Attenuated hypertrophic response to pressure overload in a lamin A/C haploinsufficiency mouse

Journal of Molecular and Cellular Cardiology

Volumn 48, Issue 6, 2010, Pages 1290-1297

  Cupesi, Mihaela ^a   Yoshioka, Jun ^a   Gannon, Joseph ^a   Kudinova, Anastacia ^a   Stewart, Colin L ^b   Lammerding, Jan ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

Hypertrophy; Lamin; Mechanical stress; Mechanotransduction; Pressure overload; Transverse aortic constriction

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; LAMIN A; LAMIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SIZE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; ECHOCARDIOGRAPHY; GENE EXPRESSION; GENOTYPE; HEART HEMODYNAMICS; HEART HYPERTROPHY; HEART MUSCLE CELL; HEART STRESS; HEART VENTRICLE FUNCTION; HETEROZYGOSITY; HETEROZYGOTE; HISTOLOGY; MORPHOLOGY; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ANIMALS; AORTA; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; HUMANS; LAMIN TYPE A; MICE; MICE, TRANSGENIC; MUTATION; NUCLEAR ENVELOPE; PHENOTYPE; STRESS, MECHANICAL;

ANIMALIA; MUS;

EID: 77952673428     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.10.024     Document Type: Article

References (55)

1. Towbin J.A., Bowles N.E. Molecular genetics of left ventricular dysfunction. Curr. Mol. Med. 2001 Mar, 1(1):81-90.
2. Sylvius N., Bilinska Z.T., Veinot J.P., Fidzianska A., Bolongo P.M., Poon S., et al. In vivo and in vitro examination of the functional significances of novel lamin gene mutations in heart failure patients. J. Med. Genet. 2005 Aug, 42(8):639-647.
3. Fatkin D., MacRae C., Sasaki T., Wolff M.R., Porcu M., Frenneaux M., et al. 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. 1999 Dec 2, 341(23):1715-1724.
4. Taylor M.R., Fain P.R., Sinagra G., Robinson M.L., Robertson A.D., Carniel E., et al. Natural history of dilated cardiomyopathy due to lamin A/C gene mutations. J. Am. Coll. Cardiol. 2003 Mar 5, 41(5):771-780.
5. Bonne G., Di Barletta M.R., Varnous S., Becane H.M., Hammouda E.H., Merlini L., et al. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 1999 Mar, 21(3):285-288.
6. Sakaki M., Koike H., Takahashi N., Sasagawa N., Tomioka S., Arahata K., et al. Interaction between emerin and nuclear lamins. J. Biochem. (Tokyo) 2001 Feb, 129(2):321-327.
7. Bione S., Maestrini E., Rivella S., Mancini M., Regis S., Romeo G., et al. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 1994 Dec, 8(4):323-327.
8. Arimura T., Helbling-Leclerc A., Massart C., Varnous S., Niel F., Lacene E., et al. Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum. Mol. Genet. 2005 Jan 1, 14(1):155-169.
9. Funakoshi M., Tsuchiya Y., Arahata K. Emerin and cardiomyopathy in Emery-Dreifuss muscular dystrophy. Neuromuscul. Disord. 1999 Mar, 9(2):108-114.
10. Wessely R., Seidl S., Schomig A. Cardiac involvement in Emery-Dreifuss muscular dystrophy. Clin. Genet. 2005 Mar, 67(3):220-223.
11. Worman H.J., Fong L.G., Muchir A., Young S.G. Laminopathies and the long strange trip from basic cell biology to therapy. J. Clin. Invest. 2009 Jul, 119(7):1825-1836.
12. Schirmer E.C., Gerace L. The stability of the nuclear lamina polymer changes with the composition of lamin subtypes according to their individual binding strengths. J. Biol. Chem. 2004 Oct 8, 279(41):42811-42817.
13. Herrmann H., Strelkov S.V., Burkhard P., Aebi U. Intermediate filaments: primary determinants of cell architecture and plasticity. J. Clin. Invest. 2009 Jul, 119(7):1772-1783.
14. Lammerding J., Fong L.G., Ji J.Y., Reue K., Stewart C.L., Young S.G., et al. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 2006 Sep 1, 281(35):25768-25780.
15. Dahl K.N., Kahn S.M., Wilson K.L., Discher D.E. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell. Sci. 2004 Sep 15, 117(Pt 20):4779-4786.
16. Libotte T., Zaim H., Abraham S., Padmakumar V.C., Schneider M., Lu W., et al. Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol. Biol. Cell. 2005 Jul, 16(7):3411-3424.
