Cardiomyocyte-specific expression of lamin A improves cardiac function in Lmna-/- mice

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Frock, Richard L ^a   Chen, Steven C ^a   Da, Dao Fu ^b   Frett, Ellie ^c   Lau, Carmen ^a   Brown, Christina ^a   Pak, Diana N ^a   Wang, Yuexia ^a   Muchir, Antoine ^e   Worman, Howard J ^e   Santana, Luis F ^b   Ladiges, Warren C ^b   Rabinovitch, Peter S ^b   Kennedy, Brian K ^a,d  

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

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

^d BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^e NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; DESMIN; LAMIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE THERAPY; HEART CONDUCTION; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART PERFORMANCE; HEART VENTRICLE SIZE; IMMUNOFLUORESCENCE; LIFE EXTENSION; MOUSE; NONHUMAN; PR INTERVAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ANIMALS; CYTOPLASM; DESMIN; ELECTROCARDIOGRAPHY; HEART VENTRICLES; LAMIN TYPE A; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, GENETIC; MUSCLE CELLS; MYOCYTES, CARDIAC; PHENOTYPE; TRANSGENES;

EID: 84865048724     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042918     Document Type: Article

References (45)

1. Lee DC, Welton KL, Smith ED, Kennedy BK, (2009) A-type nuclear lamins act as transcriptional repressors when targeted to promoters. Exp Cell Res 315: 996-1007.
2. Shumaker DK, Solimando L, Sengupta K, Shimi T, Adam SA, et al. (2008) The highly conserved nuclear lamin Ig-fold binds to PCNA: its role in DNA replication. J Cell Biol 181: 269-280.
3. Spann TP, Goldman AE, Wang C, Huang S, Goldman RD, (2002) Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J Cell Biol 156: 603-608.
4. Spann TP, Moir RD, Goldman AE, Stick R, Goldman RD, (1997) Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J Cell Biol 136: 1201-1212.
5. Worman HJ, Ostlund C, Wang Y, (2010) Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol 2: a000760.
6. Burtner CR, Kennedy BK, (2010) Progeria syndromes and ageing: what is the connection? Nat Rev Mol Cell Biol 11: 567-578.
7. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, et al. (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147: 913-920.
8. Nikolova V, Leimena C, McMahon AC, Tan JC, Chandar S, et al. (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest 113: 357-369.
9. Wolf CM, Wang L, Alcalai R, Pizard A, Burgon PG, et al. (2008) Lamin A/C haploinsufficiency causes dilated cardiomyopathy and apoptosis-triggered cardiac conduction system disease. J Mol Cell Cardiol 44: 293-303.
10. Davies BS, Barnes RH, 2nd, Tu Y, Ren S, Andres DA, et al (2010) An accumulation of non-farnesylated prelamin A causes cardiomyopathy but not progeria. Hum Mol Genet 19: 2682-2694.
11. Fong LG, Ng JK, Lammerding J, Vickers TA, Meta M, et al. (2006) Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J Clin Invest 116: 743-752.
12. Mounkes LC, Kozlov SV, Rottman JN, Stewart CL, (2005) Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum Mol Genet 14: 2167-2180.
13. Arimura T, Helbling-Leclerc A, Massart C, Varnous S, Niel F, et al. (2005) Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet 14: 155-169.
14. Bonne G, Mercuri E, Muchir A, Urtizberea A, Becane HM, et al. (2000) Clinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Ann Neurol 48: 170-180.
15. Fatkin D, MacRae C, Sasaki T, Wolff MR, Porcu M, et al. (1999) Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N Engl J Med 341: 1715-1724.
16. Wang Y, Herron AJ, Worman HJ, (2006) Pathology and nuclear abnormalities in hearts of transgenic mice expressing M371K lamin A encoded by an LMNA mutation causing Emery-Dreifuss muscular dystrophy. Hum Mol Genet 15: 2479-2489.
17. Frock RL, Kudlow BA, Evans AM, Jameson SA, Hauschka SD, et al. (2006) Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev 20: 486-500.
18. Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, et al. (2009) Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 119: 2789-2797.
19. Muchir A, Pavlidis P, Decostre V, Herron AJ, Arimura T, et al. (2007) Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery-Dreifuss muscular dystrophy. J Clin Invest 117: 1282-1293.
20. Muchir A, Wu W, Worman HJ, (2009) Reduced expression of A-type lamins and emerin activates extracellular signal-regulated kinase in cultured cells. Biochim Biophys Acta 1792: 75-81.
21. Warn-Cramer BJ, Cottrell GT, Burt JM, Lau AF, (1998) Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J Biol Chem 273: 9188-9196.
