The tomato defensin TPP3 binds phosphatidylinositol (4,5)-bisphosphate via a conserved dimeric cationic grip conformation to mediate cell lysis

Molecular and Cellular Biology

Volumn 35, Issue 11, 2015, Pages 1964-1978

  Baxter, Amy A ^a   Richter, Viviane ^a   Lay, Fung T ^a   Poon, Ivan K H ^a   Adda, Christopher G ^a   Veneer, Prem K ^a   Phan, Thanh Kha ^a   Bleackley, Mark R ^a   Anderson, Marilyn A ^a   Kvansakul, Marc ^a   Hulett, Mark D ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEFENSIN; DEFENSIN TPP3; PHOSPHATIDYLINOSITOL PHOSPHOLIPID; POLYPHOSPHOINOSITIDE; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; PHOSPHATIDYLINOSITOL; PLANT PROTEIN;

ARTICLE; CONFOCAL LASER MICROSCOPY; CYTOLYSIS; ENZYME RELEASE; FEMALE; FLOW CYTOMETRY; FUNGUS GROWTH; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE PERMEABILITY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; TRANSMISSION ELECTRON MICROSCOPY; X RAY CRYSTALLOGRAPHY; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL WALL; CONFORMATION; METABOLISM; PHYSIOLOGY; TOMATO; TUMOR CELL LINE; U937 CELL LINE;

LYCOPERSICON ESCULENTUM; MAMMALIA; NICOTIANA ALATA;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE, TUMOR; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL WALL; DEFENSINS; HELA CELLS; HUMANS; LYCOPERSICON ESCULENTUM; MOLECULAR CONFORMATION; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS; PLANT PROTEINS; U937 CELLS;

EID: 84929441376     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00282-15     Document Type: Article

References (48)