17. Padmakumar V.C., Libotte T., Lu W., Zaim H., Abraham S., Noegel A.A., et al. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J. Cell. Sci. 2005 Aug 1, 118(Pt 15):3419-3430.
18. Crisp M., Liu Q., Roux K., Rattner J.B., Shanahan C., Burke B., et al. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell. Biol. 2006 Jan 2, 172(1):41-53.
19. Haque F., Lloyd D.J., Smallwood D.T., Dent C.L., Shanahan C.M., Fry A.M., et al. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol. Cell. Biol. 2006 May, 26(10):3738-3751.
20. Hale C.M., Shrestha A.L., Khatau S.B., Stewart-Hutchinson P.J., Hernandez L., Stewart C.L., et al. Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys. J. 2008 Dec, 95(11):5462-5475.
21. Lloyd D.J., Trembath R.C., Shackleton S. A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum. Mol. Genet. 2002 Apr 1, 11(7):769-777.
22. Dreuillet C., Tillit J., Kress M., Ernoult-Lange M. In vivo and in vitro interaction between human transcription factor MOK2 and nuclear lamin A/C. Nucleic Acids Res. 2002 Nov 1, 30(21):4634-4642.
23. Ozaki T., Saijo M., Murakami K., Enomoto H., Taya Y., Sakiyama S. Complex formation between lamin A and the retinoblastoma gene product: identification of the domain on lamin A required for its interaction. Oncogene 1994 Sep, 9(9):2649-2653.
24. Ivorra C., Kubicek M., Gonzalez J.M., Sanz-Gonzalez S.M., Alvarez-Barrientos A., O'Connor J.E., et al. A mechanism of AP-1 suppression through interaction of c-Fos with lamin A/C. Genes Dev. 2006 Feb 1, 20(3):307-320.
25. Sullivan T., Escalante-Alcalde D., Bhatt H., Anver M., Bhat N., Nagashima K., et al. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell. Biol. 1999 Nov 29, 147(5):913-920.
26. Nikolova V., Leimena C., McMahon A.C., Tan J.C., Chandar S., Jogia D., et al. Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J. Clin. Invest. 2004 Feb, 113(3):357-369.
27. Grattan M.J., Kondo C., Thurston J., Alakija P., Burke B.J., Stewart C., et al. Skeletal and cardiac muscle defects in a murine model of Emery-Dreifuss muscular dystrophy. Novartis Found. Symp. 2005, 264:118-133. discussion 33-9, 227-30.
28. Raharjo W.H., Enarson P., Sullivan T., Stewart C.L., Burke B. Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J. Cell. Sci. 2001 Dec, 114(Pt 24):4447-4457.
29. Vigouroux C., Auclair M., Dubosclard E., Pouchelet M., Capeau J., Courvalin J.C., et al. Nuclear envelope disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J. Cell. Sci. 2001 Dec, 114(Pt 24):4459-4468.
30. Fidzianska A., Hausmanowa-Petrusewicz I. Architectural abnormalities in muscle nuclei. Ultrastructural differences between X-linked and autosomal dominant forms of EDMD. J. Neurol. Sci. 2003 Jun 15, 210(1-2):47-51.
31. Fidzianska A., Toniolo D., Hausmanowa-Petrusewicz I. Ultrastructural abnormality of sarcolemmal nuclei in Emery-Dreifuss muscular dystrophy (EDMD). J. Neurol. Sci. 1998 Jul 15, 159(1):88-93.
32. Markiewicz E., Venables R., Mauricio Alvarez R., Quinlan R., Dorobek M., Hausmanowa-Petrucewicz I., et al. Increased solubility of lamins and redistribution of lamin C in X-linked Emery-Dreifuss muscular dystrophy fibroblasts. J. Struct. Biol. 2002 Oct, 140(1):241-253.
33. Lammerding J., Schulze P.C., Takahashi T., Kozlov S., Sullivan T., Kamm R.D., et al. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 2004 Feb, 113(3):370-378.
34. Wolf C.M., Wang L., Alcalai R., Pizard A., Burgon P.G., Ahmad F., et al. Lamin A/C haploinsufficiency causes dilated cardiomyopathy and apoptosis-triggered cardiac conduction system disease. J. Mol. Cell. Cardiol. 2008 Feb, 44(2):293-303.
35. Mounkes L.C., Kozlov S.V., Rottman J.N., Stewart C.L. Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum. Mol. Genet. 2005 Aug 1, 14(15):2167-2180.
36. Östlund C., Bonne G., Schwartz K., Worman H.J. Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J. Cell. Sci. 2001 Dec, 114(Pt 24):4435-4445.
