Grk5l controls heart development by limiting mTOR signaling during symmetry breaking

Cell Reports

Volumn 4, Issue 4, 2013, Pages 625-632

  Burkhalter, Martin D ^a   Fralish, Gregory B ^b   Premont, Richard T ^b   Caron, Marc G ^b   Philipp, Melanie ^c  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR KINASE 5; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1;

ANIMAL TISSUE; ARTICLE; CILIARY MOTILITY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; HEART DEVELOPMENT; HEART FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; G-PROTEIN-COUPLED RECEPTOR KINASE 5; HEART; HEK293 CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MYOCARDIUM; ORGANOGENESIS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; MAMMALIA;

EID: 84883288744     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.036     Document Type: Article

References (36)

1. Amack J.D., Yost H.J. The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr. Biol. 2004, 14:685-690.
2. Bisgrove B.W., Essner J.J., Yost H.J. Regulation of midline development by antagonism of lefty and nodal signaling. Development 1999, 126:3253-3262.
3. Boehlke C., Kotsis F., Patel V., Braeg S., Voelker H., Bredt S., Beyer T., Janusch H., Hamann C., Gödel M., et al. Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat. Cell Biol. 2010, 12:1115-1122.
4. Caron A., Xu X., Lin X. Wnt/β-catenin signaling directly regulates Foxj1 expression and ciliogenesis in zebrafish Kupffer's vesicle. Development 2012, 139:514-524.
5. Chen E.P., Bittner H.B., Akhter S.A., Koch W.J., Davis R.D. Myocardial function in hearts with transgenic overexpression of the G protein-coupled receptor kinase 5. Ann. Thorac. Surg. 2001, 71:1320-1324.
6. Chen M., Philipp M., Wang J., Premont R.T., Garrison T.R., Caron M.G., Lefkowitz R.J., Chen W. G Protein-coupled receptor kinases phosphorylate LRP6 in the Wnt pathway. J.Biol. Chem. 2009, 284:35040-35048.
7. DiBella L.M., Park A., Sun Z. Zebrafish Tsc1 reveals functional interactions between the cilium and the TOR pathway. Hum. Mol. Genet. 2009, 18:595-606.
8. Eckhart A.D., Duncan S.J., Penn R.B., Benovic J.L., Lefkowitz R.J., Koch W.J. Hybrid transgenic mice reveal invivo specificity of G protein-coupled receptor kinases in the heart. Circ. Res. 2000, 86:43-50.
9. Essner J.J., Vogan K.J., Wagner M.K., Tabin C.J., Yost H.J., Brueckner M. Conserved function for embryonic nodal cilia. Nature 2002, 418:37-38.
10. Fujinaga M., Hoffman B.B., Baden J.M. Receptor subtype and intracellular signal transduction pathway associated with situs inversus induced by alpha 1 adrenergic stimulation in rat embryos. Dev. Biol. 1994, 162:558-567.
11. Gainetdinov R.R., Bohn L.M., Walker J.K., Laporte S.A., Macrae A.D., Caron M.G., Lefkowitz R.J., Premont R.T. Muscarinic supersensitivity and impaired receptor desensitization in G protein-coupled receptor kinase 5-deficient mice. Neuron 1999, 24:1029-1036.
12. Gainetdinov R.R., Bohn L.M., Sotnikova T.D., Cyr M., Laakso A., Macrae A.D., Torres G.E., Kim K.M., Lefkowitz R.J., Caron M.G., Premont R.T. Dopaminergic supersensitivity in G protein-coupled receptor kinase 6-deficient mice. Neuron 2003, 38:291-303.
13. Gold J.I., Gao E., Shang X., Premont R.T., Koch W.J. Determining the absolute requirement of G protein-coupled receptor kinase 5 for pathological cardiac hypertrophy: short communication. Circ. Res. 2012, 111:1048-1053.
14. Huang S., Ma J., Liu X., Zhang Y., Luo L. Retinoic acid signaling sequentially controls visceral and heart laterality in zebrafish. J.Biol. Chem. 2011, 286:28533-28543.
15. Huang Z.M., Gold J.I., Koch W.J. G protein-coupled receptor kinases in normal and failing myocardium. Front. Biosci. 2011, 17:3047-3060.
16. Jaffe K.M., Thiberge S.Y., Bisher M.E., Burdine R.D. Imaging cilia in zebrafish. Methods Cell Biol. 2010, 97:415-435.
17. Liggett S.B., Cresci S., Kelly R.J., Syed F.M., Matkovich S.J., Hahn H.S., Diwan A., Martini J.S., Sparks L., Parekh R.R., et al. A GRK5 polymorphism that inhibits beta-adrenergic receptor signaling is protective in heart failure. Nat. Med. 2008, 14:510-517.
