全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...

Bacillus thuringiensis Crystal Protein Cry6Aa Triggers Caenorhabditis elegans Necrosis Pathway Mediated by Aspartic Protease (ASP-1)

DOI: 10.1371/journal.ppat.1005389

Full-Text   Cite this paper   Add to My Lib

Abstract:

Cell death plays an important role in host-pathogen interactions. Crystal proteins (toxins) are essential components of Bacillus thuringiensis (Bt) biological pesticides because of their specific toxicity against insects and nematodes. However, the mode of action by which crystal toxins to induce cell death is not completely understood. Here we show that crystal toxin triggers cell death by necrosis signaling pathway using crystal toxin Cry6Aa-Caenorhabditis elegans toxin-host interaction system, which involves an increase in concentrations of cytoplasmic calcium, lysosomal lyses, uptake of propidium iodide, and burst of death fluorescence. We find that a deficiency in the necrosis pathway confers tolerance to Cry6Aa toxin. Intriguingly, the necrosis pathway is specifically triggered by Cry6Aa, not by Cry5Ba, whose amino acid sequence is different from that of Cry6Aa. Furthermore, Cry6Aa-induced necrosis pathway requires aspartic protease (ASP-1). In addition, ASP-1 protects Cry6Aa from over-degradation in C. elegans. This is the first demonstration that deficiency in necrosis pathway confers tolerance to Bt crystal protein, and that Cry6A triggers necrosis represents a newly added necrosis paradigm in the C. elegans. Understanding this model could lead to new strategies for nematode control.