37. Benedetti S., Menditto I., Degano M., Rodolico C., Merlini L., D'Amico A., et al. Phenotypic clustering of lamin A/C mutations in neuromuscular patients. Neurology 2007 Sep 18, 69(12):1285-1292.
38. Sebillon P., Bouchier C., Bidot L.D., Bonne G., Ahamed K., Charron P., et al. Expanding the phenotype of LMNA mutations in dilated cardiomyopathy and functional consequences of these mutations. J. Med. Genet. 2003 Aug, 40(8):560-567.
39. Lindsey M.L., Yoshioka J., MacGillivray C., Muangman S., Gannon J., Verghese A., et al. Effect of a cleavage-resistant collagen mutation on left ventricular remodeling. Circ. Res. 2003 Aug 8, 93(3):238-245.
40. Rockman H.A., Ross R.S., Harris A.N., Knowlton K.U., Steinhelper M.E., Field L.J., et al. Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 1991 Sep 15, 88(18):8277-8281.
41. Gottshall K.R., Hunter J.J., Tanaka N., Dalton N., Becker K.D., Ross J., et al. Ras-dependent pathways induce obstructive hypertrophy in echo-selected transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 1997 Apr 29, 94(9):4710-4715.
42. Tanaka N., Dalton N., Mao L., Rockman H.A., Peterson K.L., Gottshall K.R., et al. Transthoracic echocardiography in models of cardiac disease in the mouse. Circulation 1996 Sep 1, 94(5):1109-1117.
43. Packard G.C., Boardman T.J. The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort. Comp. Biochem. Physiol. A. 1999, 122:37-44.
44. Lammerding J., Hsiao J., Schulze P.C., Kozlov S., Stewart C.L., Lee R.T. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell. Biol. 2005 Aug 29, 170(5):781-791.
45. Zhao M., Chow A., Powers J., Fajardo G., Bernstein D. Microarray analysis of gene expression after transverse aortic constriction in mice. Physiol. Genomics 2004 Sep 16, 19(1):93-105.
46. Khachigian L.M. Early growth response-1 in cardiovascular pathobiology. Circ. Res. 2006 Feb 3, 98(2):186-191.
47. Muchir A., Pavlidis P., Bonne G., Hayashi Y.K., Worman H.J. Activation of MAPK in hearts of EMD null mice: similarities between mouse models of X-linked and autosomal dominant Emery Dreifuss muscular dystrophy. Hum. Mol. Genet. 2007 Aug 1, 16(15):1884-1895.
48. Muchir A., Pavlidis P., Decostre V., Herron A.J., Arimura T., Bonne G., et al. Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery-Dreifuss muscular dystrophy. J. Clin. Invest. 2007 May, 117(5):1282-1293.
49. Muchir A., Shan J., Bonne G., Lehnart S.E., Worman H.J. Inhibition of extracellular signal-regulated kinase signaling to prevent cardiomyopathy caused by mutation in the gene encoding A-type lamins. Hum. Mol. Genet. 2009 Jan 15, 18(2):241-247.
50. Muchir A., Wu W., Worman H.J. Reduced expression of A-type lamins and emerin activates extracellular signal-regulated kinase in cultured cells. Biochim. Biophys. Acta 2009 Jan, 1792(1):75-81.
51. Gius D., Cao X.M., Rauscher F.J., Cohen D.R., Curran T., Sukhatme V.P. Transcriptional activation and repression by Fos are independent functions: the C terminus represses immediate-early gene expression via CArG elements. Mol. Cell. Biol. 1990 Aug, 10(8):4243-4255.
52. Bloom S., Lockard V.G., Bloom M. Intermediate filament-mediated stretch-induced changes in chromatin: a hypothesis for growth initiation in cardiac myocytes. J. Mol. Cell. Cardiol. 1996 Oct, 28(10):2123-2127.
53. Wang N., Tytell J.D., Ingber D.E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell. Biol. 2009 Jan, 10(1):75-82.
54. Afilalo J., Sebag I.A., Chalifour L.E., Rivas D., Akter R., Sharma K., et al. Age-related changes in lamin A/C expression in cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 2007 Sep, 293(3):H1451-H1456.
55. Cortes R., Rosello-Lleti E., Rivera M., Martinez-Dolz L., Azorin I., Salvador A., et al. The role of the nuclear lamins in the pathogenesis of heart failure in patients undergoing cardiac transplantation. Transplant. Proc. 2009 Jul-Aug, 41(6):2227-2230.