Journal of Molecular and Cellular Cardiology
Volume 49, Issue 5 , Pages 791-800 , November 2010

VAMP-1, VAMP-2, and syntaxin-4 regulate ANP release from cardiac myocytes

  • Marcella Ferlito

      Affiliations

    • Department of Medicine, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
    • Corresponding Author InformationCorresponding author. The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Tel.: +1-410-502-5982.
  • ,
  • William B. Fulton

      Affiliations

    • Department of Pediatric Surgery, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
  • ,
  • Mohamed A. Zauher

      Affiliations

    • Department of Medicine, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
  • ,
  • Eduardo Marbán

      Affiliations

    • Cedars-Sinai Heart Institute, Cedars Sinai, Los Angeles, CA, USA
  • ,
  • Charles Steenbergen

      Affiliations

    • Department of Pathology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
  • ,
  • Charles J. Lowenstein

      Affiliations

    • Department of Medicine, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
    • The University of Rochester Medical Center, Rochester, NY 14534, USA

Received 7 January 2010 ,Revised 19 August 2010 ,Accepted 20 August 2010.

References 

  1. de Bold AJ. Atrial natriuretic factor of the rat heart. Studies on isolation and properties. Proc Soc Exp Biol Med. Jun 1982;170(2):133–138
  2. de Bold AJ, Borenstein HB, Veress AT, Sonnenberg H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci. Jan 5 1981;28(1):89–94
  3. Munagala VK, Burnett JC, Redfield MM. The natriuretic peptides in cardiovascular medicine. Curr Probl Cardiol. Dec 2004;29(12):707–769
  4. John SW, Veress AT, Honrath U, Chong CK, Peng L, Smithies O, et al. Blood pressure and fluid-electrolyte balance in mice with reduced or absent ANP. Am J Physiol. Jul 1996;271(1 Pt 2):R109–R114
  5. Steinhelper ME, Cochrane KL, Field LJ. Hypotension in transgenic mice expressing atrial natriuretic factor fusion genes. Hypertension. Sep 1990;16(3):301–307
  6. Cataliotti A, Burnett JC. Natriuretic peptides: novel therapeutic targets in heart failure. J Investig Med. Nov 2005;53(7):378–384
  7. Lee CY, Burnett JC. Natriuretic peptides and therapeutic applications. Heart Fail Rev. Jun 2007;12(2):131–142
  8. Rose RA, Giles WR. Natriuretic peptide C receptor signalling in the heart and vasculature. J Physiol. Jan 15 2008;586(2):353–366
  9. Ahluwalia A, MacAllister RJ, Hobbs AJ. Vascular actions of natriuretic peptides. Cyclic GMP-dependent and -independent mechanisms. Basic Res Cardiol. Mar 2004;99(2):83–89
  10. de Bold AJ, de Bold ML. Determinants of natriuretic peptide production by the heart: basic and clinical implications. J Investig Med. Nov 2005;53(7):371–377
  11. Yan W, Wu F, Morser J, Wu Q. Corin, a transmembrane cardiac serine protease, acts as a pro-atrial natriuretic peptide-converting enzyme. Proc Natl Acad Sci USA. Jul 18 2000;97(15):8525–8529
  12. Dietz JR. Mechanisms of atrial natriuretic peptide secretion from the atrium. Cardiovasc Res. Oct 1 2005;68(1):8–17
  13. Doubell AF. The effect of calcium antagonists on atrial natriuretic peptide (ANP) release from the rat heart during rapid cardiac pacing. J Mol Cell Cardiol. May 1989;21(5):437–440
  14. Doubell AF, Thibault G. Calcium is involved in both positive and negative modulation of the secretory system for ANP. Am J Physiol. May 1994;266(5 Pt 2):H1854–H1863
  15. Glembotski CC, Irons CE, Sprenkle AB, Sei CA. Studies of ANF processing and secretion using a primary cardiocyte culture model. Can J Physiol Pharmacol. Oct 1991;69(10):1525–1536
  16. Veress AT, Milojevic S, Yip C, Flynn TG, Sonnenberg H. In vitro secretion of atrial natriuretic factor: receptor-mediated release of prohormone. Am J Physiol. May 1988;254(5 Pt 2):R809–R814
  17. Han JH, Cao C, Kim SZ, Cho KW, Kim SH. Decreases in ANP secretion by lysophosphatidylcholine through protein kinase C. Hypertension. Jun 2003;41(6):1380–1385