References

[1]  Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N (2013) Crosstalk between apoptosis, necrosis and autophagy. Biochim Biophys Acta 1833: 3448–3459. doi: 10.1016/j.bbamcr.2013.06.001. pmid:23770045
[2]  Sridharan H, Upton JW (2014) Programmed necrosis in microbial pathogenesis. Trends Microbiol 22: 199–207. doi: 10.1016/j.tim.2014.01.005. pmid:24565922
[3]  Mohammad RM, Muqbil I, Lowe L, Yedjou C, Hsu HY, et al. (2015) Broad targeting of resistance to apoptosis in cancer. Semin Cancer Biol 35: S78–S103. doi: 10.1016/j.semcancer.2015.03.001. pmid:25936818
[4]  Chan FK, Luz NF, Moriwaki K (2015) Programmed necrosis in the cross talk of cell death and inflammation. Annu Rev Immunol 33: 79–106. doi: 10.1146/annurev-immunol-032414-112248. pmid:25493335
[5]  Troulinaki K, Tavernarakis N (2012) Necrotic cell death and neurodegeneration: The involvement of endocytosis and intracellular trafficking. Worm 1: 176–181. doi: 10.4161/worm.20457. pmid:24058844
[6]  Silke J, Rickard JA, Gerlic M (2015) The diverse role of RIP kinases in necroptosis and inflammation. Nat Immunol 16: 689–697. doi: 10.1038/ni.3206. pmid:26086143
[7]  Martin JB (1999) Molecular basis of the neurodegenerative disorders. N Engl J Med 340: 1970–1980. pmid:10379022 doi: 10.1056/nejm199906243402507
[8]  Mocarski ES, Kaiser WJ, Livingston-Rosanoff D, Upton JW, Daley-Bauer LP (2014) True grit: programmed necrosis in antiviral host defense, inflammation, and immunogenicity. J Immunol 192: 2019–2026. doi: 10.4049/jimmunol.1302426. pmid:24563506
[9]  Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, et al. (2000) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis—one species on the basis of genetic evidence. Appl Environ Microbiol 66: 2627–2630. pmid:10831447 doi: 10.1128/aem.66.6.2627-2630.2000
[10]  Pardo-Lopez L, Soberon M, Bravo A (2013) Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37: 3–22. doi: 10.1111/j.1574-6976.2012.00341.x. pmid:22540421
[11]  Vachon V, Laprade R, Schwartz JL (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol 111: 1–12. doi: 10.1016/j.jip.2012.05.001. pmid:22617276
[12]  Adang MJ, Crickmore N, Jurat-Fuentes JL (2014) Diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Adv In Insect Phys 47: 39–87. doi: 10.1016/b978-0-12-800197-4.00002-6
[13]  Melo AL, Soccol VT, Soccol CR (2015) Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Crit Rev Biotechnol: 1–10. doi: 10.3109/07388551.2014.960793
[14]  Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr. (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci U S A 103: 9897–9902. pmid:16788061 doi: 10.1073/pnas.0604017103
[15]  Zhang X, Candas M, Griko NB, Rose-Young L, Bulla LA Jr. (2005) Cytotoxicity of Bacillus thuringiensis Cry1Ab toxin depends on specific binding of the toxin to the cadherin receptor BT-R1 expressed in insect cells. Cell Death Differ 12: 1407–1416. pmid:15920532 doi: 10.1038/sj.cdd.4401675
[16]  Cappello M, Bungiro RD, Harrison LM, Bischof LJ, Griffitts JS, et al. (2006) A purified Bacillus thuringiensis crystal protein with therapeutic activity against the hookworm parasite Ancylostoma ceylanicum. Proc Natl Acad Sci U S A 103: 15154–15159. pmid:17005719 doi: 10.1073/pnas.0607002103
[17]  Zhang F, Peng D, Ye X, Yu Z, Hu Z, et al. (2012) In vitro uptake of 140 kDa Bacillus thuringiensis nematicidal crystal proteins by the second stage juvenile of Meloidogyne hapla. PLoS One 7: e38534. doi: 10.1371/journal.pone.0038534. pmid:22737212
[18]  Li XQ, Wei JZ, Tan A, Aroian RV (2007) Resistance to root-knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant Biotechnol J 5: 455–464. pmid:17451491 doi: 10.1111/j.1467-7652.2007.00257.x
[19]  Li XQ, Tan A, Voegtline M, Bekele S, Chen CS, et al. (2008) Expression of Cry5B protein from Bacillus thuringiensis in plant roots confers resistance to root-knot nematode. Biol Control 47: 97–102. doi: 10.1016/j.biocontrol.2008.06.007
[20]  Hui F, Scheib U, Hu Y, Sommer RJ, Aroian RV, et al. (2012) Structure and glycolipid binding properties of the nematicidal protein Cry5B. Biochemistry 51: 9911–9921. doi: 10.1021/bi301386q. pmid:23150986
[21]  Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B, et al. (2005) Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 307: 922–925. pmid:15705852 doi: 10.1126/science.1104444
[22]  Marroquin LD, Elyassnia D, Griffitts JS, Feitelson JS, Aroian RV (2000) Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics 155: 1693–1699. pmid:10924467
[23]  Scott BA, Avidan MS, Crowder CM (2002) Regulation of hypoxic death in C. elegans by the insulin/IGF receptor homolog DAF-2. Science 296: 2388–2391. pmid:12065745 doi: 10.1126/science.1072302
[24]  Nikoletopoulou V, Tavernarakis N (2014) Necrotic cell death in Caenorhabditis elegans. Methods Enzymol 545: 127–155. doi: 10.1016/B978-0-12-801430-1.00006-8. pmid:25065889
