The C-terminus of the long AKAP13 isoform (AKAP-Lbc) is critical for development of compensatory cardiac hypertrophy

Journal of Molecular and Cellular Cardiology

Volumn 66, Issue , 2014, Pages 27-40

  Taglieri, Domenico M ^a   Johnson, Keven R ^a   Burmeister, Brian T ^a   Monasky, Michelle M ^a   Spindler, Matthew J ^b   DeSantiago, Jaime ^a   Banach, Kathrin ^a   Conklin, Bruce R ^b   Carnegie, Graeme K ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

Author keywords

A Kinase Anchoring Protein (AKAP); Cardiac hypertrophy; Heart failure; Protein kinase D

Indexed keywords

A KINASE ANCHORING PROTEIN LBC; ANGIOTENSIN II; COLLAGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; HISTONE DEACETYLASE 5; PHENYLEPHRINE; PROTEIN KINASE D; PROTEIN KINASE D1; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GENE EXPRESSION; HEART FAILURE; HEART HYPERTROPHY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

MUS;

1M; A-KINASE ANCHORING PROTEIN (AKAP); ANGIOTENSIN II; AT-II; CARDIAC HYPERTROPHY; E/A RATIO; EARLY (E) TO LATE (ATRIAL A) VENTRICULAR FILLING VELOCITY RATIO; EDT; EDV; EF; EJECTION FRACTION; END-DIASTOLIC VOLUME; ENDOTHELIN1; ET1; FRACTIONAL SHORTENING; FS; G PROTEIN COUPLED RECEPTOR; GPCR; HDAC5; HEART FAILURE; HEART WEIGHT TO BODY WEIGHT RATIO; HISTONE DEACETYLASE 5; HOP; HW/BW; HYDROXYPROLINE; LEFT VENTRICULAR DIASTOLIC ANTERIOR WALL THICKNESS; LEFT VENTRICULAR DIASTOLIC POSTERIOR WALL THICKNESS; LEFT VENTRICULAR/VENTRICLE; LV; LVAWD; LVPWD; ONE MONTH; PE; PHENYLEPHRINE; PKA; PKC; PKD; PROTEIN KINASE A; PROTEIN KINASE C; PROTEIN KINASE D; TAC; TRANSMITRAL EARLY FILLING DECELERATION TIME; TRANSVERSE AORTIC CONSTRICTION; WILD TYPE; WT;

A KINASE ANCHOR PROTEINS; ANGIOTENSIN II; ANIMALS; AORTA; APOPTOSIS; CARDIOMEGALY; COLLAGEN; FEMALE; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEART FAILURE; HISTONE DEACETYLASES; MALE; MICE; MICE, TRANSGENIC; MYOCARDIUM; PHENYLEPHRINE; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84888272031     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.10.010     Document Type: Article

References (58)