18. Martini J.S., Raake P., Vinge L.E., DeGeorge B.R., Chuprun J.K., Harris D.M., Gao E., Eckhart A.D., Pitcher J.A., Koch W.J. Uncovering G protein-coupled receptor kinase-5 as a histone deacetylase kinase in the nucleus of cardiomyocytes. Proc. Natl. Acad. Sci. USA 2008, 105:12457-12462.
19. Michal A.M., So C.H., Beeharry N., Shankar H., Mashayekhi R., Yen T.J., Benovic J.L. G Protein-coupled receptor kinase 5 is localized to centrosomes and regulates cell cycle progression. J.Biol. Chem. 2012, 287:6928-6940.
20. Okada Y., Takeda S., Tanaka Y., Izpisúa Belmonte J.C., Hirokawa N. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 2005, 121:633-644.
21. Oteíza P., Köppen M., Concha M.L., Heisenberg C.P. Origin and shaping of the laterality organ in zebrafish. Development 2008, 135:2807-2813.
22. Pearce L.R., Alton G.R., Richter D.T., Kath J.C., Lingardo L., Chapman J., Hwang C., Alessi D.R. Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem. J. 2010, 431:245-255.
23. Philipp M., Fralish G.B., Meloni A.R., Chen W., MacInnes A.W., Barak L.S., Caron M.G. Smoothened signaling in vertebrates is facilitated by a G protein-coupled receptor kinase. Mol. Biol. Cell 2008, 19:5478-5489.
24. Pierpont M.E., Basson C.T., Benson D.W., Gelb B.D., Giglia T.M., Goldmuntz E., McGee G., Sable C.A., Srivastava D., Webb C.L. Genetic basis for congenital heart defects: current knowledge: a scientific statement from the American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. Circulation 2007, 115:3015-3038. American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young.
25. Premont R.T., Gainetdinov R.R. Physiological roles of G protein-coupled receptor kinases and arrestins. Annu. Rev. Physiol. 2007, 69:511-534.
26. Premont R.T., Macrae A.D., Aparicio S.A., Kendall H.E., Welch J.E., Lefkowitz R.J. The GRK4 subfamily of G protein-coupled receptor kinases. Alternative splicing, gene organization, and sequence conservation. J.Biol. Chem. 1999, 274:29381-29389.
27. Ramsdell A.F. Left-right asymmetry and congenital cardiac defects: getting to the heart of the matter in vertebrate left-right axis determination. Dev. Biol. 2005, 288:1-20.
28. Rockman H.A., Choi D.J., Rahman N.U., Akhter S.A., Lefkowitz R.J., Koch W.J. Receptor-specific invivo desensitization by the G protein-coupled receptor kinase-5 in transgenic mice. Proc. Natl. Acad. Sci. USA 1996, 93:9954-9959.
29. Rosner M., Schipany K., Hengstschläger M. p70 S6K1 nuclear localization depends on its mTOR-mediated phosphorylation at T389, but not on its kinase activity towards S6. Amino Acids 2012, 42:2251-2256.
30. Schilling T.F., Concordet J.P., Ingham P.W. Regulation of left-right asymmetries in the zebrafish by Shh and BMP4. Dev. Biol. 1999, 210:277-287.
31. Sorriento D., Santulli G., Fusco A., Anastasio A., Trimarco B., Iaccarino G. Intracardiac injection of AdGRK5-NT reduces left ventricular hypertrophy by inhibiting NF-kappaB-dependent hypertrophic gene expression. Hypertension 2010, 56:696-704.
32. Sun Z., Amsterdam A., Pazour G.J., Cole D.G., Miller M.S., Hopkins N. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 2004, 131:4085-4093.
33. Sutherland M.J., Ware S.M. Disorders of left-right asymmetry: heterotaxy and situs inversus. Am. J. Med. Genet. C. Semin. Med. Genet. 2009, 151C:307-317.
34. Yuan S., Li J., Diener D.R., Choma M.A., Rosenbaum J.L., Sun Z. Target-of-rapamycin complex 1 (Torc1) signaling modulates cilia size and function through protein synthesis regulation. Proc. Natl. Acad. Sci. USA 2012, 109:2021-2026.
35. Zoncu R., Efeyan A., Sabatini D.M. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 2011, 12:21-35.
36. Zullo A., Iaconis D., Barra A., Cantone A., Messaddeq N., Capasso G., Dollé P., Igarashi P., Franco B. Kidney-specific inactivation of Ofd1 leads to renal cystic disease associated with upregulation of the mTOR pathway. Hum. Mol. Genet. 2010, 19:2792-2803.