1. Broekaert WF, Terras FR, Cammue BP, Osborn RW. 1995. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 108:1353-1358. http://dx.doi.org/10.1104/pp.108.4.1353.
2. Lay F, Anderson M. 2005. Defensins-components of the innate immune system in plants. Curr Protein Pept Sci 6:85-101. http://dx.doi.org/10.2174/1389203053027575.
3. Van der Weerden NL, Anderson MA. 2013. Plant defensins: common fold, multiple functions. Fungal Biol Rev 26:121-131. http://dx.doi.org/10.1016/j.fbr.2012.08.004.
4. Kushmerick C, de Souza Castro M, Santos Cruz J, Bloch C, Jr, Beirao PS. 1998. Functional and structural features of gamma-zeathionins, a new class of sodium channel blockers. FEBS Lett 440:302-306. http://dx.doi.org/10.1016/S0014-5793(98)01480-X.
5. Pelegrini PB, Lay FT, Murad AM, Anderson MA, Franco OL. 2008. Novel insights on the mechanism of action of alpha-amylase inhibitors from the plant defensin family. Proteins 73:719-729. http://dx.doi.org/10.1002/prot.22086.
6. Lay FT, Brugliera F, Anderson MA. 2003. Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol 131: 1283-1293. http://dx.doi.org/10.1104/pp.102.016626.
7. Lay FT, Poon S, McKenna JA, Connelly AA, Barbeta BL, McGinness BS, Fox JL, Daly NL, Craik DJ, Heath RL. 2014. The C-terminal propeptide of a plant defensin confers cytoprotective and subcellular targeting functions. BMC Plant Biol 14:41. http://dx.doi.org/10.1186/1471-2229-14-41.
8. Thevissen K, de Mello Tavares P, Xu D, Blankenship J, Vandenbosch D, Idkowiak-Baldys J, Govaert G, Bink A, Rozental S, De Groot PW. 2012. The plant defensin RsAFP2 induces cell wall stress, septin mislocalization and accumulation of ceramides in Candida albicans. Mol Microbiol 84:166-180. http://dx.doi.org/10.1111/j.1365-2958.2012.08017.x.
9. Ramamoorthy V, Cahoon EB, Li J, Thokala M, Minto RE, Shah DM. 2007. Glucosylceramide synthase is essential for alfalfa defensin-mediated growth inhibition but not for pathogenicity of Fusarium graminearum. Mol Microbiol 66:771-786. http://dx.doi.org/10.1111/j.1365-2958.2007.05955.x.
10. Aerts AM, François IE, Bammens L, Cammue B, Smets B, Winderickx J, Accardo S, De Vos DE, Thevissen K. 2006. Level of M(IP)2C sphingolipid affects plant defensin sensitivity, oxidative stress resistance and chronological life-span in yeast. FEBS Lett 580:1903-1907. http://dx.doi.org/10.1016/j.febslet.2006.02.061.
11. Sagaram US, El-Mounadi K, Buchko GW, Berg HR, Kaur J, Pandurangi RS, Smith TJ, Shah DM. 2013. Structural and functional studies of a phosphatidic acid-binding antifungal plant defensin MtDef4: identification of an RGFRRR motif governing fungal cell entry. PLoS One 8:e82485. http://dx.doi.org/10.1371/journal.pone.0082485.
12. Hayes BM, Bleackley MR, Wiltshire JL, Anderson MA, Traven A, van der Weerden NL. 2013. Identification and mechanism of action of the plant defensin NaD1 as a new member of the antifungal drug arsenal against Candida albicans. Antimicrob Agents Chemother 57:3667-3675. http://dx.doi.org/10.1128/AAC.00365-13.
13. van der Weerden NL, Lay FT, Anderson MA. 2008. The plant defensin, NaD1, enters the cytoplasm of Fusarium oxysporum hyphae. J Biol Chem 283:14445-14452. http://dx.doi.org/10.1074/jbc.M709867200.
14. van der Weerden NL, Hancock RE, Anderson MA. 2010. Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall-dependent process. J Biol Chem 285:37513-37520. http://dx.doi.org/10.1074/jbc.M110.134882.
15. Lay FT, Mills GD, Poon IK, Cowieson NP, Kirby N, Baxter AA, van der Weerden NL, Dogovski C, Perugini MA, Anderson MA, Kvansakul M, Hulett MD. 2012. Dimerization of plant defensin NaD1 enhances its antifungal activity. J Biol Chem 287:19961-19972. http://dx.doi.org/10.1074/jbc.M111.331009.
