Annexin A7 and SNAP23 interactions in alveolar type II cells and in vitro: A role for Ca2+ and PKC

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 10, 2012, Pages 1796-1806

  Gerelsaikhan, Tudevdagva ^a   Vasa, Pavan Kumar ^a   Chander, Avinash ^a  

^a STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Exocytosis; Lamellar body; Lung surfactant secretion; Membrane fusion; Protein kinase C; T SNARE protein

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A3; CALCIMYCIN; CALCIUM; MEMBRANE PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PROTEIN SNAP23; RECOMBINANT PROTEIN; SNARE PROTEIN; SYNEXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOFLUORESCENCE; IMMUNOLOCALIZATION; IN VITRO STUDY; LAMELLAR BODY; LUNG ALVEOLUS CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; ANNEXIN A7; ANTIBODIES; ATP-BINDING CASSETTE TRANSPORTERS; CALCIMYCIN; CALCIUM; PHOSPHORYLATION; PNEUMOCYTES; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; SNARE PROTEINS; TETRADECANOYLPHORBOL ACETATE; VESICULAR TRANSPORT PROTEINS;

EID: 84864764963     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.06.010     Document Type: Article

References (51)

1. Rooney S.A. Regulation of surfactant secretion. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2001, 129:233-243.
2. Andreeva A.V., Kutuzov M.A., Voyno-Yasenetskaya T.A. Regulation of surfactant secretion in alveolar type II cells. Am. J. Physiol. 2007, 293:L259-L271.
3. Chander A., Fisher A.B. Regulation of lung surfactant secretion. Am. J. Physiol. 1990, 258:L241-L253.
4. Chander A., Wu R.D. In vitro fusion of lung lamellar bodies and plasma membrane is augmented by lung synexin. Biochim. Biophys. Acta 1991, 1086:157-166.
5. Chander A., Sen N., Spitzer A.R. Synexin and GTP increase surfactant secretion in permeabilized alveolar type II cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2001, 280:L991-L998.
6. Chander A., Chen X.L., Naidu D.G. A role for diacylglycerol in annexin A7-mediated fusion of lung lamellar bodies. Biochim. Biophys. Acta 2007, 1771:1308-1318.
7. Dietrich L.E., Boeddinghaus C., LaGrassa T.J., Ungermann C. Control of eukaryotic membrane fusion by N-terminal domains of SNARE proteins. Biochim. Biophys. Acta 2003, 1641:111-119.
8. Fasshauer D. Structural insights into the SNARE mechanism. Biochim. Biophys. Acta 2003, 1641:87-97.
9. Gerst J.E. SNARE regulators: matchmakers and matchbreakers. Biochim. Biophys. Acta 2003, 1641:99-110.
10. Rothman J.E. Mechanisms of intracellular protein transport. Nature 1994, 372:55-63.
11. Mayer A. Membrane fusion in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 2002, 18:289-314.
12. Paumet F., Rahimian V., Rothman J.E. The specificity of SNARE-dependent fusion is encoded in the SNARE motif. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3376-3380.
13. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Bendito G., Molnar Z., Becher M.W., Valenzuela C.F., Partridge L.D., Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 2002, 5:19-26.
14. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science (New York, N.Y.) 2001, 294:1117-1122.
15. Liu L., Wang M., Fisher A.B., Zimmerman U.J. Involvement of annexin II in exocytosis of lamellar bodies from alveolar epithelial type II cells. Am. J. Physiol. 1996, 270:L668-L676.
16. Chattopadhyay S., Sun P., Wang P., Abonyo B., Cross N.L., Liu L. Fusion of lamellar body with plasma membrane is driven by the dual action of annexin II tetramer and arachidonic acid. J. Biol. Chem. 2003, 278:39675-39683.
17. Hong K., Duzgunes N., Ekerdt R., Papahadjopoulos D. Synexin facilitates fusion of specific phospholipid membranes at divalent cation concentrations found intracellularly. Proc. Natl. Acad. Sci. U. S. A. 1982, 79:4642-4644.
18. Caohuy H., Pollard H.B. Activation of annexin 7 by protein kinase C in vitro and in vivo. J. Biol. Chem. 2001, 276:12813-12821.
19. Sen N., Spitzer A.R., Chander A. Calcium-dependence of synexin binding may determine aggregation and fusion of lamellar bodies. Biochem. J. 1997, 322(Pt 1):103-109.
20. Abonyo B.O., Gou D., Wang P., Narasaraju T., Wang Z., Liu L. Syntaxin 2 and SNAP-23 are required for regulated surfactant secretion. Biochemistry 2004, 43:3499-3506.
21. Wang P., Chintagari N.R., Gou D., Su L., Liu L. Physical and functional interactions of SNAP-23 with annexin A2. Am. J. Respir. Cell Mol. Biol. 2007, 37:467-476.
22. Chander A., Sen N., Naidu D.G., Spitzer A.R. Calcium ionophore and phorbol ester increase membrane binding of annexin a7 in alveolar type II cells. Cell Calcium 2003, 33:11-17.
