Phospholipase A activity of adenylate cyclase toxin mediates translocation of its adenylate cyclase domain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 33, 2017, Pages E6784-E6793

  González Bullón, David ^a   Uribe, Kepa B ^a   Martín, César ^a   Ostolaza, Helena ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Bacterial toxins; Biological membranes; Membrane remodeling; Protein translocation; RTX toxin family

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE TOXIN; FATTY ACID AMIDASE; LIPOSOME; LYSOPHOSPHOLIPASE; LYSOPHOSPHOLIPID; MUTANT PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A; CYCLIC AMP; MEMBRANE LIPID;

ARTICLE; BACTERIAL INFECTION; BIOCHEMISTRY; BIOPHYSICS; CELL MEMBRANE; CONCENTRATION PROCESS; CYTOTOXICITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; HOST CELL; MACROPHAGE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; AMINO ACID SEQUENCE; ANIMAL; BORDETELLA PERTUSSIS; CELL LINE; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MOUSE; PERTUSSIS; PHYSIOLOGY; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY;

ADENYLATE CYCLASE TOXIN; AMINO ACID SEQUENCE; ANIMALS; BORDETELLA PERTUSSIS; CATALYTIC DOMAIN; CELL LINE; CELL MEMBRANE; CYCLIC AMP; HUMANS; MACROPHAGES; MEMBRANE LIPIDS; MICE; PHOSPHOLIPASES A; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID; WHOOPING COUGH;

EID: 85027395413     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1701783114     Document Type: Article

References (63)

