DI, Currie PD (2003) The zebrafish as a model for muscular dystrophy and congenital myopathy. Hum Mol Genet 12 Spec No 2: R265-270.
37. Bessou C, Giugia JB, Franks CJ, Holden-Dye L, Segalat L (1998) Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission. Neurogenetics 2: 61-72.
38. Neuman S, Kaban A, Volk T, Yaffe D, Nudel U (2001) The dystrophin/ utrophin homologues in Drosophila and in sea urchin. Gene 263: 17-29.
39. Roberts RG, Bobrow M (1998) Dystrophins in vertebrates and invertebrates. Hum Mol Genet 7: 589-595.
40. Shcherbata HR, Yatsenko AS, Patterson L, Sood VD, Nudel U, et al. (2007) Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. Embo J 26: 481-493.
41. van der Plas MC, Pilgram GS, de Jong AW, Bansraj MR, Fradkin LG, et al. (2007) Drosophila Dystrophin is required for integrity of the musculature. Mech Dev. pp 617-630.
42. van der Plas MC, Pilgram GS, Plomp JJ, de Jong A, Fradkin LG, et al. (2006) Dystrophin is required for appropriate retrograde control of neurotransmitter release at the Drosophila neuromuscular junction. J Neurosci 26: 333-344.
43. Jin H, Tan S, Hermanowski J, Bohm S, Pacheco S, et al. (2007) The dystrotelin, dystrophin and dystrobrevin superfamily: new paralogues and old isoforms. BMC Genomics 8: 19.
44. Regulski M, Stasiv Y, Tully T, Enikolopov G (2004) Essential function of nitric oxide synthase in Drosophila. Curr Biol 14: R881-882.
45. Nambu JR, Chen W, Hu S, Crews ST (1996) The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1 alpha and Drosophila single-minded. Gene 172: 249-254.
46. Lavista-Llanos S, Centanin L, Irisarri M, Russo DM, Gleadle JM, et al. (2002) Control of the hypoxic response in Drosophila melanogaster by the basic helixloop- helix PAS protein similar. Mol Cell Biol 22: 6842-6853.
47. Sonnenfeld M, Ward M, Nystrom G, Mosher J, Stahl S, et al. (1997) The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development 124: 4571-4582.
48. Liu G, Roy J, Johnson EA (2006) Identification and function of hypoxiaresponse genes in Drosophila melanogaster. Physiol Genomics 25: 134-141.
49. Gullan PJ, Cranston PS (1994) The insects: an outline of entomology. London; New York: Chapman & Hall. xiv, 491 p.
50. Consoulas C, Theophilidis G (1992) Anatomy, innervation and motor control of the abdominal dorsal muscles of Decticus albifrons (Orthoptera). Journal of Insect Physiology 38: 997-1010.
51. West JB (1996) Prediction of barometric pressures at high altitudes with the use of model atmospheres. J Appl Physiol 81: 1850-1854.
52. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
53. Krishnan SN, Sun Y-A, Mohsenin A, Wyman RJ, Haddad GG (1997) Behavioral and Electrophysiologic Responses of Drosophila melanogaster to Prolonged Periods of Anoxia. Journal of Insect Physiology 43: 203-210.
54. Benzer S (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Natl Acad Sci U S A 58: 1112-1119.
55. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, et al. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A 100: 4078-4083.
56. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
57. Abraham RT (2005) TOR Signaling: An Odyssey from Cellular Stress to the Cell Growth Machinery. Current Biology 15: R139-R141.
58. Horowitz A, Simons M (2008) Branching Morphogenesis. Circ Res 103: 784-795.
59. Reddy BVVG, Irvine KD (2008) The Fat and Warts signaling pathways: new insights into their regulation, mechanism and conservation. Development 135: 2827-2838.
60. Priti A, Gabriel GH (2009) Survival in Acute and Severe Low O2 Environment. Annals of the New York Academy of Sciences 1177: 39-47.
61. Scrable H, Medrano S, Ungewitter E (2009) Running on empty: How p53 controls INS/IGF signaling and affects life span. Experimental Gerontology 44: 93-100.
62. Fradkin LG, Baines MC, Noordermeer JN (2008) The dystrophin Dp186 isoform regulates neurotransmitter release at a central synapse in Drosophila. J Neurosci 28: 5105-5114.
63. Huang H, Haddad GG (2007) Drosophila dMRP4 regulates responsiveness to O2 deprivation and development under hypoxia. Physiol Genomics 29: 260-266.
64. Zhou D, Xue J, Chen J, Morcillo P, Lambert JD, et al. (2007) Experimental selection for Drosophila survival in extremely low O2 environment. PLoS ONE 2: e490.
65. Baird NA, Turnbull DW, Johnson EA (2006) Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxiainducible factor-1. J Biol Chem 281: 38675-38681.
66. Pelham HR (1982) A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 30: 517-528.
67. Orosz A, Wisniewski J, Wu C (1996) Regulation of Drosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization. Mol Cell Biol 16: 7018-7030.
68. Snoeckx LH, Cornelussen RN, Van Nieuwenhoven FA, Reneman RS, Van Der Vusse GJ (2001) Heat shock proteins and cardiovascular pathophysiology. Physiol Rev 81: 1461-1497.
69. Michaud S, Marin R, Tanguay RM (1997) Regulation of heat shock gene induction and expression during Drosophila development. Cellular and Molecular Life Sciences (CMLS) 53: 104-113.
70. Azad P, Zhou D, Russo E, Haddad GG (2009) Distinct Mechanisms Underlying Tolerance to Intermittent and Constant Hypoxia in Drosophila melanogaster. PLoS ONE 4: e5371.
71. Bornman L, Polla BS, Gericke GS (1996) Heat-shock protein 90 and ubiquitin: developmental regulation during myogenesis. Muscle Nerve 19: 574-580.
72. Bornman L, Polla BS, Lotz BP, Gericke GS (1995) Expression of heat-shock/stress proteins in Duchenne muscular dystrophy. Muscle Nerve 18: 23-31.
73. Doran P, Martin G, Dowling P, Jockusch H, Ohlendieck K (2006) Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 6: 4610-4621.
74. Lundby C, Calbet JA, Robach P (2009) The response of human skeletal muscle tissue to hypoxia. Cell Mol Life Sci 66: 3615-3623.
75. West JB (2000) The physiologival challenge of climbing Mt. Everest. Annals of the New York Academy of Sciences 899: 15-27.
76. West JB (2003) George I. Finch and his pioneering use of oxygen for climbing at extreme altitudes. J Appl Physiol 94: 1702-1713.
77. Bailey DD, Bruce (1997) Physiological implications of altitude training for endurance performance at sea level: a review. British Journal of Sport Medicine 31: 183-190.
78. Brutsaert T (2008) Do high-altitude natives have enhanced exercise performance at altitude? Applied Physiology Nutritional and Metabolism 33: 582-592.
79. Askew EW (2002) Work at high altitude and oxidative stress: antioxidant nutrients. Toxicology 180: 107-119.
80. Ouarda T-L, Takeshi A, Grant H, Uri N, David Y, et al. (2008) Dystrophin deficiency in Drosophila reduces lifespan and causes a dilated cardiomyopathy phenotype. Aging Cell 7: 237-249.
81. Slama K (1988) A New Look at Insect Respiration. Biol Bull 175: 289-300.
82. Bradley TJ (2008) Control of the Respiratory Pattern in Insects. Hypoxia And The Circulation. pp 211-220.