1. Chien K.R., Olson E.N. Converging pathways and principles in heart development and disease. Cell 2002, 110(2):153-162.
2. Mudd J.O., Kass D.A. Tackling heart failure in the twenty-first century. Nature 2008, 451(7181):919-928.
3. Carnegie G.K., Means C.K., Scott J.D. A-kinase anchoring proteins: from protein complexes to physiology and disease. IUBMB Life 2009, 61(4):394-406.
4. Mauban J.R., O'Donnell M., Warrier S., Manni S., Bond M. AKAP-scaffolding proteins and regulation of cardiac physiology. Physiology (Bethesda) 2009, 24:78-87.
5. Carnegie G.K., Burmeister B.T. A-kinase anchoring proteins that regulate cardiac remodeling. J Cardiovasc Pharmacol 2011, 58(5):451-458.
6. Hulme J.T., Lin T.W., Westenbroek R.E., Scheuer T., Catterall W.A. Beta-adrenergic regulation requires direct anchoring of PKA to cardiac CaV1.2 channels via a leucine zipper interaction with A kinase-anchoring protein 15. Proc Natl Acad Sci U S A 2003, 100(22):13093-13098.
7. Lygren B., Carlson C.R., Santamaria K., Lissandron V., McSorley T., Litzenberg J., et al. AKAP complex regulates Ca2+ re-uptake into heart sarcoplasmic reticulum. EMBO Rep 2007, 8(11):1061-1067.
8. Kapiloff M.S., Schillace R.V., Westphal A.M., Scott J.D. mAKAP: an A-kinase anchoring protein targeted to the nuclear membrane of differentiated myocytes. J Cell Sci 1999, 112(Pt 16):2725-2736.
9. Russell M.A., Lund L.M., Haber R., McKeegan K., Cianciola N., Bond M. The intermediate filament protein, synemin, is an AKAP in the heart. Arch Biochem Biophys 2006, 456(2):204-215.
10. Reynolds J.G., McCalmon S.A., Tomczyk T., Naya F.J. Identification and mapping of protein kinase A binding sites in the costameric protein myospryn. Biochim Biophys Acta 2007, 1773(6):891-902.
11. Sumandea C.A., Garcia-Cazarin M.L., Bozio C.H., Sievert G.A., Balke C.W., Sumandea M.P. Cardiac troponin T, a sarcomeric AKAP, tethers protein kinase A at the myofilaments. J Biol Chem 2011, 286(1):530-541.
12. Aye T.T., Soni S., van Veen T.A., van der Heyden M.A., Cappadona S., Varro A. Reorganized PKA-AKAP associations in the failing human heart. J Mol Cell Cardiol Feb. 2012, 52(2):511-518.
13. Diviani D., Soderling J., Scott J.D. AKAP-Lbc anchors protein kinase A and nucleates Galpha 12-selective Rho-mediated stress fiber formation. J Biol Chem 2001, 276(47):44247-44257.
14. Toksoz D., Williams D.A. Novel human oncogene lbc detected by transfection with distinct homology regions to signal transduction proteins. Oncogene 1994, 9(2):621-628.
15. Carnegie G.K., Smith F.D., McConnachie G., Langeberg L.K., Scott J.D. AKAP-Lbc nucleates a protein kinase D activation scaffold. Mol Cell 2004, 15:889-899.
16. Cariolato L., Cavin S., Diviani D. A-kinase anchoring protein (AKAP)-Lbc anchors a PKN-based signaling complex involved in alpha1-adrenergic receptor-induced p38 activation. J Biol Chem 2011, 286(10):7925-7937.
17. Smith F.D., Langeberg L.K., Cellurale C., Pawson T., Morrison D.K., Davis R.J., et al. AKAP-Lbc enhances cyclic AMP control of the ERK1/2 cascade. Nat Cell Biol 2010, 12(12):1242-1249.
18. Del Vescovo C.D., Cotecchia S., Diviani D. Akap-Lbc anchors IKKbeta to support interleukin-6-mediated cardiomyocyte hypertrophy. Mol Cell Biol Jan. 2013, 33(1):14-27.
19. Burmeister B.T., Taglieri D.M., Wang L., Carnegie G.K. SH2 domain-containing phosphatase 2 (Shp2) is a component of the AKAP-Lbc complex and is inhibited by protein kinase A (PKA) under pathological hypertrophic conditions in the heart. J Biol Chem Nov. 2012, 287(48):40535-40546.
20. Mayers C.M., Wadell J., McLean K., Venere M., Malik M., Shibata T., et al. The Rho guanine nucleotide exchange factor AKAP13 (BRX) is essential for cardiac development in mice. J Biol Chem 2010, 285(16):12344-12354.