[25]  Krishnamoorthy M, Jurat-Fuentes JL, McNall RJ, Andacht T, Adang MJ (2007) Identification of novel Cry1Ac binding proteins in midgut membranes from Heliothis virescens using proteomic analyses. Insect Biochem Mol Biol 37: 189–201. pmid:17296494 doi: 10.1016/j.ibmb.2006.10.004
[26]  Fernandez-Luna MT, Lanz-Mendoza H, Gill SS, Bravo A, Soberon M, et al. (2010) An alpha-amylase is a novel receptor for Bacillus thuringiensis ssp. israelensis Cry4Ba and Cry11Aa toxins in the malaria vector mosquito Anopheles albimanus (Diptera: Culicidae). Environ Microbiol 12: 746–757. doi: 10.1111/j.1462-2920.2009.02117.x. pmid:20002140
[27]  Candas M, Loseva O, Oppert B, Kosaraju P, Bulla LA Jr. (2003) Insect resistance to Bacillus thuringiensis: alterations in the indianmeal moth larval gut proteome. Mol Cell Proteomics 2: 19–28. pmid:12601079 doi: 10.1074/mcp.m200069-mcp200
[28]  Tcherepanova I, Bhattacharyya L, Rubin CS, Freedman JH (2000) Aspartic proteases from the nematode Caenorhabditis elegans. Structural organization and developmental and cell-specific expression of asp-1. J Biol Chem 275: 26359–26369. pmid:10854422 doi: 10.1074/jbc.m000956200
[29]  Wei JZ, Hale K, Carta L, Platzer E, Wong C, et al. (2003) Bacillus thuringiensis crystal proteins that target nematodes. Proc Natl Acad Sci U S A 100: 2760–2765. pmid:12598644 doi: 10.1073/pnas.0538072100
[30]  Talaei-Hassanloui R, Bakhshaei R, Hosseininaveh V, Khorramnezhad A (2013) Effect of midgut proteolytic activity on susceptibility of lepidopteran larvae to Bacillus thuringiensis subsp. Kurstaki. Front Physiol 4: 406. doi: 10.3389/fphys.2013.00406. pmid:24474937
[31]  Allison K T, Tracy L M, Tori D G, Kimberly M (2013) Use of Necrotic Markers in the Drosophila Ovary. Methods Mol Biol 1004: 215–228. doi: 10.1007/978-1-62703-383-1_16. pmid:23733580
[32]  Smith TK, Lund EK, Parker ML, Clarke RG, Johnson IT (2004) Allyl-isothiocyanate causes mitotic block, loss of cell adhesion and disrupted cytoskeletal structure in HT29 cells. Carcinogenesis 25: 1409–1415. pmid:15033907 doi: 10.1093/carcin/bgh149
[33]  Unal Cevik I, Dalkara T (2003) Intravenously administered propidium iodide labels necrotic cells in the intact mouse brain after injury. Cell Death Differ 10: 928–929. pmid:12868000 doi: 10.1038/sj.cdd.4401250
[34]  Geng X, Huang C, Qin Y, McCombs JE, Yuan Q, et al. (2012) Hepatitis B virus X protein targets Bcl-2 proteins to increase intracellular calcium, required for virus replication and cell death induction. Proc Natl Acad Sci U S A 109: 18471–18476. doi: 10.1073/pnas.1204668109. pmid:23091012
[35]  Kourtis N, Nikoletopoulou V, Tavernarakis N (2012) Small heat-shock proteins protect from heat-stroke-associated neurodegeneration. Nature 490: 213–218. doi: 10.1038/nature11417. pmid:22972192
[36]  Luke CJ, Pak SC, Askew YS, Naviglia TL, Askew DJ, et al. (2007) An intracellular serpin regulates necrosis by inhibiting the induction and sequelae of lysosomal injury. Cell 130: 1108–1119. pmid:17889653 doi: 10.1016/j.cell.2007.07.013
[37]  Artal-Sanz M, Samara C, Syntichaki P, Tavernarakis N (2006) Lysosomal biogenesis and function is critical for necrotic cell death in Caenorhabditis elegans. J Cell Biol 173: 231–239. pmid:16636145 doi: 10.1083/jcb.200511103
[38]  Troulinaki K, Tavernarakis N (2012) Endocytosis and intracellular trafficking contribute to necrotic neurodegeneration in C. elegans. EMBO J 31: 654–666. doi: 10.1038/emboj.2011.447. pmid:22157748
[39]  Hinas A, Wright AJ, Hunter CP (2012) SID-5 is an endosome-associated protein required for efficient systemic RNAi in C. elegans. Curr Biol 22: 1938–1943. doi: 10.1016/j.cub.2012.08.020. pmid:22981770
[40]  Treusch S, Knuth S, Slaugenhaupt SA, Goldin E, Grant BD, et al. (2004) Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc Natl Acad Sci U S A 101: 4483–4488. pmid:15070744 doi: 10.1073/pnas.0400709101
[41]  Geng X, Harry BL, Zhou Q, Skeen-Gaar RR, Ge X, et al. (2012) Hepatitis B virus X protein targets the Bcl-2 protein CED-9 to induce intracellular Ca2+ increase and cell death in Caenorhabditis elegans. Proc Natl Acad Sci U S A 109: 18465–18470. doi: 10.1073/pnas.1204652109. pmid:23091037
[42]  Palmer AE, Tsien RY (2006) Measuring calcium signaling using genetically targetable fluorescent indicators. Nat Protoc 1: 1057–1065. pmid:17406387 doi: 10.1038/nprot.2006.172
[43]  Coburn C, Allman E, Mahanti P, Benedetto A, Cabreiro F, et al. (2013) Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans. PLoS Biol 11: e1001613. doi: 10.1371/journal.pbio.1001613. pmid:23935448
[44]  Syntichaki P, Xu K, Driscoll M, Tavernarakis N (2002) Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419: 939–944. pmid:12410314 doi: 10.1038/nature01108
[45]  Pigott CR, Ellar DJ (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71: 255–281. pmid:17554045 doi: 10.1128/mmbr.00034-06
