Role of dystrophin in airway smooth muscle phenotype, contraction and lung function

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Sharma, Pawan ^a,b,c   Basu, Sujata ^a,b   Mitchell, Richard W ^a,b   Stelmack, Gerald L ^a,b   Anderson, Judy E ^a   Halayko, Andrew J ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b MANITOBA INSTITUTE OF CHILD HEALTH   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALPONIN; DYSTROPHIN; GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN TARGET OF RAPAMYCIN; METHACHOLINE; MYOSIN HEAVY CHAIN; PHOSPHATIDYLINOSITOL 3 KINASE; METHACHOLINE CHLORIDE;

ACTIN FILAMENT; AIRWAY CONSTRICTION; AIRWAY RESISTANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MATURATION; CONTROLLED STUDY; EX VIVO STUDY; GOLDEN RETRIEVER; IN VITRO STUDY; IN VIVO STUDY; LUNG FUNCTION; MOUSE; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE CONTRACTION; STRESS FIBER; TRACHEA MUSCLE; ANIMAL; CELL CULTURE; CYTOLOGY; DEFICIENCY; DOG; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LUNG; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; RESPIRATORY SYSTEM; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; TRACHEA; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DOGS; DYSTROPHIN; IMMUNOHISTOCHEMISTRY; LUNG; METHACHOLINE CHLORIDE; MICE, INBRED MDX; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; MYOSIN HEAVY CHAINS; PHOSPHATIDYLINOSITOL 3-KINASES; RESPIRATORY SYSTEM; SIGNAL TRANSDUCTION; TRACHEA;

EID: 84904680018     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102737     Document Type: Article

References (89)

1. Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
2. Muntoni F, Torelli S, Ferlini A (2003) Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet neurology 2: 731-740. (Pubitemid 37443515)
3. Lapidos KA, Kakkar R, McNally EM (2004) The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 94: 1023-1031. (Pubitemid 38579696)
4. Ervasti JM (2007) Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochimica et biophysica acta 1772: 108-117.
5. North AJ, Galazkiewicz B, Byers TJ, Glenney JR Jr, Small JV (1993) Complementary distributions of vinculin and dystrophin define two distinct sarcolemma domains in smooth muscle. J Cell Biol 120: 1159-1167.
6. Halayko AJ, Stelmack GL (2005) The association of caveolae, actin, and the dystrophin-glycoprotein complex: a role in smooth muscle phenotype and function? Can J Physiol Pharmacol 83: 877-891. (Pubitemid 43235413)
7. Sharma P, Tran T, Stelmack GL, McNeill K, Gosens R, et al. (2008) Expression of the dystrophin-glycoprotein complex is a marker for human airway smooth muscle phenotype maturation. Am J Physiol Lung Cell Mol Physiol 294: L57-68. (Pubitemid 351380318)
8. Chamberlain JS (1991) Duchenne muscular dystrophy. Current opinion in genetics & development 1: 11-14.
9. Emery AE (1990) Dystrophin function. Lancet 335: 1289.
10. Mokri B, Engel AG (1998) Duchenne dystrophy: electron microscopic findings pointing to a basic or early abnormality in the plasma membrane of the muscle fiber. 1975. Neurology 51: 1 and 10 pages following.
11. Rowland LP (1976) Pathogenesis of muscular dystrophies. Archives of neurology 33: 315-321.
12. Bradley WG, Fulthorpe JJ (1978) Studies of sarcolemmal integrity in myopathic muscle. Neurology 28: 670-677. (Pubitemid 8364272)
13. Straub V, Campbell KP (1997) Muscular dystrophies and the dystrophinglycoprotein complex. Curr Opin Neurol 10: 168-175.
14. Barohn RJ, Levine EJ, Olson JO, Mendell JR (1988) Gastric hypomotility in Duchenne's muscular dystrophy. N Engl J Med 319: 15-18.
15. Jaffe KM, McDonald CM, Ingman E, Haas J (1990) Symptoms of upper gastrointestinal dysfunction in Duchenne muscular dystrophy: case-control study. Arch Phys Med Rehabil 71: 742-744. (Pubitemid 20283084)
16. Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proceedings of the National Academy of Sciences of the United States of America 81: 1189-1192. (Pubitemid 14171480)
17. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, et al. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580. (Pubitemid 19189735)
18. Pastoret C, Sebille A (1995) mdx mice show progressive weakness and muscle deterioration with age. Journal of the neurological sciences 129: 97-105.
19. Pastoret C, Sebille A (1995) Age-related differences in regeneration of dystrophic (mdx) and normal muscle in the mouse. Muscle & nerve 18: 1147-1154.