21. Carnegie G.K., Soughayer J., Smith F.D., Pedroja B.S., Zhang F., Diviani D., et al. AKAP-Lbc mobilizes a cardiac hypertrophy signaling pathway. Mol Cell 2008, 32(2):169-179.
22. Appert-Collin A., Cotecchia S., Nenniger-Tosato M., Pedrazzini T., Diviani D. The A-kinase anchoring protein (AKAP)-Lbc-signaling complex mediates alpha1 adrenergic receptor-induced cardiomyocyte hypertrophy. Proc Natl Acad Sci U S A 2007, 104(24):10140-10145.
23. Heineke J., Molkentin J.D. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006, 7(8):589-600.
24. Hill J.A., Olson E.N. Cardiac plasticity. N Engl J Med 2008, 358(13):1370-1380.
25. Haworth R.S., Goss M.W., Rozengurt E., Avkiran M. Expression and activity of protein kinase D/protein kinase C mu in myocardium: evidence for alpha1-adrenergic receptor- and protein kinase C-mediated regulation. J Mol Cell Cardiol 2000, 32(6):1013-1023.
26. Avkiran M., Rowland A.J., Cuello F., Haworth R.S. Protein kinase d in the cardiovascular system: emerging roles in health and disease. Circ Res 2008, 102(2):157-163.
27. Bossuyt J., Chang C.W., Helmstadter K., Kunkel M.T., Newton A.C., Campbell K.S. Spatiotemporally distinct PKD activation in adult cardiomyocytes in response to phenylephrine and endothelin. J Biol Chem Sep. 2011, 286(38):33390-33400.
28. McKinsey T.A., Zhang C.L., Olson E.N. Identification of a signal-responsive nuclear export sequence in class II histone deacetylases. Mol Cell Biol 2001, 21(18):6312-6321.
29. Vega R.B., Harrison B.C., Meadows E., Roberts C.R., Papst P.J., Olson E.N., et al. Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 2004, 24(19):8374-8385.
30. Spindler M.J., Burmeister B.T., Huang Y., Hsiao E.C., Salomonis N., Scott M.J., et al. AKAP13 Rho-GEF and PKD-binding domain deficient mice develop normally but have an abnormal response to β-adrenergic-induced cardiac hypertrophy. PLoS ONE Apr 26 2013, 8(4).
31. Skarnes W.C. Gene trapping methods for the identification and functional analysis of cell surface proteins in mice. Methods Enzymol 2000, 328:592-615.
32. Hastie C.J., McLauchlan H.J., Cohen P. Assay of protein kinases using radiolabeled ATP: a protocol. Nat Protoc 2006, 1(2):968-971.
33. Tanabe S., Kreutz B., Suzuki N., Kozasa T. Regulation of RGS-RhoGEFs by Galpha12 and Galpha13 proteins. Methods Enzymol 2004, 390:285-294.
34. DeSantiago J., Bare D.J., Semenov I., Minshall R.D., Geenen D.L., Wolska B.M., et al. Excitation-contraction coupling in ventricular myocytes is enhanced by paracrine signaling from mesenchymal stem cells. J Mol Cell Cardiol 2012, 52(6):1249-1256.
35. Taglieri D.M., Monasky M.M., Knezevic I., Sheehan K.A., Lei M., Wang X., et al. Ablation of p21-activated kinase-1 in mice promotes isoproterenol-induced cardiac hypertrophy in association with activation of Erk1/2 and inhibition of protein phosphatase 2A. J Mol Cell Cardiol 2011, 51(6):988-996.
36. deAlmeida A.C., van Oort R.J., Wehrens X.H. Transverse aortic constriction in mice. J Vis Exp 2010, (38).
37. Picard M.H., Adams D., Bierig S.M., Dent J.M., Douglas P.S., Gillam L.D., et al. American Society of Echocardiography recommendations for quality echocardiography laboratory operations. J Am Soc Echocardiogr 2011, 24(1):1-10.
38. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3(6):1101-1108.
39. Baisamy L., Jurisch N., Diviani D. Leucine zipper-mediated homo-oligomerization regulates the Rho-GEF activity of AKAP-Lbc. J Biol Chem Apr 15 2005, 280(15):15405-15412.
40. Hong K.W., Lim J.E., Oh B. A regulatory SNP in AKAP13 is associated with blood pressure in Koreans. J Hum Genet Mar 2011, 56(3):205-210.
