Ablation of the Cardiac-Specific Gene Leucine-Rich Repeat Containing 10 (Lrrc10) Results in Dilated Cardiomyopathy

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Brody, Matthew J ^a,b   Hacker, Timothy A ^a   Patel, Jitandrakumar R ^a   Feng, Li ^a   Sadoshima, Junichi ^c   Tevosian, Sergei G ^d   Balijepalli, Ravi C ^a   Moss, Richard L ^a   Lee, Youngsook ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA ACTININ; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PROTEIN SERINE THREONINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ANALYSIS; HEART FUNCTION; HEART MUSCLE; IMMUNOPRECIPITATION; LRRC10 GENE; MICROARRAY ANALYSIS; MOUSE; MUSCLE CONTRACTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN CONTENT; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ACTININ; ACTINS; ANIMALS; BLOTTING, WESTERN; CARDIOMYOPATHY, DILATED; CYTOSKELETON; ECHOCARDIOGRAPHY; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MUSCLE PROTEINS; MYOCARDIUM; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

MAMMALIA; MUS;

EID: 84870951489     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051621     Document Type: Article

References (88)

1. Olson EN, (2004) A decade of discoveries in cardiac biology. Nat Med 10: 467-474.
2. Kimura A (2008) Molecular etiology and pathogenesis of hereditary cardiomyopathy. Circ J 72 Suppl A: A38-48.
3. Frank D, Frey N, (2011) Cardiac Z-disc Signaling Network. J Biol Chem 286: 9897-9904.
4. Kim KH, Kim TG, Micales BK, Lyons GE, Lee Y, (2007) Dynamic expression patterns of leucine-rich repeat containing protein 10 in the heart. Dev Dyn 236: 2225-2234.
5. Nakane T, Satoh T, Inada Y, Nakayama J, Itoh F, et al. (2004) Molecular cloning and expression of HRLRRP, a novel heart-restricted leucine-rich repeat protein. Biochem Biophys Res Commun 314: 1086-1092.
6. Kim KH, Antkiewicz DS, Yan L, Eliceiri KW, Heideman W, et al. (2007) Lrrc10 is required for early heart development and function in zebrafish. Dev Biol 308: 494-506.
7. Adameyko II, Mudry RE, Houston-Cummings NR, Veselov AP, Gregorio CC, et al. (2005) Expression and regulation of mouse SERDIN1, a highly conserved cardiac-specific leucine-rich repeat protein. Dev Dyn 233: 540-552.
8. Kobe B, Deisenhofer J, (1995) Proteins with leucine-rich repeats. Curr Opin Struct Biol 5: 409-416.
9. Yan J, Aldrich RW, (2010) LRRC26 auxiliary protein allows BK channel activation at resting voltage without calcium. Nature 466: 513-516.
10. Will RD, Eden M, Just S, Hansen A, Eder A, et al. (2010) Myomasp/LRRC39, a heart- and muscle-specific protein, is a novel component of the sarcomeric M-band and is involved in stretch sensing. Circ Res 107: 1253-1264.
11. Luther PK, (2009) The vertebrate muscle Z-disc: sarcomere anchor for structure and signalling. J Muscle Res Cell Motil 30: 171-185.
12. Ervasti JM, (2003) Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278: 13591-13594.
13. Hoshijima M, (2006) Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am J Physiol Heart Circ Physiol 290: H1313-1325.
14. Zheng M, Cheng H, Li X, Zhang J, Cui L, et al. (2009) Cardiac-specific ablation of Cypher leads to a severe form of dilated cardiomyopathy with premature death. Hum Mol Genet 18: 701-713.
15. Arber S, Hunter JJ, Ross J Jr, Hongo M, Sansig G, et al. (1997) MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88: 393-403.
16. Cheng H, Kimura K, Peter AK, Cui L, Ouyang K, et al. (2010) Loss of enigma homolog protein results in dilated cardiomyopathy. Circ Res 107: 348-356.
17. White DE, Coutu P, Shi YF, Tardif JC, Nattel S, et al. (2006) Targeted ablation of ILK from the murine heart results in dilated cardiomyopathy and spontaneous heart failure. Genes Dev 20: 2355-2360.
18. Zemljic-Harpf AE, Miller JC, Henderson SA, Wright AT, Manso AM, et al. (2007) Cardiac-myocyte-specific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy. Mol Cell Biol 27: 7522-7537.
19. Vatta M, Mohapatra B, Jimenez S, Sanchez X, Faulkner G, et al. (2003) Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol 42: 2014-2027.
20. Knoll R, Hoshijima M, Hoffman HM, Person V, Lorenzen-Schmidt I, et al. (2002) The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell 111: 943-955.