  18. Bensimon M, Chang AI, de Bold ML, Ponce A, Carreras D, De Bold AJ. Participation of G proteins in natriuretic peptide hormone secretion from heart atria. Endocrinology. Nov 2004;145(11):5313–5321
  19. Iida H, Page E. Inhibition of atrial natriuretic peptide secretion by forskolin in noncontracting cultured atrial myocytes. Biochem Biophys Res Commun. Nov 30 1988;157(1):330–336
  20. Muir TM, Hair J, Inglis GC, Dow JW, Lindop GB, Leckie BJ. Hormonal control of atrial natriuretic peptide synthesis and secretion from cultured atrial myocytes. J Mol Cell Cardiol. May 1993;25(5):509–518
  21. Jahn R, Lang T, Sudhof TC. Membrane fusion. Cell. Feb 21 2003;112(4):519–533
  22. Jahn R, Sudhof TC. Membrane fusion and exocytosis. Annu Rev Biochem. 1999;68:863–911
  23. Mellman I, Warren G. The road taken: past and future foundations of membrane traffic. Cell. Jan 7 2000;100(1):99–112
  24. Sevilla L, Tomas E, Munoz P, Guma A, Fischer Y, Thomas J, et al. Characterization of two distinct intracellular GLUT4 membrane populations in muscle fiber. Differential protein composition and sensitivity to insulin. Endocrinology. Jul 1997;138(7):3006–3015
  25. Kang Y, Leung YM, Manning-Fox JE, Xia F, Xie H, Sheu L, et al. Syntaxin-1A inhibits cardiac KATP channels by its actions on nucleotide binding folds 1 and 2 of sulfonylurea receptor 2A. J Biol Chem. Nov 5 2004;279(45):47125–47131
  26. Peters CG, Miller DF, Giovannucci DR. Identification, localization and interaction of SNARE proteins in atrial cardiac myocytes. J Mol Cell Cardiol. Mar 2006;40(3):361–374
  27. Cingolani E, Ramirez Correa GA, Kizana E, Murata M, Cho HC, Marban E. Gene therapy to inhibit the calcium channel beta subunit: physiological consequences and pathophysiological effects in models of cardiac hypertrophy. Circ Res. Jul 20 2007;101(2):166–175
  28. Ferlito M, Irani K, Faraday N, Lowenstein CJ. Nitric oxide inhibits exocytosis of cytolytic granules from lymphokine-activated killer cells. Proc Natl Acad Sci USA. Aug 1 2006;103(31):11689–11694
  29. Wei YF, Rodi CP, Day ML, Wiegand RC, Needleman LD, Cole BR, et al. Developmental changes in the rat atriopeptin hormonal system. J Clin Invest. May 1987;79(5):1325–1329
  30. Doyle DD, Ambler SK, Upshaw-Earley J, Bastawrous A, Goings GE, Page E. Type B atrial natriuretic peptide receptor in cardiac myocyte caveolae. Circ Res. Jul 1997;81(1):86–91
  31. Jamieson JD, Palade GE. Specific granules in atrial muscle cells. J Cell Biol. Oct 1964;23:151–172
  32. Foster LJ, Yaworsky K, Trimble WS, Klip A. SNAP23 promotes insulin-dependent glucose uptake in 3T3-L1 adipocytes: possible interaction with cytoskeleton. Am J Physiol. May 1999;276(5 Pt 1):C1108–C1114
  33. Lew RA, Baertschi AJ. Endothelial cells stimulate ANF secretion from atrial myocytes in co-culture. Biochem Biophys Res Commun. Sep 15 1989;163(2):701–709
  34. Fukuda Y, Hirata Y, Taketani S, Kojima T, Oikawa S, Nakazato H, et al. Endothelin stimulates accumulations of cellular atrial natriuretic peptide and its messenger RNA in rat cardiocytes. Biochem Biophys Res Commun. Nov 15 1989;164(3):1431–1436
  35. Deitcher DL, Ueda A, Stewart BA, Burgess RW, Kidokoro Y, Schwarz TL. Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J Neurosci. Mar 15 1998;18(6):2028–2039
  36. Schoch S, Deak F, Konigstorfer A, Mozhayeva M, Sara Y, Sudhof TC, et al. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science. Nov 2 2001;294(5544):1117–1122
  37. Montecucco C, Schiavo G. Mechanism of action of tetanus and botulinum neurotoxins. Mol Microbiol. Jul 1994;13(1):1–8
  38. Teter K, Chandy G, Quinones B, Pereyra K, Machen T, Moore HP. Cellubrevin-targeted fluorescence uncovers heterogeneity in the recycling endosomes. J Biol Chem. Jul 31 1998;273(31):19625–19633