22. Ruch RJ, Trosko JE, Madhukar BV, (2001) Inhibition of connexin43 gap junctional intercellular communication by TPA requires ERK activation. J Cell Biochem 83: 163-169.
23. Sosinsky GE, Solan JL, Gaietta GM, Ngan L, Lee GJ, et al. (2007) The C-terminus of connexin43 adopts different conformations in the Golgi and gap junction as detected with structure-specific antibodies. Biochem J 408: 375-385.
24. Gary-Bobo G, Parlakian A, Escoubet B, Franco CA, Clement S, et al. (2008) Mosaic inactivation of the serum response factor gene in the myocardium induces focal lesions and heart failure. Eur J Heart Fail 10: 635-645.
25. Gutstein DE, Morley GE, Fishman GI, (2001) Conditional gene targeting of connexin43: exploring the consequences of gap junction remodeling in the heart. Cell Commun Adhes 8: 345-348.
26. Gonzalez S, Aguilera S, Urzua U, Quest AF, Molina C, et al. (2011) Mechanotransduction and epigenetic control in autoimmune diseases. Autoimmun Rev 10: 175-179.
27. Dahl KN, Ribeiro AJ, Lammerding J, (2008) Nuclear shape, mechanics, and mechanotransduction. Circ Res 102: 1307-1318.
28. Favreau C, Delbarre E, Courvalin JC, Buendia B, (2008) Differentiation of C2C12 myoblasts expressing lamin A mutated at a site responsible for Emery-Dreifuss muscular dystrophy is improved by inhibition of the MEK-ERK pathway and stimulation of the PI3-kinase pathway. Exp Cell Res 314: 1392-1405.
29. Gonzalez JM, Navarro-Puche A, Casar B, Crespo P, Andres V, (2008) Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. J Cell Biol 183: 653-666.
30. Rodriguez J, Calvo F, Gonzalez JM, Casar B, Andres V, et al. (2010) ERK1/2 MAP kinases promote cell cycle entry by rapid, kinase-independent disruption of retinoblastoma-lamin A complexes. J Cell Biol 191: 967-979.
31. Muchir A, Shan J, Bonne G, Lehnart SE, Worman HJ, (2009) Inhibition of extracellular signal-regulated kinase signaling to prevent cardiomyopathy caused by mutation in the gene encoding A-type lamins. Hum Mol Genet 18: 241-247.
32. Wu W, Muchir A, Shan J, Bonne G, Worman HJ, (2011) Mitogen-activated protein kinase inhibitors improve heart function and prevent fibrosis in cardiomyopathy caused by mutation in lamin A/C gene. Circulation 123: 53-61.
33. Kodama H, Fukuda K, Pan J, Sano M, Takahashi T, et al. (2000) Significance of ERK cascade compared with JAK/STAT and PI3-K pathway in gp130-mediated cardiac hypertrophy. Am J Physiol Heart Circ Physiol 279: H1635-1644.
34. Laird DW, (2006) Life cycle of connexins in health and disease. Biochem J 394: 527-543.
35. Guerrero PA, Schuessler RB, Davis LM, Beyer EC, Johnson CM, et al. (1997) Slow ventricular conduction in mice heterozygous for a connexin43 null mutation. J Clin Invest 99: 1991-1998.
36. Danik SB, Liu F, Zhang J, Suk HJ, Morley GE, et al. (2004) Modulation of cardiac gap junction expression and arrhythmic susceptibility. Circ Res 95: 1035-1041.
37. Eckardt D, Theis M, Degen J, Ott T, van Rijen HV, et al. (2004) Functional role of connexin43 gap junction channels in adult mouse heart assessed by inducible gene deletion. J Mol Cell Cardiol 36: 101-110.
38. Gutstein DE, Danik SB, Lewitton S, France D, Liu F, et al. (2005) Focal gap junction uncoupling and spontaneous ventricular ectopy. Am J Physiol Heart Circ Physiol 289: H1091-1098.
39. Gard JJ, Yamada K, Green KG, Eloff BC, Rosenbaum DS, et al. (2005) Remodeling of gap junctions and slow conduction in a mouse model of desmin-related cardiomyopathy. Cardiovasc Res 67: 539-547.
40. Aplin M, Christensen GL, Schneider M, Heydorn A, Gammeltoft S, et al. (2007) Differential extracellular signal-regulated kinases 1 and 2 activation by the angiotensin type 1 receptor supports distinct phenotypes of cardiac myocytes. Basic Clin Pharmacol Toxicol 100: 296-301.
41. Ivorra C, Kubicek M, Gonzalez JM, Sanz-Gonzalez SM, Alvarez-Barrientos A, et al. (2006) A mechanism of AP-1 suppression through interaction of c-Fos with lamin A/C. Genes Dev 20: 307-320.
42. Polontchouk L, Ebelt B, Jackels M, Dhein S, (2002) Chronic effects of endothelin 1 and angiotensin II on gap junctions and intercellular communication in cardiac cells. Faseb J 16: 87-89.
43. Lu G, Haider H, Porollo A, Ashraf M, (2010) Mitochondria-specific transgenic overexpression of connexin-43 simulates preconditioning-induced cytoprotection of stem cells. Cardiovasc Res 88: 277-286.
44. Rottlaender D, Boengler K, Wolny M, Michels G, Endres-Becker J, et al. (2010) Connexin 43 acts as a cytoprotective mediator of signal transduction by stimulating mitochondrial KATP channels in mouse cardiomyocytes. J Clin Invest 120: 1441-1453.
45. Roth DM, Swaney JS, Dalton ND, Gilpin EA, Ross J Jr, (2002) Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol 282: H2134-2140.