21. Hassel D, Dahme T, Erdmann J, Meder B, Huge A, et al. (2009) Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat Med 15: 1281-1288.
22. Duboscq-Bidot L, Xu P, Charron P, Neyroud N, Dilanian G, et al. (2008) Mutations in the Z-band protein myopalladin gene and idiopathic dilated cardiomyopathy. Cardiovasc Res 77: 118-125.
23. Knoll R, Postel R, Wang J, Kratzner R, Hennecke G, et al. (2007) Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116: 515-525.
24. Li D, Tapscoft T, Gonzalez O, Burch PE, Quinones MA, et al. (1999) Desmin mutation responsible for idiopathic dilated cardiomyopathy. Circulation 100: 461-464.
25. Manuylov NL, Manuylova E, Avdoshina V, Tevosian S, (2008) Serdin1/Lrrc10 is dispensable for mouse development. Genesis 46: 441-446.
26. Harris SP, Bartley CR, Hacker TA, McDonald KS, Douglas PS, et al. (2002) Hypertrophic cardiomyopathy in cardiac myosin binding protein-C knockout mice. Circ Res 90: 594-601.
27. Zhou YQ, Foster FS, Qu DW, Zhang M, Harasiewicz KA, et al. (2002) Applications for multifrequency ultrasound biomicroscopy in mice from implantation to adulthood. Physiol Genomics 10: 113-126.
28. O'Connell TD, Rodrigo MC, Simpson PC, (2007) Isolation and culture of adult mouse cardiac myocytes. Methods Mol Biol 357: 271-296.
29. Mysliwiec MR, Kim TG, Lee Y, (2007) Characterization of zinc finger protein 496 that interacts with Jumonji/Jarid2. FEBS Lett 581: 2633-2640.
30. Jung J, Kim TG, Lyons GE, Kim HR, Lee Y, (2005) Jumonji regulates cardiomyocyte proliferation via interaction with retinoblastoma protein. J Biol Chem 280: 30916-30923.
31. Mysliwiec MR, Carlson CD, Tietjen J, Hung H, Ansari AZ, et al. (2012) Jarid2 (Jumonji, AT rich interactive domain 2) regulates NOTCH1 expression via histone modification in the developing heart. J Biol Chem 287: 1235-1241.
32. Polge C, Heng AE, Jarzaguet M, Ventadour S, Claustre A, et al. (2011) Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1. FASEB J 25: 3790-3802.
33. Olsson MC, Patel JR, Fitzsimons DP, Walker JW, Moss RL, (2004) Basal myosin light chain phosphorylation is a determinant of Ca2+ sensitivity of force and activation dependence of the kinetics of myocardial force development. Am J Physiol 287: H2712-H2718.
34. Patel JR, Fitzsimons DP, Buck SH, Muthuchamy M, Wieczorek DF, et al. (2001) PKA accelerates rate of force development in murine skinned myocardium expressing α- or β-tropomyosin. Am J Physiol 280: H2732-H2739.
35. Brenner B, Eisenberg E, (1986) Rate of force generation in muscle: correlation with actomysoin ATPase activity in solution. Proc Natl Acad Sci USA 83: 3542-3546.
36. Chase PB, Martyn DA, Hannon JD, (1994) Isometric force redevelopment of skinned muscle fibers from rabbit activated with and without Ca2+. Biophys J 67: 1994-2001.
37. Mysliwiec MR, Bresnick EH, Lee Y (2011) Endothelial Jarid2/Jumonji is required for normal cardiac development and proper Notch1 expression. J Biol Chem.
38. Vollrath AL, Smith AA, Craven M, Bradfield CA, (2009) EDGE(3): a web-based solution for management and analysis of Agilent two color microarray experiments. BMC Bioinformatics 10: 280.
39. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
40. Vandekerckhove J, Weber K, (1979) The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle, and rabbit slow skeletal muscle. A protein-chemical analysis of muscle actin differentiation. Differentiation 14: 123-133.
41. Frank D, Kuhn C, Brors B, Hanselmann C, Ludde M, et al. (2008) Gene expression pattern in biomechanically stretched cardiomyocytes: evidence for a stretch-specific gene program. Hypertension 51: 309-318.
42. Russell B, Curtis MW, Koshman YE, Samarel AM, (2010) Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width. J Mol Cell Cardiol 48: 817-823.
43. Goldspink PH, Montgomery DE, Walker LA, Urboniene D, McKinney RD, et al. (2004) Protein kinase Cepsilon overexpression alters myofilament properties and composition during the progression of heart failure. Circ Res 95: 424-432.
44. Huang XP, Pi Y, Lokuta AJ, Greaser ML, Walker JW, (1997) Arachidonic acid stimulates protein kinase C-epsilon redistribution in heart cells. J Cell Sci 110 (Pt 14): 1625-1634.