1. Carbonetti NH (2010) Pertussis toxin and adenylate cyclase toxin: Key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol 5:455–469.
2. Mattoo S, Cherry JD (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18:326–382.
3. Goodwin MSM, Weiss AA (1990) Adenylate cyclase toxin is critical for colonization and pertussis toxin is critical for lethal infection by Bordetella pertussis in infant mice. Infect Immun 58:3445–3447.
4. Guermonprez P, et al. (2001) The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J Exp Med 193:1035–1044.
5. Berkowitz SA, Goldhammer AR, Hewlett EL, Wolff J (1980) Activation of prokaryotic adenylate cyclase by calmodulin. Ann N Y Acad Sci 356:360.
6. Confer DL, Eaton JW (1982) Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 217:948–950.
7. Weingart CL, Weiss AA (2000) Bordetella pertussis virulence factors affect phagocytosis by human neutrophils. Infect Immun 68:1735–1739.
8. Ehrmann IE, Gray MC, Gordon VM, Gray LS, Hewlett EL (1991) Hemolytic activity of adenylate cyclase toxin from Bordetella pertussis. FEBS Lett 278:79–83.
9. Hewlett EL, Donato GM, Gray MC (2006) Macrophage cytotoxicity produced by adenylate cyclase toxin from Bordetella pertussis: More than just making cyclic AMP! Mol Microbiol 59:447–459.
10. Benz R, Maier E, Ladant D, Ullmann A, Sebo P (1994) Adenylate cyclase toxin (CyaA) of Bordetella pertussis. Evidence for the formation of small ion-permeable channels and comparison with HlyA of Escherichia coli. J Biol Chem 269:27231–27239.
11. Dal Molin F, et al. (2006) Cell entry and cAMP imaging of anthrax edema toxin. EMBO J 25:5405–5413.
12. Ladant D, Ullmann A (1999) Bordatella pertussis adenylate cyclase: A toxin with multiple talents. Trends Microbiol 7:172–176.
13. Glaser P, Sakamoto H, Bellalou J, Ullmann A, Danchin A (1988) Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J 7:3997–4004.
14. Bellalou J, Sakamoto H, Ladant D, Geoffroy C, Ullmann A (1990) Deletions affecting hemolytic and toxin activities of Bordetella pertussis adenylate cyclase. Infect Immun 58:3242–3247.
15. Sakamoto H, Bellalou J, Sebo P, Ladant D (1992) Bordetella pertussis adenylate cyclase toxin. Structural and functional independence of the catalytic and hemolytic activities. J Biol Chem 267:13598–13602.
16. Hackett M, Guo L, Shabanowitz J, Hunt DF, Hewlett EL (1994) Internal lysine palmitoylation in adenylate cyclase toxin from Bordetella pertussis. Science 266:433–435.
17. Bauche C, et al. (2006) Structural and functional characterization of an essential RTX subdomain of Bordetella pertussis adenylate cyclase toxin. J Biol Chem 281: 16914–16926.
18. Rose T, Sebo P, Bellalou J, Ladant D (1995) Interaction of calcium with Bordetella pertussis adenylate cyclase toxin. Characterization of multiple calcium-binding sites and calcium-induced conformational changes. J Biol Chem 270:26370–26376.
19. El-Azami-El-Idrissi M, et al. (2003) Interaction of Bordetella pertussis adenylate cyclase with CD11b/CD18: Role of toxin acylation and identification of the main integrin interaction domain. J Biol Chem 278:38514–38521.
20. Rogel A, Hanski E (1992) Distinct steps in the penetration of adenylate cyclase toxin of Bordetella pertussis into sheep erythrocytes. Translocation of the toxin across the membrane. J Biol Chem 267:22599–22605.
21. Basler M, et al. (2007) Segments crucial for membrane translocation and pore-forming activity of Bordetella adenylate cyclase toxin. J Biol Chem 282:12419–12429.
22. Gordon VM, et al. (1989) Adenylate cyclase toxins from Bacillus anthracis and Bordetella pertussis. Different processes for interaction with and entry into target cells. J Biol Chem 264:14792–14796.
23. Gmira S, Karimova G, Ladant D (2001) Characterization of recombinant Bordetella pertussis adenylate cyclase toxins carrying passenger proteins. Res Microbiol 152: 889–900.
24. Osicková A, Osicka R, Maier E, Benz R, Sebo P (1999) An amphipathic alpha-helix including glutamates 509 and 516 is crucial for membrane translocation of adenylate cyclase toxin and modulates formation and cation selectivity of its membrane channels. J Biol Chem 274:37644–37650.
25. Osickova A, et al. (2010) Adenylate cyclase toxin translocates across target cell membrane without forming a pore. Mol Microbiol 75:1550–1562.
26. Holubova J, et al. (2012) Delivery of large heterologous polypeptides across the cytoplasmic membrane of antigen-presenting cells by the Bordetella RTX hemolysin moiety lacking the adenylyl cyclase domain. Infect Immun 80:1181–1192.
27. Karst JC, et al. (2012) Identification of a region that assists membrane insertion and translocation of the catalytic domain of Bordetella pertussis CyaA toxin. J Biol Chem 287:9200–9212.
28. Subrini O, et al. (2013) Characterization of a membrane-active peptide from the Bordetella pertussis CyaA toxin. J Biol Chem 288:32585–32598.
29. Bumba L, Masin J, Fiser R, Sebo P (2010) Bordetella adenylate cyclase toxin mobilizes its beta2 integrin receptor into lipid rafts to accomplish translocation across target cell membrane in two steps. PLoS Pathog 6:e1000901.
30. Rogel A, et al. (1989) Bordetella pertussis adenylate cyclase: Purification and characterization of the toxic form of the enzyme. EMBO J 8:2755–2760.
