Dystrophin-deficient cardiomyopathy in mouse: Expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart

Neuromuscular Disorders

Volumn 18, Issue 5, 2008, Pages 371-381

  Spurney, Christopher F ^a   Knoblach, Susan ^a   Pistilli, Emidio E ^a   Nagaraju, Kanneboyina ^a   Martin, Gerard R ^a   Hoffman, Eric P ^a  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Cardiomyopathy; Duchenne muscular dystrophy; Echocardiography; Lox; Mouse; Nox4

Indexed keywords

DYSTROPHIN; MESSENGER RNA; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CARDIOVASCULAR PARAMETERS; CONNECTIVE TISSUE; CONTROLLED STUDY; DISEASE ASSOCIATION; DUCHENNE MUSCULAR DYSTROPHY; ELECTROCARDIOGRAPHY; FIBROSIS; GENE ACTIVATION; GENE EXPRESSION; GENETIC ANALYSIS; HEART; HEART DISEASE; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HISTOLOGY; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; VALIDATION PROCESS; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; DYSTROPHIN; ECHOCARDIOGRAPHY; EXTRACELLULAR MATRIX PROTEINS; FIBROSIS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENE EXPRESSION PROFILING; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM; MYOCYTES, CARDIAC; NADPH OXIDASE; PROTEIN-LYSINE 6-OXIDASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VENTRICULAR DYSFUNCTION;

EID: 43449105011     PISSN: 09608966     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nmd.2008.03.008     Document Type: Article

References (54)