45. Gu X, Bishop SP, (1994) Increased protein kinase C and isozyme redistribution in pressure-overload cardiac hypertrophy in the rat. Circ Res 75: 926-931.
46. Dorn GWII, Souroujon MC, Liron T, Chen CH, Gray MO, et al. (1999) Sustained in vivo cardiac protection by a rationally designed peptide that causes epsilon protein kinase C translocation. Proc Natl Acad Sci U S A 96: 12798-12803.
47. Nugent AW, Daubeney PE, Chondros P, Carlin JB, Cheung M, et al. (2003) The epidemiology of childhood cardiomyopathy in Australia. N Engl J Med 348: 1639-1646.
48. Lipshultz SE, Sleeper LA, Towbin JA, Lowe AM, Orav EJ, et al. (2003) The incidence of pediatric cardiomyopathy in two regions of the United States. N Engl J Med 348: 1647-1655.
49. Brancaccio M, Fratta L, Notte A, Hirsch E, Poulet R, et al. (2003) Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat Med 9: 68-75.
50. Frey N, Barrientos T, Shelton JM, Frank D, Rütten H, et al. (2004) Mice lacking calsarcin-1 are sensitized to calcineurin signaling and show accelerated cardiomyopathy in response to pathological biomechanical stress. Nat Med 10: 1336-1343.
51. Mohapatra B, Jimenez S, Lin JH, Bowles KR, Coveler KJ, et al. (2003) Mutations in the muscle LIM protein and alpha-actinin-2 genes in dilated cardiomyopathy and endocardial fibroelastosis. Mol Genet Metab 80: 207-215.
52. Fujita M, Mitsuhashi H, Isogai S, Nakata T, Kawakami A, et al. (2012) Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Dev Biol 361: 79-89.
53. Olson TM, Michels VV, Thibodeau SN, Tai YS, Keating MT, (1998) Actin mutations in dilated cardiomyopathy, a heritable form of heart failure. Science 280: 750-752.
54. Toko H, Takahashi H, Kayama Y, Oka T, Minamino T, et al. (2010) Ca2+/calmodulin-dependent kinase IIdelta causes heart failure by accumulation of p53 in dilated cardiomyopathy. Circulation 122: 891-899.
55. Tsukada T, Kotlyanskaya L, Huynh R, Desai B, Novak SM, et al. (2011) Identification of residues within tropomodulin-1 responsible for its localization at the pointed ends of the actin filaments in cardiac myocytes. J Biol Chem 286: 2194-2204.
56. Wang R, Kaul A, Sperry AO, (2010) TLRR (lrrc67) interacts with PP1 and is associated with a cytoskeletal complex in the testis. Biol Cell 102: 173-189.
57. Wang R, Sperry AO, (2011) PP1 forms an active complex with TLRR (lrrc67), a putative PP1 regulatory subunit, during the early stages of spermiogenesis in mice. PLoS One 6: e21767.
58. Babbitt CJ, Shai SY, Harpf AE, Pham CG, Ross RS, (2002) Modulation of integrins and integrin signaling molecules in the pressure-loaded murine ventricle. Histochem Cell Biol 118: 431-439.
59. Sopko N, Qin Y, Finan A, Dadabayev A, Chigurupati S, et al. (2011) Significance of thymosin beta4 and implication of PINCH-1-ILK-alpha-parvin (PIP) complex in human dilated cardiomyopathy. PLoS One 6: e20184.
60. Li R, Wu Y, Manso AM, Gu Y, Liao P, et al. (2012) beta1 Integrin Gene Excision in the Adult Murine Cardiac Myocyte Causes Defective Mechanical and Signaling Responses. Am J Pathol.
61. Colak D, Kaya N, Al-Zahrani J, Al Bakheet A, Muiya P, et al. (2009) Left ventricular global transcriptional profiling in human end-stage dilated cardiomyopathy. Genomics 94: 20-31.
62. Asakura M, Kitakaze M, (2009) Global gene expression profiling in the failing myocardium. Circ J 73: 1568-1576.
63. Grzeskowiak R, Witt H, Drungowski M, Thermann R, Hennig S, et al. (2003) Expression profiling of human idiopathic dilated cardiomyopathy. Cardiovasc Res 59: 400-411.
64. Barrans JD, Allen PD, Stamatiou D, Dzau VJ, Liew CC, (2002) Global gene expression profiling of end-stage dilated cardiomyopathy using a human cardiovascular-based cDNA microarray. Am J Pathol 160: 2035-2043.
65. Xu J, Gong NL, Bodi I, Aronow BJ, Backx PH, et al. (2006) Myocyte enhancer factors 2A and 2C induce dilated cardiomyopathy in transgenic mice. J Biol Chem 281: 9152-9162.
