Annexin A7 trafficking to alveolar type II cell surface: Possible roles for protein insertion into membranes and lamellar body secretion

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 5, 2013, Pages 1244-1255

  Chander, Avinash ^a   Gerelsaikhan, Tudevdagva ^a   Vasa, Pavan K ^a   Holbrook, Kelly ^a  

^a STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Biotin labeling of proteins; Fluorescence quenching; Immuno fluorescence; Lung surfactant secretion; Protein cross linking

Indexed keywords

SYNEXIN;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; IMMUNOHISTOCHEMISTRY; LAMELLAR BODY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION;

ANIMALS; ANNEXIN A7; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; LIPIDS; LUNG; MEMBRANE FUSION; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; PULMONARY ALVEOLI; PULMONARY SURFACTANTS; RATS;

EID: 84875254663     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.02.006     Document Type: Article

References (46)

1. Rooney S.A. Regulation of surfactant secretion. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2001, 129:233-243.
2. Chander A., Fisher A.B. Regulation of lung surfactant secretion. Am. J. Physiol. 1990, 258:L241-L253.
3. 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.
4. Dietl P., Haller T. Exocytosis of lung surfactant: from the secretory vesicle to the air-liquid interface. Annu. Rev. Physiol. 2005, 67:595-621.
5. Rothman J.E. Mechanisms of intracellular protein transport. Nature 1994, 372:55-63.
6. 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.
7. Dietl P., Liss B., Felder E., Miklavc P., Wirtz H. Lamellar body exocytosis by cell stretch or purinergic stimulation: possible physiological roles, messengers and mechanisms. Cell. Physiol. Biochem. 2010, 25:1-12.
8. Chamberlain L.H., Burgoyne R.D., Gould G.W. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5619-5624.
9. Chintagari N.R., Jin N., Wang P., Narasaraju T.A., Chen J., Liu L. Effect of cholesterol depletion on exocytosis of alveolar type II cells. Am. J. Respir. Cell Mol. Biol. 2006, 34:677-687.
10. Bickel P.E., Scherer P.E., Schnitzer J.E., Oh P., Lisanti M.P., Lodish H.F. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 1997, 272:13793-13802.
11. Schneider A., Rajendran L., Honsho M., Gralle M., Donnert G., Wouters F., Hell S.W., Simons M. Flotillin-dependent clustering of the amyloid precursor protein regulates its endocytosis and amyloidogenic processing in neurons. J. Neurosci. 2008, 28:2874-2882.
12. Gerst J.E. SNARE regulators: matchmakers and matchbreakers. Biochim. Biophys. Acta 2003, 1641:99-110.
13. 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.
14. Creutz C.E. The annexins and exocytosis. Science (New York, N.Y.) 1992, 258:924-931.
15. Pollard H.B., Guy H.R., Arispe N., de la Fuente M., Lee G., Rojas E.M., Pollard J.R., Srivastava M., Zhang-Keck Z.Y., Merezhinskaya N., et al. Calcium channel and membrane fusion activity of synexin and other members of the Annexin gene family. Biophys. J. 1992, 62:15-18.
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. 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.
18. Chander A., Sen N., Spitzer A.R. Synexin and GTP increase surfactant secretion in permeabilized alveolar type II cells. Am. J. Physiol. 2001, 280:L991-L998.
19. 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.
20. Naidu D.G., Raha A., Chen X.L., Spitzer A.R., Chander A. Partial truncation of the NH2-terminus affects physical characteristics and membrane binding, aggregation, and fusion properties of annexin A7. Biochim. Biophys. Acta 2005, 1734:152-168.
21. 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.
22. 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.
23. Gerelsaikhan T., Vasa P.K., Chander A. Annexin A7 and SNAP23 interactions in alveolar type II cells and in vitro: a role for Ca(2+) and PKC. Biochim. Biophys. Acta 2012, 1823:1796-1806.
24. Oling F., Santos J.S., Govorukhina N., Mazeres-Dubut C., Bergsma-Schutter W., Oostergetel G., Keegstra W., Lambert O., Lewit-Bentley A., Brisson A. Structure of membrane-bound annexin A5 trimers: a hybrid cryo-EM - X-ray crystallography study. J. Mol. Biol. 2000, 304:561-573.
25. Pigault C., Follenius-Wund A., Schmutz M., Freyssinet J.M., Brisson A. Formation of two-dimensional arrays of annexin V on phosphatidylserine-containing liposomes. J. Mol. Biol. 1994, 236:199-208.
26. Reviakine I.I., Bergsma-Schutter W., Brisson A. Growth of protein 2-D crystals on supported planar lipid bilayers imaged in situ by AFM. J. Struct. Biol. 1998, 121:356-361.
27. Voges D., Berendes R., Burger A., Demange P., Baumeister W., Huber R. Three-dimensional structure of membrane-bound annexin V. A correlative electron microscopy-X-ray crystallography study. J. Mol. Biol. 1994, 238:199-213.
28. Gerke V., Creutz C.E., Moss S.E. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6:449-461.
29. 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.
30. Chander A., Naidu D.G., Chen X.L. A ten-residue domain (Y11-A20) in the NH2-terminus modulates membrane association of annexin A7. Biochim. Biophys. Acta 2006, 1761:775-784.
31. Rosengarth A., Gerke V., Luecke H. X-ray structure of full-length annexin 1 and implications for membrane aggregation. J. Mol. Biol. 2001, 306:489-498.
32. Chander A., Sen N. Inhibition of phosphatidylcholine secretion by stilbene disulfonates in alveolar type II cells. Biochem. Pharmacol. 1993, 45:1905-1912.
33. 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.
34. 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.
35. Bers D.M. A simple method for the accurate determination of free [Ca] in Ca-EGTA solutions. Am. J. Physiol. 1982, 242:C404-C408.
36. Chander A., Dodia C.R., Gil J., Fisher A.B. Isolation of lamellar bodies from rat granular pneumocytes in primary culture. Biochim. Biophys. Acta 1983, 753:119-129.
37. Chander A. Dicyclohexylcarbodiimide and vanadate sensitive ATPase of lung lamellar bodies. Biochim. Biophys. Acta 1992, 1123:198-206.
38. Chander A., Fisher A.B., Strauss J.F. Role of an acidic compartment in synthesis of disaturated phosphatidylcholine by rat granular pneumocytes. Biochem. J. 1982, 208:651-658.
39. 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.
40. Gerke V., Moss S.E. Annexins: from structure to function. Physiol. Rev. 2002, 82:331-371.
41. Liemann S., Bringemeier I., Benz J., Gottig P., Hofmann A., Huber R., Noegel A.A., Jacob U. Crystal structure of the C-terminal tetrad repeat from synexin (annexin VII) of Dictyostelium discoideum. J. Mol. Biol. 1997, 270:79-88.
42. Huber R., Romisch J., Paques E.P. The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes. EMBO J. 1990, 9:3867-3874.
43. Chapman E.R., Davis A.F. Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. J. Biol. Chem. 1998, 273:13995-14001.
44. Pollard H.B., Burns A.L., Rojas E. A molecular basis for synexin-driven, calcium-dependent membrane fusion. J. Exp. Biol. 1988, 139:267-286.
45. Burns A.L., Magendzo K., Shirvan A., Srivastava M., Rojas E., Alijani M.R., Pollard H.B. Calcium channel activity of purified human synexin and structure of the human synexin gene. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:3798-3802.
46. 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.