20. Lynch GS, Hinkle RT, Chamberlain JS, Brooks SV, Faulkner JA (2001) Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. The Journal of physiology 535: 591-600. (Pubitemid 32825693)
21. Coulton GR, Curtin NA, Morgan JE, Partridge TA (1988) The mdx mouse skeletal muscle myopathy: II. Contractile properties. Neuropathology and applied neurobiology 14: 299-314.
22. Dangain J, Vrbova G (1984) Muscle development in mdx mutant mice. Muscle & nerve 7: 700-704. (Pubitemid 15209285)
23. 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.
24. Valentine BA, Winand NJ, Pradhan D, Moise NS, de Lahunta A, et al. (1992) Canine X-linked muscular dystrophy as an animal model of Duchenne muscular dystrophy: a review. American journal of medical genetics 42: 352-356.
25. Childers MK, Okamura CS, Bogan DJ, Bogan JR, Petroski GF, et al. (2002) Eccentric contraction injury in dystrophic canine muscle. Archives of physical medicine and rehabilitation 83: 1572-1578. (Pubitemid 35304136)
26. Childers MK, Staley JT, Kornegay JN, McDonald KS (2005) Skinned single fibers from normal and dystrophin-deficient dogs incur comparable stretch-induced force deficits. Muscle & nerve 31: 768-771. (Pubitemid 40734687)
27. Kornegay JN, Bogan JR, Bogan DJ, Childers MK, Grange RW (2011) Golden retriever muscular dystrophy (GRMD): Developing and maintaining a colony and physiological functional measurements. Methods in molecular biology 709: 105-123.
28. Kornegay JN, Tuler SM, Miller DM, Levesque DC (1988) Muscular dystrophy in a litter of golden retriever dogs. Muscle & nerve 11: 1056-1064.
29. Carpenter JL, Hoffman EP, Romanul FC, Kunkel LM, Rosales RK, et al. (1989) Feline muscular dystrophy with dystrophin deficiency. The American journal of pathology 135: 909-919. (Pubitemid 20009501)
30. Cooper BJ (1989) Animal models of Duchenne and Becker muscular dystrophy. British medical bulletin 45: 703-718.
31. Cooper BJ, Valentine BA, Wilson S, Patterson DF, Concannon PW (1988) Canine muscular dystrophy: confirmation of X-linked inheritance. The Journal of heredity 79: 405-408. (Pubitemid 19022078)
32. Winand NJ, Edwards M, Pradhan D, Berian CA, Cooper BJ (1994) Deletion of the dystrophin muscle promoter in feline muscular dystrophy. Neuromuscular disorders: NMD 4: 433-445. (Pubitemid 24331530)
33. Bloch RJ, Gonzalez-Serratos H (2003) Lateral force transmission across costameres in skeletal muscle. Exercise and sport sciences reviews 31: 73-78. (Pubitemid 36443764)
34. Ervasti JM (2003) Costameres: the Achilles' heel of Herculean muscle. The Journal of biological chemistry 278: 13591-13594.
35. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, et al. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90: 729-738. (Pubitemid 27357964)
36. Brooks SV (1998) Rapid recovery following contraction-induced injury to in situ skeletal muscles in mdx mice. Journal of muscle research and cell motility 19: 179-187.
37. Dellorusso C, Crawford RW, Chamberlain JS, Brooks SV (2001) Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. Journal of muscle research and cell motility 22: 467-475. (Pubitemid 34264077)
38. Faulkner JA, Ng R, Davis CS, Li S, Chamberlain JS (2008) Diaphragm muscle strip preparation for evaluation of gene therapies in mdx mice. Clinical and experimental pharmacology & physiology 35: 725-729. (Pubitemid 351725232)
39. Moens P, Baatsen PH, Marechal G (1993) Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. Journal of muscle research and cell motility 14: 446-451. (Pubitemid 23267492)
40. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proceedings of the National Academy of Sciences of the United States of America 90: 3710-3714. (Pubitemid 23111437)
41. Nguyen F, Cherel Y, Guigand L, Goubault-Leroux I, Wyers M (2002) Muscle lesions associated with dystrophin deficiency in neonatal golden retriever puppies. Journal of comparative pathology 126: 100-108.
42. Turgeman T, Hagai Y, Huebner K, Jassal DS, Anderson JE, et al. (2008) Prevention of muscle fibrosis and improvement in muscle performance in the mdx mouse by halofuginone. Neuromuscular disorders: NMD 18: 857-868.