23. Gerelsaikhan T., Chen X.L., Chander A. Secretagogues of lung surfactant increase annexin A7 localization with ABCA3 in alveolar type II cells. Biochim. Biophys. Acta 2011, 1813:2017-2025.
24. Yamano G., Funahashi H., Kawanami O., Zhao L.X., Ban N., Uchida Y., Morohoshi T., Ogawa J., Shioda S., Inagaki N. ABCA3 is a lamellar body membrane protein in human lung alveolar type II cells. FEBS Lett. 2001, 508:221-225.
25. Mulugeta S., Gray J.M., Notarfrancesco K.L., Gonzales L.W., Koval M., Feinstein S.I., Ballard P.L., Fisher A.B., Shuman H. Identification of LBM180, a lamellar body limiting membrane protein of alveolar type II cells, as the ABC transporter protein ABCA3. J. Biol. Chem. 2002, 277:22147-22155.
26. Chander A., Sen N. Inhibition of phosphatidylcholine secretion by stilbene disulfonates in alveolar type II cells. Biochem. Pharmacol. 1993, 45:1905-1912.
27. Chander A., Johnson R.G., Reicherter J., Fisher A.B. Lung lamellar bodies maintain an acidic internal pH. J. Biol. Chem. 1986, 261:6126-6131.
28. 2-terminus affects physical characteristics and membrane binding, aggregation, and fusion properties of annexin A7. Biochim. Biophys. Acta 2005, 1734:152-168.
29. Bers D.M. A simple method for the accurate determination of free [Ca] in Ca-EGTA solutions. Am. J. Physiol. 1982, 242:C404-C408.
30. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
31. Chander A., Sen N., Wu A.M., Spitzer A.R. Protein kinase C in ATP regulation of lung surfactant secretion in type II cells. Am. J. Physiol. 1995, 268:L108-L116.
32. Linke M.J., Burton F.M., Fiedeldey D.T., Rice W.R. Surfactant phospholipid secretion from rat alveolar type II cells: possible role of PKC isozymes. Am. J. Physiol. 1997, 272:L171-L177.
33. Gerke V., Moss S.E. Annexins and membrane dynamics. Biochim. Biophys. Acta 1997, 1357:129-154.
34. Raynal P., Pollard H.B. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1994, 1197:63-93.
35. Johnstone S.A., Hubaishy I., Waisman D.M. Phosphorylation of annexin II tetramer by protein kinase C inhibits aggregation of lipid vesicles by the protein. J. Biol. Chem. 1992, 267:25976-25981.
36. Lau C.G., Takayasu Y., Rodenas-Ruano A., Paternain A.V., Lerma J., Bennett M.V., Zukin R.S. SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J. Neurosci. 2010, 30:242-254.
37. Rickman C., Davletov B. Mechanism of calcium-independent synaptotagmin binding to target SNAREs. J. Biol. Chem. 2003, 278:5501-5504.
38. Quetglas S., Iborra C., Sasakawa N., De Haro L., Kumakura K., Sato K., Leveque C., Seagar M. Calmodulin and lipid binding to synaptobrevin regulates calcium-dependent exocytosis. EMBO J. 2002, 21:3970-3979.
39. 2+/calmodulin-activated protein kinase II to syntaxin 1A. J. Neurosci. 2002, 22:3342-3351.
40. Condliffe S.B., Zhang H., Frizzell R.A. Syntaxin 1A regulates ENaC channel activity. J. Biol. Chem. 2004, 279:10085-10092.
41. Edelmann L., Hanson P.I., Chapman E.R., Jahn R. Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J. 1995, 14:224-231.
42. Duman J.G., Forte J.G. What is the role of SNARE proteins in membrane fusion?. Am. J. Physiol. Cell Physiol. 2003, 285:C237-C249.
43. Fukuda M. Vesicle-associated membrane protein-2/synaptobrevin binding to synaptotagmin I promotes O-glycosylation of synaptotagmin I. J. Biol. Chem. 2002, 277:30351-30358.
44. 2+-triggered dimerization. J. Biol. Chem. 1996, 271:5844-5849.
45. Sutton R.B., Ernst J.A., Brunger A.T. Crystal structure of the cytosolic C2A-C2B domains of synaptotagmin III. Implications for Ca(+2)-independent snare complex interaction. J. Cell Biol. 1999, 147:589-598.
46. Bai J., Tucker W.C., Chapman E.R. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat. Struct. Mol. Biol. 2004, 11:36-44.
47. Fernandez-Chacon R., Konigstorfer A., Gerber S.H., Garcia J., Matos M.F., Stevens C.F., Brose N., Rizo J., Rosenmund C., Sudhof T.C. Synaptotagmin I functions as a calcium regulator of release probability. Nature 2001, 410:41-49.
48. 2+ affinity of synaptotagmin 1. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18664-18669.
49. Herrick D.Z., Kuo W., Huang H., Schwieters C.D., Ellena J.F., Cafiso D.S. Solution and membrane-bound conformations of the tandem C2A and C2B domains of synaptotagmin 1: evidence for bilayer bridging. J. Mol. Biol. 2009, 390:913-923.
50. Caohuy H., Pollard H.B. Protein kinase C and guanosine triphosphate combine to potentiate calcium-dependent membrane fusion driven by annexin 7. J. Biol. Chem. 2002, 277:25217-25225.
51. 2+/GTP sensor in exocytotic secretion. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:10797-10802.