  39. Daro E, van der Sluijs P, Galli T, Mellman I. Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc Natl Acad Sci USA. Sep 3 1996;93(18):9559–9564
  40. Hackam DJ, Rotstein OD, Sjolin C, Schreiber AD, Trimble WS, Grinstein S. v-SNARE-dependent secretion is required for phagocytosis. Proc Natl Acad Sci USA. Sep 29 1998;95(20):11691–11696
  41. Schraw TD, Rutledge TW, Crawford GL, Bernstein AM, Kalen AL, Pessin JE, et al. Granule stores from cellubrevin/VAMP-3 null mouse platelets exhibit normal stimulus-induced release. Blood. Sep 1 2003;102(5):1716–1722
  42. Polgar J, Chung SH, Reed GL. Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood. Aug 1 2002;100(3):1081–1083
  43. Volchuk A, Wang Q, Ewart HS, Liu Z, He L, Bennett MK, et al. Syntaxin 4 in 3T3-L1 adipocytes: regulation by insulin and participation in insulin-dependent glucose transport. Mol Biol Cell. Jul 1996;7(7):1075–1082
  44. Tellam JT, Macaulay SL, McIntosh S, Hewish DR, Ward CW, James DE. Characterization of Munc-18c and syntaxin-4 in 3T3-L1 adipocytes. Putative role in insulin-dependent movement of GLUT-4. J Biol Chem. Mar 7 1997;272(10):6179–6186
  45. Miyata T, Ohnishi H, Suzuki J, Yoshikumi Y, Ohno H, Mashima H, et al. Involvement of syntaxin 4 in the transport of membrane-type 1 matrix metalloproteinase to the plasma membrane in human gastric epithelial cells. Biochem Biophys Res Commun. Oct 8 2004;323(1):118–124
  46. Thibault G, Haile-Meskel H, Wrobel-Konrad E, Ballak M, Garcia R, Genest J, et al. Processing of the atrial natriuretic factor propeptide by atrial cardiocytes as revealed by immunocryoultramicrotomy. Endocrinology. Jun 1989;124(6):3109–3116
  47. Slot JW, Garruti G, Martin S, Oorschot V, Posthuma G, Kraegen EW, et al. Glucose transporter (GLUT-4) is targeted to secretory granules in rat atrial cardiomyocytes. J Cell Biol. Jun 16 1997;137(6):1243–1254
  48. Berlin JR. Spatiotemporal changes of Ca2+ during electrically evoked contractions in atrial and ventricular cells. Am J Physiol. Sep 1995;269(3 Pt 2):H1165–H1170
  49. Huser J, Lipsius SL, Blatter LA. Calcium gradients during excitation-contraction coupling in cat atrial myocytes. J Physiol. Aug 1 1996;494(Pt 3):641–651
  50. Mackenzie L, Bootman MD, Berridge MJ, Lipp P. Predetermined recruitment of calcium release sites underlies excitation-contraction coupling in rat atrial myocytes. J Physiol. Feb 1 2001;530(Pt 3):417–429
  51. Yamasaki Y, Furuya Y, Araki K, Matsuura K, Kobayashi M, Ogata T. Ultra-high-resolution scanning electron microscopy of the sarcoplasmic reticulum of the rat atrial myocardial cells. Anat Rec. May 1997;248(1):70–75
  52. Franzini-Armstrong C, Protasi F, Tijskens P. The assembly of calcium release units in cardiac muscle. Ann NY Acad Sci. Jun 2005;1047:76–85
  53. Bootman MD, Higazi DR, Coombes S, Roderick HL. Calcium signalling during excitation-contraction coupling in mammalian atrial myocytes. J Cell Sci. Oct 1 2006;119(Pt 19):3915–3925
  54. Kockskamper J, Sheehan KA, Bare DJ, Lipsius SL, Mignery GA, Blatter LA. Activation and propagation of Ca(2+) release during excitation-contraction coupling in atrial myocytes. Biophys J. Nov 2001;81(5):2590–2605
  55. Giraudo CG, Eng WS, Melia TJ, Rothman JE. A clamping mechanism involved in SNARE-dependent exocytosis. Science. Aug 4 2006;313(5787):676–680
  56. Schaub JR, Lu X, Doneske B, Shin YK, McNew JA. Hemifusion arrest by complexin is relieved by Ca2+-synaptotagmin I. Nat Struct Mol Biol. Aug 2006;13(8):748–750
  57. Tang J, Maximov A, Shin OH, Dai H, Rizo J, Sudhof TC. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell. Sep 22 2006;126(6):1175–1187
  58. Ren Q, Barber HK, Crawford GL, Karim ZA, Zhao C, Choi W, et al. Endobrevin/VAMP-8 is the primary v-SNARE for the platelet release reaction. Mol Biol Cell. Jan 2007;18(1):24–33

PII: S0022-2828(10)00321-4

doi: 10.1016/j.yjmcc.2010.08.020

Journal of Molecular and Cellular Cardiology
Volume 49, Issue 5 , Pages 791-800 , November 2010