41. Christoffersen T.E., Aplin M., Strom C.C., Sheikh S.P., Skott O., Busk P.K., et al. Increased natriuretic peptide receptor A and C gene expression in rats with pressure-overload cardiac hypertrophy. Am J Physiol Heart Circ Physiol Apr 2006, 290(4):H1635-H1641.
42. Schwartz K., Carrier L., Chassagne C., Wisnewsky C., Boheler K.R. Regulation of myosin heavy chain and actin isogenes during cardiac growth and hypertrophy. Symp Soc Exp Biol 1992, 46:265-272.
43. Dorn G.W., Robbins J., Ball N., Walsh R.A. Myosin heavy chain regulation and myocyte contractile depression after LV hypertrophy in aortic-banded mice. Am J Physiol Heart Circ Physiol 1994, 267(1):H400-H405.
44. Potthoff M.J., Olson E.N. MEF2: a central regulator of diverse developmental programs. Development Dec 2007, 134(23):4131-4140.
45. el Azzouzi H., van Oort R.J., van der Nagel R., Sluiter W., Bergmann M.W., De Windt L.J. MEF2 transcriptional activity maintains mitochondrial adaptation in cardiac pressure overload. Eur J Heart Fail Jan 2010, 12(1):4-12.
46. Goodall M.H., Wardlow R.D., Goldblum R.R., Ziman A., Lederer W.J., Randall W., et al. Novel function of cardiac protein kinase D1 as a dynamic regulator of Ca2+ sensitivity of contraction. J Biol Chem 2010, 285(53):41686-41700.
47. Aita Y., Kurebayashi N., Hirose S., Maturana A.D. Protein kinase D regulates the human cardiac L-type voltage-gated calcium channel through serine 1884. FEBS Lett 2011, 585(24):3903-3906.
48. Koncz P., Szanda G., Fulop L., Rajki A., Spat A. Mitochondrial Ca2+ uptake is inhibited by a concerted action of p38 MAPK and protein kinase D. Cell Calcium 2009, 46(2):122-129.
49. Bardswell S.C., Cuello F., Rowland A.J., Sadayappan S., Robbins J., Gautel M., et al. Distinct sarcomeric substrates are responsible for protein kinase D-mediated regulation of cardiac myofilament Ca2+ sensitivity and cross-bridge cycling. J Biol Chem 2010, 285(8):5674-5682.
50. Cuello F., Bardswell S.C., Haworth R.S., Yin X., Lutz S., Wieland T., et al. Protein kinase D selectively targets cardiac troponin I and regulates myofilament Ca2+ sensitivity in ventricular myocytes. Circ Res 2007, 100(6):864-873.
51. Ozgen N., Guo J., Gertsberg Z., Danilo P., Rosen M.R., Steinberg S.F. Reactive oxygen species decrease cAMP response element binding protein expression in cardiomyocytes via a protein kinase D1-dependent mechanism that does not require Ser133 phosphorylation. Mol Pharmacol 2009, 76(4):896-902.
52. Storz P., Doppler H., Toker A. Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol Cell Biol 2005, 25(19):8520-8530.
53. Stetler R.A., Gao Y., Zhang L., Weng Z., Zhang F., Hu X., et al. Phosphorylation of HSP27 by protein kinase D is essential for mediating neuroprotection against ischemic neuronal injury. J Neurosci 2011, 32(8):2667-2682.
54. Xiang S.Y., Vanhoutte D., Del Re D.P., Purcell N.H., Ling H., Banerjee I., et al. RhoA protects the mouse heart against ischemia/reperfusion injury. J Clin Invest 2011, 121(8):3269-3276.
55. Steinberg S.F. Regulation of protein kinase D1 activity. Mol Pharmacol 2012, 81(3):284-291.
56. Baicu C.F., Stroud J.D., Livesay V.A., Hapke E., Holder J., Spinale F.G., et al. Changes in extracellular collagen matrix alter myocardial systolic performance. Am J Physiol Heart Circ Physiol 2003, 284(1):H122-H132.
57. Fielitz J., Kim M.S., Shelton J.M., Qi X., Hill J.A., Richardson J.A., et al. Requirement of protein kinase D1 for pathological cardiac remodeling. Proc Natl Acad Sci U S A 2008, 105(8):3059-3063.
58. Massare J., Berry J.M., Luo X., Rob F., Johnstone J.L., Shelton J.M., et al. Diminished cardiac fibrosis in heart failure is associated with altered ventricular arrhythmia phenotype. J Cardiovasc Electrophysiol 2010, 21(9):1031-1037.