16. Hayes BM, Anderson MA, Traven A, van der Weerden NL, Bleackley MR. 2014. Activation of stress signalling pathways enhances tolerance of fungi to chemical fungicides and antifungal proteins. Cell Mol Life Sci 71:2651-2666. http://dx.doi.org/10.1007/s00018-014-1573-8.
17. Song X, Zhang M, Zhou Z, Gong W. 2011. Ultra-high resolution crystal structure of a dimeric defensin SPE10. FEBS Lett 585:300-306. http://dx.doi.org/10.1016/j.febslet.2010.12.039.
18. Poon IK, Baxter AA, Lay FT, Mills GD, Adda CG, Payne JA, Phan TK, Ryan GF, White JA, Veneer PK, van der Weerden NL, Anderson MA, Kvansakul M, Hulett MD. 2014. Phosphoinositide-mediated oligomerization of a defensin induces cell lysis. eLife 3:e01808. http://dx.doi.org/10.7554/eLife.01808.
19. Milligan SB, Gasser CS. 1995. Nature and regulation of pistil-expressed genes in tomato. Plant Mol Biol 28:691-711. http://dx.doi.org/10.1007/BF00021194.
20. Lay FT, Schirra HJ, Scanlon MJ, Anderson MA, Craik DJ. 2003. The three-dimensional solution structure of NaD1, a new floral defensin from Nicotiana alata and its application to a homology model of the crop defense protein alfAFP. J Mol Biol 325:175-188. http://dx.doi.org/10.1016/S0022-2836(02)01103-8.
21. Lay FT, Veneer PK, Hulett MD, Kvansakul M. 2012. Recombinant expression and purification of the tomato defensin TPP3 and its preliminary X-ray crystallographic analysis. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:314-316. http://dx.doi.org/10.1107/S1744309112001510.
22. van Dijk A, Veldhuizen EJ, Haagsman HP. 2008. Avian defensins. Vet Immunol Immunopathol 124:1-18. http://dx.doi.org/10.1016/j.vetimm.2007.12.006.
23. Poon IK, Hulett MD, Parish CR. 2010. Histidine-rich glycoprotein is a novel plasma pattern recognition molecule that recruits IgG to facilitate necrotic cell clearance via FcgammaRI on phagocytes. Blood 115:2473-2482. http://dx.doi.org/10.1182/blood-2009-07-234013.
24. Storoni LC, McCoy AJ, Read RJ. 2004. Likelihood-enhanced fast rotation functions. Acta Crystallogr Sect D Biol Crystallogr 60:432-438. http://dx.doi.org/10.1107/S0907444903028956.
25. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr SectDBiol Crystallogr 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158.
26. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Biol Crystallogr 66:213-221. http://dx.doi.org/10.1107/S0907444909052925.
27. Holm L, Rosenstrom P. 2010. Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545-W549. http://dx.doi.org/10.1093/nar/gkq366.
28. Schibli DJ, Hunter HN, Aseyev V, Starner TD, Wiencek JM, McCray PB, Tack BF, Vogel HJ. 2002. The solution structures of the human β-defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus. J Biol Chem 277:8279-8289. http://dx.doi.org/10.1074/jbc.M108830200.
29. Wommack AJ, Robson SA, Wanniarachchi YA, Wan A, Turner CJ, Wagner G, Nolan EM. 2012. NMR solution structure and conditiondependent oligomerization of the antimicrobial peptide human defensin 5. Biochemistry 51:9624-9637. http://dx.doi.org/10.1021/bi301255u.
30. Garcia P, Gupta R, Shah S, Morris AJ, Rudge SA, Scarlata S, Petrova V, McLaughlin S, Rebecchi MJ. 1995. The pleckstrin homology domain of phospholipase C-delta 1 binds with high affinity to phosphatidylinositol 4,5-bisphosphate in bilayer membranes. Biochemistry 34:16228-16234. http://dx.doi.org/10.1021/bi00049a039.
31. Arbuzova A, Martushova K, Hangyás-Mihályné G, Morris AJ, Ozaki S, Prestwich GD, McLaughlin S. 2000. Fluorescently labeled neomycin as a probe of phosphatidylinositol-4,5-bisphosphate in membranes. Biochim Biophys Acta 1464:35-48. http://dx.doi.org/10.1016/S0005-2736(99)00243-6.
32. Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P. 2000. GAP43, MARCKS, and CAP23 modulate PI (4, 5) P2 at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149:1455-1472. http://dx.doi.org/10.1083/jcb.149.7.1455.