43. Huebner KD, Jassal DS, Halevy O, Pines M, Anderson JE (2008) Functional resolution of fibrosis in mdx mouse dystrophic heart and skeletal muscle by halofuginone. American journal of physiology Heart and circulatory physiology 294: H1550-1561. (Pubitemid 351490584)
44. Naureckas ET, Ndukwu IM, Halayko AJ, Maxwell C, Hershenson MB, et al. (1999) Bronchoalveolar lavage fluid from asthmatic subjects is mitogenic for human airway smooth muscle. Am J Respir Crit Care Med 160: 2062-2066. (Pubitemid 30004719)
45. Halayko AJ, Camoretti-Mercado B, Forsythe SM, Vieira JE, Mitchell RW, et al. (1999) Divergent differentiation paths in airway smooth muscle culture: induction of functionally contractile myocytes. Am J Physiol 276: L197-206. (Pubitemid 29061681)
46. Sharma P, Ghavami S, Stelmack GL, McNeill KD, Mutawe MM, et al. (2010) beta-Dystroglycan binds caveolin-1 in smooth muscle: a functional role in caveolae distribution and Ca2+ release. J Cell Sci 123: 3061-3070.
47. Gosens R, Stelmack GL, Dueck G, Mutawe MM, Hinton M, et al. (2007) Caveolae facilitate muscarinic receptor-mediated intracellular Ca2+ mobilization and contraction in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 293: L1406-1418. (Pubitemid 350255023)
48. Mitchell RW, Halayko AJ, Kahraman S, Solway J, Wylam ME (2000) Selective restoration of calcium coupling to muscarinic M(3) receptors in contractile cultured airway myocytes. Am J Physiol Lung Cell Mol Physiol 278: L1091-1100. (Pubitemid 30351067)
49. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450. (Pubitemid 15114340)
50. Sharma P, Ryu MH, Basu S, Maltby SA, Yeganeh B, et al. (2012) Epithelium-dependent modulation of responsiveness of airways from caveolin-1 knockout mice is mediated through cyclooxygenase-2 and 5-lipoxygenase. British Journal of Pharmacology.
51. Sharma P, Ghavami S, Stelmack GL, McNeill KD, Mutawe MM, et al. (2010) The Dystrophin Glycoprotein Complex (DGC) Regulates Spatial Organization And Function Of Caveolae In Human Airway Smooth Muscle Cells. Am J of Respir Crit Care Med 181: A5294.
52. Kadkhoda K, Wang S, Fan Y, Qiu H, Basu S, et al. (2011) ICOS ligand expression is essential for allergic airway hyperresponsiveness. Int Immunol 23: 239-249.
53. Ma Y, Halayko AJ, Basu S, Guan Q, Weiss CR, et al. (2013) Sustained suppression of IL-13 by a vaccine attenuates airway inflammation and remodeling in mice. Am J Respir Cell Mol Biol 48: 540-549.
54. McGovern TK, Robichaud A, Fereydoonzad L, Schuessler TF, Martin JG (2013) Evaluation of respiratory system mechanics in mice using the forced oscillation technique. J Vis Exp: e50172.
55. Halayko AJ, Stelmack GL, Yamasaki A, McNeill K, Unruh H, et al. (2005) Distribution of phenotypically disparate myocyte subpopulations in airway smooth muscle. Can J Physiol Pharmacol 83: 104-116. (Pubitemid 40754782)
56. Halayko AJ, Kartha S, Stelmack GL, McConville J, Tam J, et al. (2004) Phophatidylinositol-3 kinase/mammalian target of rapamycin/p70S6K regulates contractile protein accumulation in airway myocyte differentiation. Am J Respir Cell Mol Biol 31: 266-275. (Pubitemid 39180295)
57. Tran T, Ens-Blackie K, Rector ES, Stelmack GL, McNeill KD, et al. (2007) Laminin-binding integrin alpha7 is required for contractile phenotype expression by human airway myocytes. Am J Respir Cell Mol Biol 37: 668-680. (Pubitemid 350211637)
58. Halayko AJ, Solway J (2001) Molecular mechanisms of phenotypic plasticity in smooth muscle cells. J Appl Physiol 90: 358-368. (Pubitemid 32038538)
59. Owens GK (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487-517.
60. Zhou L, Goldsmith AM, Bentley JK, Jia Y, Rodriguez ML, et al. (2005) 4E-binding protein phosphorylation and eukaryotic initiation factor-4E release are required for airway smooth muscle hypertrophy. Am J Respir Cell Mol Biol 33: 195-202. (Pubitemid 41473057)
61. Darby PJ, Kwan CY, Daniel EE (2000) Caveolae from canine airway smooth muscle contain the necessary components for a role in Ca(2+) handling. Am J Physiol Lung Cell Mol Physiol 279: L1226-1235. (Pubitemid 32009509)
62. Fujimoto T (1993) Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol 120: 1147-1157.
63. Fujimoto T, Nakade S, Miyawaki A, Mikoshiba K, Ogawa K (1992) Localization of inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae. The Journal of cell biology 119: 1507-1513.
64. Gosens R, Stelmack GL, Bos ST, Dueck G, Mutawe MM, et al. (2010) Caveolin-1 is Required for Contractile Phenotype Expression by Airway Smooth Muscle Cells. J Cell Mol Med.