1. Hoffman E.P., Brown R.H., and Kunkel L.M. Dystrophin, the protein product of the Duchenne muscular dystrophy locus. Cell 51 (1987) 919-928
2. Gilroy J., Cahalan J.L., Berman R., and Newman M. Cardiac and pulmonary complications in Duchenne's progressive muscular dystrophy. Circulation 27 (1963) 484-493
3. De Kermadec J.M., Becane H.M., Chenard A., Tertrain F., and Weiss Y. Prevalence of left ventricular systolic dysfunction in Duchenne muscular dystrophy: an echocardiographic study. Am Heart J 127 (1994) 618-623
4. Kirchmann C., Kececioglu D., Korinthenberg R., and Dittrich S. Echocardiographic and electrocardiographic findings of cardiomyopathy in Duchenne and Becker-Kiener muscular dystrophies. Pediatr Cardiol 26 (2005) 66-72
5. Gulati S., Saxena A., Kumar V., and Kalra V. Duchenne muscular dystrophy: prevalence and patterns of cardiac involvement. Indian J Pediatr 72 (2005) 389-393
6. Eagle M., Baudouin S.V., Chandler C., Giddings D.R., Bullock R., and Bushby K. Survival in Duchenne muscular dystrophy: improvements in left expectancy since 1967 and the impact of home nocturnal ventilation. Neuromuscul Disord 12 (2002) 926-929
7. Emery A.E. Population frequencies of inherited neuromuscular diseases: a world survey. Neuromuscul Disord 1 (1991) 19-29
8. Hoffman E.P., Kunkel L.M., Angelini C., Clarke A., Johnson M., and Harris J.B. Improved diagnosis of Becker muscular dystrophy by dystrophin testing. Neurology 39 (1989) 1011-1017
9. Melacini P., Fanin M., Danieli G.A., et al. Cardiac involvement in Becker muscular dystrophy. J Am Coll Cardiol 22 7 (1993) 1927-1934
10. Melacini P., Fanin M., Danieli G.A., et al. Myocardial involvement is very frequent among patients affected with subclinical Becker's muscular dystrophy. Circulation 94 (1996) 3168-3175
11. Leferovich J.M., Bedelbaeva K., Samulewicz S., et al. Heart regeneration in adult MRL mice. Proc Natl Acad Sci USA 98 17 (2001) 9830-9835
12. Poss K.D., Wilson L.G., and Keating M.T. Heart regeneration in zebrafish. Science 298 (2002) 2188-2190
13. Ryder-Cook A.S., Sicinski P., Thomas K., et al. Localization of the mdx mutation within the mouse dystrophin gene. EMBO J 7 10 (1988) 3017-3021
14. Sicinski P., Geng Y., Ryder-Cook A.S., Barnard E.A., Darlison M.G., and Barnard P.J. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244 4912 (1989) 1578-1580
15. Quinlan J.G., Hahn H.S., Wong B.L., Lorenz J.N., Wenisch A.S., and Levin L.S. Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul Disord 14 (2004) 491-496
16. Schiller N.B., Shah P.M., Crawford M., et al. Recommendations for quantification if the left ventricle by two-dimensional echocardiography. American society of echocardiography committee on standards, subcommittee on quantitation of two-dimensional echocardiograms. J Am Soc Echocardiogr 2 5 (1989) 358-367
17. Curtis A.S. Area and volume measurements by random sampling methods. Med Biol Illus 10 (1960) 261
18. Seo J., and Hoffman E.P. Prove set algorithms: is there a rational best bet?. BMC Bioinform 7 (2006) 395-407
19. Kawahara T., Ritsick D., Cheng G., and Lambeth J.D. Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation. J Biol Chem 280 (2005) 31859-31869
20. Collins K.A., Korcarz C.E., Shroff S.G., et al. Accuracy of echocardiographic estimates of left ventricular mass in mice. Am J Physiol Heart Circ Physiol 280 (2001) H1954-H1962
21. Youn H.J., Rokosh G., Lester S.J., Simpson P., Schiller N.B., and Foster E. Two-dimensional echocardiography with a 15-MHz transducer is a promising alternative for in vivo measurement of left ventricular mass in mice. J Am Soc Echocardiogr 12 (1999) 70-75
22. Hilenski L.L., Clempus R.E., Quinn M.T., Lambeth J.D., and Griendling K.K. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24 (2004) 677-683
23. Roth D.M., Swaney J.S., Dalton N.D., Gilpin E.A., and Ross Jr. J. Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol 282 (2002) H2134-H2140
24. Loufrani L., Matrougui K., Gorny D., et al. Flow (shear stress)-induced endothelium-dependent dilation is altered in mice lacking the gene encoding for dystrophin. Circulation 103 6 (2001) 864-870
25. Loufrani L., Levy B.I., and Henrion D. Defect in microvascular adaptation to chronic changes in blood flow in mice lacking the gene encoding for dystrophin. Circ Res 91 12 (2002) 1183-1189
26. Okajima K., Abe Y., Fujimoto K., et al. Comparative study of high-resolution microimaging with 30-MHz scanner for evaluating cardiac function in mice. J Am Soc Echocardiogr 20 (2007) 1203-1210
27. Zhou Y.Q., Foster F.S., Nieman B.J., et al. Comprehensive transthoracic cardiac imaging in mice using ultrasound biomicroscopy with anatomical confirmation by magnetic resonance imaging. Physiol Genomics 18 (2004) 232-244
28. Lu H., Fedak P.W., Dai X., et al. Integrin-linked kinase expression is elevated in human cardiac hypertrophy and induces hypertrophy in transgenic mice. Circulation 114 (2006) 2271-2279