[46]  Lettre G, Hengartner MO (2006) Developmental apoptosis in C. elegans: a complex CEDnario. Nat Rev Mol Cell Biol 7: 97–108. pmid:16493416 doi: 10.1038/nrm1836
[47]  Samara C, Syntichaki P, Tavernarakis N (2008) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15: 105–112. pmid:17901876 doi: 10.1038/sj.cdd.4402231
[48]  Zou CG, Ma YC, Dai LL, Zhang KQ (2014) Autophagy protects C. elegans against necrosis during Pseudomonas aeruginosa infection. Proc Natl Acad Sci U S A 111: 12480–12485. doi: 10.1073/pnas.1405032111. pmid:25114220
[49]  Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9: 1102–1109. pmid:17909521 doi: 10.1038/ncb1007-1102
[50]  Ogura K, Wicky C, Magnenat L, Tobler H, Mori I, et al. (1994) Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev 8: 2389–2400. pmid:7958904 doi: 10.1101/gad.8.20.2389
[51]  Wong D, Bazopoulou D, Pujol N, Tavernarakis N, Ewbank JJ (2007) Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol 8: R194. pmid:17875205 doi: 10.1186/gb-2007-8-9-r194
[52]  Wang X, Li Y, Liu S, Yu X, Li L, et al. (2014) Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. Proc Natl Acad Sci U S A 111: 15438–15443. doi: 10.1073/pnas.1412767111. pmid:25316792
[53]  Rodrigue-Gervais IG, Labbe K, Dagenais M, Dupaul-Chicoine J, Champagne C, et al. (2014) Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host Microbe 15: 23–35. doi: 10.1016/j.chom.2013.12.003. pmid:24439895
[54]  Ruan L, Wang H, Cai G, Peng D, Zhou H, et al. (2015) A two-domain protein triggers heat shock pathway and necrosis pathway both in model plant and nematode. Environ Microbiol. doi: 10.1111/1462-2920.12968
[55]  Rahman K, Abdullah MA, Ambati S, Taylor MD, Adang MJ (2012) Differential protection of Cry1Fa toxin against Spodoptera frugiperda larval gut proteases by cadherin orthologs correlates with increased synergism. Appl Environ Microbiol 78: 354–362. doi: 10.1128/AEM.06212-11. pmid:22081566
[56]  Ruan L, Crickmore N, Peng D, Sun M (2015) Are nematodes a missing link in the confounded ecology of the entomopathogen Bacillus thuringiensis? Trends Microbiol 23: 341–346. doi: 10.1016/j.tim.2015.02.011. pmid:25818004
[57]  Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, et al. (2004) Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A 101: 10995–11000. pmid:15256590 doi: 10.1073/pnas.0404073101
[58]  Kao CY, Los FC, Huffman DL, Wachi S, Kloft N, et al. (2011) Global functional analyses of cellular responses to pore-forming toxins. PLoS Pathog 7: e1001314. doi: 10.1371/journal.ppat.1001314. pmid:21408619
[59]  Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94. pmid:4366476
[60]  Guo S, Liu M, Peng D, Ji S, Wang P, et al. (2008) New strategy for isolating novel nematicidal crystal protein genes from Bacillus thuringiensis strain YBT-1518. Appl Environ Microbiol 74: 6997–7001. doi: 10.1128/AEM.01346-08. pmid:18820056
[61]  Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254. pmid:942051 doi: 10.1016/0003-2697(76)90527-3
[62]  Bischof LJ, Huffman DL, Aroian RV (2006) Assays for toxicity studies in C. elegans with Bt crystal proteins. Methods Mol Biol 351: 139–154. pmid:16988432 doi: 10.1385/1-59745-151-7:139
[63]  Schrimpf SP, Langen H, Gomes AV, Wahlestedt C (2001) A two-dimensional protein map of Caenorhabditis elegans. Electrophoresis 22: 1224–1232. pmid:11358149 doi: 10.1002/1522-2683()22:6<1224::aid-elps1224>3.3.co;2-9
[64]  Mello C, Fire A (1995) DNA transformation. Methods Cell Biol 48: 451–482. pmid:8531738 doi: 10.1016/s0091-679x(08)61399-0
[65]  Griffitts JS, Huffman DL, Whitacre JL, Barrows BD, Marroquin LD, et al. (2003) Resistance to a bacterial toxin is mediated by removal of a conserved glycosylation pathway required for toxin-host interactions. J Biol Chem 278: 45594–45602. pmid:12944392 doi: 10.1074/jbc.m308142200
[66]  Zhang R, Hua G, Andacht TM, Adang MJ (2008) A 106-kDa aminopeptidase is a putative receptor for Bacillus thuringiensis Cry11Ba toxin in the mosquito Anopheles gambiae. Biochemistry 47: 11263–11272. doi: 10.1021/bi801181g. pmid:18826260
[67]  Ladbury JE, Chowdhry BZ (1996) Sensing the heat: the application of isothermal titration calorimetry to thermodynamic studies of biomolecular interactions. Chem Biol 3: 791–801. pmid:8939696 doi: 10.1016/s1074-5521(96)90063-0
[68]  Fragoso RR, Lourenco IT, Batista JA, Oliveira-Neto OB, Silva MC, et al. (2009) Meloidogyne incognita: molecular cloning and characterization of a cDNA encoding a cathepsin D-like aspartic proteinase. Exp Parasitol 121: 115–123. doi: 10.1016/j.exppara.2008.09.017. pmid:18952081
[69]  Finney D (1971) Probit analysis. Cambridge, England: University Press.

Full-Text

comments powered by Disqus

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133

WeChat 1538708413