31. Eby JC, Gray MC, Mangan AR, Donato GM, Hewlett EL (2012) Role of CD11b/CD18 in the process of intoxication by the adenylate cyclase toxin of Bordetella pertussis. Infect Immun 80:850–859.
32. Martín C, et al. (2004) Membrane restructuring by Bordetella pertussis adenylate cyclase toxin, a member of the RTX toxin family. J Bacteriol 186:3760–3765.
33. Contreras FX, Sánchez-Magraner L, Alonso A, Goñi FM (2010) Transbilayer (flip-flop) lipid motion and lipid scrambling in membranes. FEBS Lett 584:1779–1786.
34. Gaspar AH, Machner MP (2014) VipD is a Rab5-activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion. Proc Natl Acad Sci USA 111: 4560–4565.
35. Tamura M, et al. (2004) Lysophospholipase A activity of Pseudomonas aeruginosa type III secretory toxin ExoU. Biochem Biophys Res Commun 316:323–331.
36. Hirschberg HJHB, Simons JW, Dekker N, Egmond MR (2001) Cloning, expression, purification and characterization of patatin, a novel phospholipase A. Eur J Biochem 268:5037–5044.
37. Rydel TJ, et al. (2003) The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad. Biochemistry 42: 6696–6708.
38. Wang A, Yang HC, Friedman P, Johnson CA, Dennis EA (1999) A specific human lysophospholipase: cDNA cloning, tissue distribution and kinetic characterization. Biochim Biophys Acta 1437:157–169.
39. Lio YC, Reynolds LJ, Balsinde J, Dennis EA (1996) Irreversible inhibition of Ca(2+)independent phospholipase A2 by methylarachidonylfluorophosphate. Biochim Biophys Acta 1302:55–60.
40. Dole VP, Meinertz H (1960) Microdetermination of long-chain fatty acids in plasma and tissues. J Biol Chem 235:2595–2599.
41. Schaloske RH, Dennis EA (2006) The phospholipase A2 superfamily and its group numbering system. Biochim Biophys Acta 1761:1246–1259.
42. Martín C, Gómez-Bilbao G, Ostolaza H (2010) Bordetella adenylate cyclase toxin promotes calcium entry into both CD11b+ and CD11b- cells through cAMP-dependent L-type-like calcium channels. J Biol Chem 285:357–364.
43. Yoo J, Cui Q (2009) Curvature generation and pressure profile modulation in membrane by lysolipids: Insights from coarse-grained simulations. Biophys J 97:2267–2276.
44. Basañez G, et al. (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 277: 49360–49365.
45. Gilbert RJC (2016) Protein-lipid interactions and non-lamellar lipidic structures in membrane pore formation and membrane fusion. Biochim Biophys Acta 1858: 487–499.
46. Allende D, Simon SA, McIntosh TJ (2005) Melittin-induced bilayer leakage depends on lipid material properties: Evidence for toroidal pores. Biophys J 88:1828–1837.
47. Karatekin E, et al. (2003) Cascades of transient pores in giant vesicles: Line tension and transport. Biophys J 84:1734–1749.
48. Eby JC, et al. (2013) Quantification of the adenylate cyclase toxin of Bordetella pertussis in vitro and during respiratory infection. Infect Immun 81:1390–1398.
49. Strickland JA, Orr GL, Walsh TA (1995) Inhibition of diabrotica larval growth by patatin, the lipid acyl hydrolase from potato tubers. Plant Physiol 109:667–674.
50. Agarwal S, et al. (2015) Autophagy and endosomal trafficking inhibition by Vibrio cholerae MARTX toxin phosphatidylinositol-3-phosphate-specific phospholipase A1 activity. Nat Commun 6:8745;
51. erratum in Agarwal S, et al. Autophagy and endosomal trafficking inhibition by Vibrio cholerae MARTX toxin phosphatidylinositol-3-phosphate-specific phospholipase A1 activity. Nat Commun (2015) 6:10135.
52. Henriksen J, et al. (2006) Universal behavior of membranes with sterols. Biophys J 90: 1639–1649.
53. Bagatolli LA, Gratton E (2000) A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: A two-photon fluorescence microscopy study. Biophys J 79:434–447.
54. Leidy C, Wolkers WF, Jørgensen K, Mouritsen OG, Crowe JH (2001) Lateral organization and domain formation in a two-component lipid membrane system. Biophys J 80:1819–1828.
55. van den Brink-van der Laan E, Killian JA, de Kruijff B (2004) Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim Biophys Acta 1666:275–288.
56. Epand RF, Martinou JC, Fornallaz-Mulhauser M, Hughes DW, Epand RM (2002) The apoptotic protein tBid promotes leakage by altering membrane curvature. J Biol Chem 277:32632–32639.
57. Epand RM (1996) Functional roles of non-lamellar forming lipids. Chem Phys Lipids 81: 101–104.
58. Terrones O, et al. (2004) Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J Biol Chem 279:30081–30091.
59. Karimova G, Pidoux J, Ullmann A, Ladant D (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752–5756.
60. Bychkova VE, Pain RH, Ptitsyn OB (1988) The ‘molten globule’ state is involved in the translocation of proteins across membranes? FEBS Lett 238:231–234.
61. Ptitsyn OB, Pain RH, Semisotnov GV, Zerovnik E, Razgulyaev OI (1990) Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett 262: 20–24.
62. Karst JC, et al. (2014) Calcium, acylation, and molecular confinement favor folding of Bordetella pertussis adenylate cyclase CyaA toxin into a monomeric and cytotoxic form. J Biol Chem 289:30702–30716.
63. Gray M, Szabo G, Otero AS, Gray L, Hewlett E (1998) Distinct mechanisms for K+ efflux, intoxication, and hemolysis by Bordetella pertussis AC toxin. J Biol Chem 273: 18260–18267.