29. Radke M.H., Peng J., Wu Y., et al. Targeted deletion of titin N2B region leads to diastolic dysfunction and cardiac atrophy. Proc Natl Acad Sci USA 104 (2007) 3444-3449
30. Chen H., Yong W., Ren S., et al. Over expression of bone morphogenetic protein 10 in myocardium disrupts cardiac postnatal hypertrophic growth. J Biol Chem 281 (2006) 27481-27491
31. Zhang Y., Takagawa J., Sievers R.E., et al. Validation of the wall motion score and myocardial performance indexes as novel techniques to assess cardiac function in mice after myocardial infarction. Am J Physiol Heart Circ Physiol 292 (2007) H1187-H1192
32. Dawson D., Lygate C.A., Saunders J., et al. Quantitative 3-dimensional echocardiography for accurate and rapid cardiac phenotype characterization in mice. Circulation 110 (2004) 1632-1637
33. Wilding J.R., Schneider J.E., Sang A.E., Davies K.E., Neubauer S., and Clarke K. Dystrophin- and MLP-deficient mouse hearts: marked differences in morphology and function, but similar accumulation of cytoskeletal proteins. FASEB J 19 (2005) 79-81
34. Kober F., Iltis I., Cozzone P.J., and Bernard M. Cine-MRI assessment of cardiac function in mice anesthetized with ketamine/xylazine and isoflurane. MAGMA 17 (2004) 157-161
35. Bridges L.R. The association of cardiac muscle necrosis and inflammation with the degenerative and persistent myopathy of MDX mice. J Neurol Sci 72 2-3 (1986) 147-157
36. Lefaucher J.P., Pastoret C., and Sebille A. Phenotype of dystrinopathy in old mdx mice. Anat Rec 242 1 (1995) 70-76
37. Cohn R.D., Durbeej M., Moore S.A., Coral-Vazquez R., Prouty S., and Campbell K.P. Prevention of cardiomyopathy in mouse models lacking the smooth muscle sarcoglycan-sarcospan complex. J Clin Invest 107 2 (2001) R1-R7
38. Nakamura A., Yoshida K., Takeda S., Dohi N., and Ikeda S. Progression of dystrophic features and activation of mitogen-activated protein kinases and calcineurin by physical exercise, in hearts of mdx mice. FEBS Lett 520 1-3 (2002) 18-24
39. Taylor L.A., Carthy C.M., Yang D., et al. Host gene regulation during coxsackievirus B3 infection in mice; assessment by microarrays. Circ Res 87 (2000) 328-334
40. Blaxall B.C., Spang R., Rockman H.A., and Koch W.J. Differential myocardial gene expression in the development and rescue of murine heart failure. Physiol Genomics 15 (2003) 105-114
41. Tan F.L., Moravec C.S., Li J., et al. The gene expression fingerprint of human heart failure. Proc Natl Acad Sci USA 99 (2002) 11387-11392
42. Barth A.S., Kuner R., Buness A., et al. Identification of a common gene expression signature in dilated cardiomyopathy across independent microarray studies. J Am Coll Cardiol 48 (2006) 1610-1617
43. Sanoudou D., Vafiadaki E., Arvanitis D.A., Kranias E., and Kontrogianni-Konstantopoulos A. Array lessons from the heart: focus on the genome and transcriptome of cardiomyopathies. Physiol Genomics 21 (2005) 131-143
44. Hwang J.J., Allen P.D., Tseng G.C., et al. Microarray gene expression profiles in dilated and hypertrophic cardiomyopathic end-stage heart failure. Physiol Genomics 10 (2002) 31-44
45. Lucero H.A., and Kagan H.M. Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell Mol Life Sci 63 19-20 (2006) 2304-2316
46. Maki J.M., Rasanen J., Tikkanen H., et al. Inactivation of the Lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation 106 19 (2002) 2503-2509
47. Hayashi K., Fong K.S., Mercier F., Boyd C.D., Csiszar K., and Hayashi M. Comparative immunocytochemical localization of Lysyl oxidase (LOX) and the Lysyl oxidase-like (LOXL) proteins: changes in the expression of LOXL during development and growth of mouse tissues. J Mol Histol 35 8-9 (2004) 845-855
48. Tsuda T., Gao E., Evangelist L., Markova D., Ma X., and Chu M.L. Post-ischemic myocardial fibrosis occurs independent of hemodynamic changes. Cardiovasc Res 59 4 (2003) 926-933
49. Lijnen P.J., Petrov V.V., Turner M., and Fagard R.H. Collagen production in cardiac fibroblasts during inhibition of aminopeptidase B. J Renin Angiotensin Aldosterone Syst 6 2 (2005) 69-77
50. Lijnen P., Petrov V., Diaz-Araya G., and Fagard R. Effect of bestatin on angiotensin I-, II-, III-induced collagen gel contraction in cardiac fibroblasts. J Renin Angiotensin Aldosterone Syst 5 4 (2004) 183-188
51. Cross A.R., and Segal A.W. The NADPH oxidase of professional phagocytes - prototype of the NOX electron transport chain systems. Biochim Biophys Acta 1657 1 (2004) 1-22
52. Nguyen H.X., and Tidball J.G. Null mutation of gpphox91 reduces muscle membrane lysis during muscle inflammation in mice. J Physiol 553 pt 3 (2003) 833-841
53. Cucoranu I., Clempus R., Dikalova A., et al. NAD(P)H oxidase 4 mediates transforming factor-β1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 97 (2005) 900-907
54. 2 dependent arachidonic acid production in adult cardiac fibroblasts. FEBS Lett 579 (2005) 2533-2540