66. Kehat I, Molkentin JD, (2010) Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 122: 2727-2735.
67. Huang X, Walker JW, (2004) Myofilament anchoring of protein kinase C-epsilon in cardiac myocytes. J Cell Sci 117: 1971-1978.
68. Iwata M, Maturana A, Hoshijima M, Tatematsu K, Okajima T, et al. (2005) PKCepsilon-PKD1 signaling complex at Z-discs plays a pivotal role in the cardiac hypertrophy induced by G-protein coupling receptor agonists. Biochem Biophys Res Commun 327: 1105-1113.
69. Robia SL, Kang M, Walker JW, (2005) Novel determinant of PKC-epsilon anchoring at cardiac Z-lines. Am J Physiol Heart Circ Physiol 289: H1941-1950.
70. Takeishi Y, Ping P, Bolli R, Kirkpatrick DL, Hoit BD, et al. (2000) Transgenic overexpression of constitutively active protein kinase C epsilon causes concentric cardiac hypertrophy. Circ Res 86: 1218-1223.
71. Hankiewicz JH, Goldspink PH, Buttrick PM, Lewandowski ED, (2008) Principal strain changes precede ventricular wall thinning during transition to heart failure in a mouse model of dilated cardiomyopathy. Am J Physiol Heart Circ Physiol 294: H330-336.
72. Strait JB III, Martin JL, Bayer A, Mestril R, Eble DM, et al. (2001) Role of protein kinase C-epsilon in hypertrophy of cultured neonatal rat ventricular myocytes. Am J Physiol Heart Circ Physiol 280: H756-766.
73. Kehat I, Davis J, Tiburcy M, Accornero F, Saba-El-Leil MK, et al. (2011) Extracellular signal-regulated kinases 1 and 2 regulate the balance between eccentric and concentric cardiac growth. Circ Res 108: 176-183.
74. Miyamoto T, Takeishi Y, Takahashi H, Shishido T, Arimoto T, et al. (2004) Activation of distinct signal transduction pathways in hypertrophied hearts by pressure and volume overload. Basic Res Cardiol 99: 328-337.
75. Matsui T, Nagoshi T, Rosenzweig A, (2005) Akt and PI 3-kinase signaling in cardiomyocyte hypertrophy and survival. Cell Cycle 2: 220-223.
76. Miyamoto S, Rubio M, Sussman MA, (2009) Nuclear and mitochondrial signalling Akts in cardiomyocytes. Cardiovasc Res 82: 272-285.
77. Wang YY, Morimoto S, Du CK, Lu QW, Zhan DY, et al. (2010) Up-regulation of type 2 iodothyronine deiodinase in dilated cardiomyopathy. Cardiovasc Res 87: 636-646.
78. Sasaki H, Asanuma H, Fujita M, Takahama H, Wakeno M, et al. (2009) Metformin prevents progression of heart failure in dogs: role of AMP-activated protein kinase. Circulation 119: 2568-2577.
79. Pepe M, Mamdani M, Zentilin L, Csiszar A, Qanud K, et al. (2010) Intramyocardial VEGF-B167 gene delivery delays the progression towards congestive failure in dogs with pacing-induced dilated cardiomyopathy. Circ Res 106: 1893-1903.
80. Sheikh F, Raskin A, Chu PH, Lange S, Domenighetti AA, et al. (2008) An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice. J Clin Invest 118: 3870-3880.
81. Haq S, Choukroun G, Lim H, Tymitz KM, del Monte F, et al. (2001) Differential activation of signal transduction pathways in human hearts with hypertrophy versus advanced heart failure. Circulation 103: 670-677.
82. Ping P, Zhang J, Pierce WM Jr, Bolli R, (2001) Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ Res 88: 59-62.
83. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, et al. (2003) Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92: 873-880.
84. Miyamoto S, Murphy AN, Brown JH, (2008) Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ 15: 521-529.
85. Reiter JF, Alexander J, Rodaway A, Yelon D, Patient R, et al. (1999) Gata5 is required for the development of the heart and endoderm in zebrafish. Genes Dev 13: 2983-2995.
86. Molkentin JD, Tymitz KM, Richardson JA, Olson EN, (2000) Abnormalities of the genitourinary tract in female mice lacking GATA5. Mol Cell Biol 20: 5256-5260.
87. van der Meer DL, Marques IJ, Leito JT, Besser J, Bakkers J, et al. (2006) Zebrafish cypher is important for somite formation and heart development. Dev Biol 299: 356-372.
88. Zhou Q, Chu PH, Huang C, Cheng CF, Martone ME, et al. (2001) Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J Cell Biol 155: 605-612.