33. Vandamme D, Landuyt B, Luyten W, Schoofs L. 2012. A comprehensive summary of LL-37, the factotum human cathelicidin peptide. Cell Immunol 280:22-35. http://dx.doi.org/10.1016/j.cellimm.2012.11.009.
34. Hoover DM, Rajashankar KR, Blumenthal R, Puri A, Oppenheim JJ, Chertov O, Lubkowski J. 2000. The structure of human β-defensin-2 shows evidence of higher order oligomerization. J Biol Chem 275:32911-32918. http://dx.doi.org/10.1074/jbc.M006098200.
35. Dhople V, Krukemeyer A, Ramamoorthy A. 2006. The human betadefensin-3, an antibacterial peptide with multiple biological functions. Biochim Biophys Acta 1758:1499-1512. http://dx.doi.org/10.1016/j.bbamem.2006.07.007.
36. Mani R, Cady SD, Tang M, Waring AJ, Lehrer RI, Hong M. 2006. Membrane-dependent oligomeric structure and pore formation of a β-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR. Proc Natl Acad Sci U S A 103:16242-16247. http://dx.doi.org/10.1073/pnas.0605079103.
37. Szyk A, Wu Z, Tucker K, Yang D, Lu W, Lubkowski J. 2006. Crystal structures of human α-defensins HNP4, HD5, and HD6. Protein Sci 15: 2749-2760. http://dx.doi.org/10.1110/ps.062336606.
38. Chu H, Pazgier M, Jung G, Nuccio S-P, Castillo PA, de Jong MF, Winter MG, Winter SE, Wehkamp J, Shen B. 2012. Human α-defensin 6 promotes mucosal innate immunity through self-assembled peptide nanonets. Science 337:477-481. http://dx.doi.org/10.1126/science.1218831.
39. Garvey M, Meehan S, Gras SL, Schirra HJ, Craik DJ, Van der Weerden NL, Anderson MA, Gerrard JA, Carver JA. 2013. A radish seed antifungal peptide with a high amyloid fibril-forming propensity. Biochim Biophys Acta 1834:1615-1623. http://dx.doi.org/10.1016/j.bbapap.2013.04.030.
40. Schneider T, Kruse T, Wimmer R, Wiedemann I, Sass V, Pag U, Jansen A, Nielsen AK, Mygind PH, Raventós DS. 2010. Plectasin, a fungal defensin, targets the bacterial cell wall precursor Lipid II. Science 328: 1168-1172. http://dx.doi.org/10.1126/science.1185723.
41. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284-295. http://dx.doi.org/10.1016/j.cell.2010.06.008.
42. Dove SK, Cooke FT, Douglas MR, Sayers LG, Parker PJ, Michell RH. 1997. Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187-192. http://dx.doi.org/10.1038/36613.
43. Okumura K, Itoh A, Isogai E, Hirose K, Hosokawa Y, Abiko Y, Shibata T, Hirata M, Isogai H. 2004. C-terminal domain of human CAP18 antimicrobial peptide induces apoptosis in oral squamous cell carcinoma SAS-H1 cells. Cancer Lett 212:185-194. http://dx.doi.org/10.1016/j.canlet.2004.04.006.
44. Ghavami S, Asoodeh A, Klonisch T, Halayko AJ, Kadkhoda K, Kroczak TJ, Gibson SB, Booy EP, Naderi-Manesh H, Los M. 2008. Brevinin-2R1 semi-selectively kills cancer cells by a distinct mechanism, which involves the lysosomal-mitochondrial death pathway. J Cell Mol Med 12:1005-1022. http://dx.doi.org/10.1111/j.1582-4934.2008.00129.x.
45. Broberg CA, Zhang L, Gonzalez H, Laskowski-Arce MA, Orth K. 2010. A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity. Science 329:1660-1662. http://dx.doi.org/10.1126/science.1192850.
46. Niebuhr K, Giuriato S, Pedron T, Philpott DJ, Gaits F, Sable J, Sheetz MP, Parsot C, Sansonetti PJ, Payrastre B. 2002. Conversion of PtdIns(4, 5)P2 into PtdIns(5)P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J 21:5069-5078. http://dx.doi.org/10.1093/emboj/cdf522.
47. García-Sáez AJ, Buschhorn SB, Keller H, Anderluh G, Simons K, Schwille P. 2011. Oligomerization and pore formation by equinatoxin II inhibit endocytosis and lead to plasma membrane reorganization. J Biol Chem 286:37768-37777. http://dx.doi.org/10.1074/jbc.M111.281592.
48. Krissinel E, Henrick K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr Sect D Biol Crystallogr 60:2256-2268. http://dx.doi.org/10.1107/S0907444904026460.