65. Prakash YS, Thompson MA, Vaa B, Matabdin I, Peterson TE, et al. (2007) Caveolins and intracellular calcium regulation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 293: L1118-1126. (Pubitemid 350159396)
66. Gabella G (1984) Structural apparatus for force transmission in smooth muscles. Physiol Rev 64: 455-477.
67. Montesano R (1979) Inhomogeneous distribution of filipin-sterol complexes in smooth-muscle cell plasma-membrane. Nature 280: 328-329.
68. Small JV (1985) Geometry of actin-membrane attachments in the smooth muscle cell: the localisations of vinculin and alpha-actinin. EMBO J 4: 45-49.
69. Small JV, Gimona M (1998) The cytoskeleton of the vertebrate smooth muscle cell. Acta Physiologica Scandinavica 164: 341-348. (Pubitemid 29015653)
70. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, et al. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019. (Pubitemid 34428747)
71. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, et al. (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013. (Pubitemid 34428746)
72. Gordon BS, Lowe DA, Kostek MC (2014) Exercise increases utrophin protein expression in the mdx mouse model of Duchenne muscular dystrophy. Muscle Nerve 49: 915-918.
73. Perkins KJ, Davies KE (2002) The role of utrophin in the potential therapy of Duchenne muscular dystrophy. Neuromuscul Disord 12 Suppl 1: S78-89. (Pubitemid 36158777)
74. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, et al. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4: 1441-1444. (Pubitemid 28553471)
75. Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823. (Pubitemid 23241091)
76. Dye WW, Gleason RL, Wilson E, Humphrey JD (2007) Altered biomechanical properties of carotid arteries in two mouse models of muscular dystrophy. J Appl Physiol 103: 664-672. (Pubitemid 47204987)
77. Mancinelli R, Tonali P, Romani R, Tringali A, Vargiu R, et al. (1999) Mechanical properties of smooth muscle portal vein in normal and dystrophin-deficient (mdx) mice. Exp Physiol 84: 929-940. (Pubitemid 29465709)
78. Ito K, Kimura S, Ozasa S, Matsukura M, Ikezawa M, et al. (2006) Smooth muscle-specific dystrophin expression improves aberrant vasoregulation in mdx mice. Hum Mol Genet 15: 2266-2275. (Pubitemid 43985517)
79. Morel JL, Rakotoarisoa L, Jeyakumar LH, Fleischer S, Mironneau C, et al. (2004) Decreased expression of ryanodine receptors alters calcium-induced calcium release mechanism in mdx duodenal myocytes. J Biol Chem 279: 21287-21293. (Pubitemid 38656535)
80. Cohn RD, Durbeej M, Moore SA, Coral-Vazquez R, Prouty S, et al. (2001) Prevention of cardiomyopathy in mouse models lacking the smooth muscle sarcoglycan-sarcospan complex. J Clin Invest 107: R1-7. (Pubitemid 32096840)
81. Sharma P, Ryu MH, Basu S, Maltby SA, Yeganeh B, et al. (2012) Epithelium-dependent modulation of responsiveness of airways from caveolin-1 knockout mice is mediated through cyclooxygenase-2 and 5-lipoxygenase. Br J Pharmacol 167: 548-560.
82. Gunst SJ, Stropp JQ, Flavahan NA (1989) Muscarinic receptor reserve and beta-adrenergic sensitivity in tracheal smooth muscle. J Appl Physiol (1985) 67: 1294-1298.
83. Meurs H, Roffel AF, Postema JB, Timmermans A, Elzinga CR, et al. (1988) Evidence for a direct relationship between phosphoinositide metabolism and airway smooth muscle contraction induced by muscarinic agonists. Eur J Pharmacol 156: 271-274. (Pubitemid 18260488)
84. Brooks SV, Faulkner JA (1988) Contractile properties of skeletal muscles from young, adult and aged mice. The Journal of physiology 404: 71-82.
85. Dick J, Vrbova G (1993) Progressive deterioration of muscles in mdx mice induced by overload. Clinical science 84: 145-150. (Pubitemid 23053220)
86. Petrof BJ (1998) The molecular basis of activity-induced muscle injury in Duchenne muscular dystrophy. Molecular and cellular biochemistry 179: 111-123.
87. Weller B, Karpati G, Carpenter S (1990) Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions. Journal of the neurological sciences 100: 9-13.
88. Danialou G, Comtois AS, Dudley R, Karpati G, Vincent G, et al. (2001) Dystrophin-deficient cardiomyocytes are abnormally vulnerable to mechanical stress-induced contractile failure and injury. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 15: 1655-1657.
89. Yasuda S, Townsend D, Michele DE, Favre EG, Day SM, et al. (2005) Dystrophic heart failure blocked by membrane sealant poloxamer. Nature 436: 1025-1029. (Pubitemid 41191686)