Disruption of the C. elegans intestinal brush border by the fungal lectin CCL2 phenocopies dietary lectin toxicity in mammals

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Stutz, Katrin ^a   Kaech, Andres ^a   Aebi, Markus ^b   Künzler, Markus ^b   Hengartner, Michael O ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COPRINOPSIS CINEREA LECTIN 2 PROTEIN; FATTY ACID; LECTIN; UNCLASSIFIED DRUG; FUNGAL PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL DISRUPTION; CELL LOSS; CONTROLLED STUDY; GENOTYPE; INTESTINE BRUSH BORDER; INTESTINE EPITHELIUM; LONG TERM EXPOSURE; METABOLOMICS; MICROVILLUS; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; RNA INTERFERENCE; SURFACE PROPERTY; TOXICITY TESTING; WILD TYPE; ALLELE; ANIMAL; CELL MEMBRANE; DIET; FUNGUS; GENETIC SCREENING; GENETICS; GLYCOCALYX; INTESTINE; MAMMAL; METABOLISM; MICROBIOLOGY; PROCEDURES;

CAENORHABDITIS ELEGANS; COPRINOPSIS CINEREA; FUNGI; MAMMALIA; NEMATODA; RATTUS; TRITICUM AESTIVUM;

ALLELES; ANIMALS; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CHEMOKINE CCL2; DIET; FUNGAL PROTEINS; FUNGI; GENETIC TESTING; GLYCOCALYX; INTESTINES; LECTINS; MAMMALS;

EID: 84936863599     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129381     Document Type: Article

References (67)

1. Gabius H. Eukaryotic Glycosylation and Lectins: Hardware of the Sugar Code (Glycocode) in Biological Information Transfer. EJPathol. 2001; 7.
2. Van Damme EJM, Barre A, Rougé P, Peumans WJ. Cytoplasmic/nuclear plant lectins: a new story. Trends Plant Sci. 2004; 9: 484-489. doi: 10.1016/j.tplants.2004.08.003 PMID: 15465683
3. Khan F, Islam Khan M. Fungal Lectins: Current molecular and biochemical perspectives. Int J Biol Chem. 2011; 5: 1-20. doi: 10.3923/ijbc.2011.1.20
4. Peumans W, Damme E Van. Lectins as plant defense proteins. Plant Physiol. 1995; 347-352.
5. Bleuler-Martínez S, Butschi A, Garbani M, Wa¨lti MA, Wohlschlager T, Potthoff E, et al. A lectin-mediated resistance of higher fungi against predators and parasites. Mol Ecol. 2011; 20: 3056-3070. doi: 10.1111/j.1365-294X.2011.05093.x PMID: 21486374
6. Hamid R, Masood A. Dietary Lectins as Disease Causing Toxicants. Pakistan J Nutr. 2009; 8: 293-303. doi: 10.3923/pjn.2009.293.303
7. McGhee JD. The C. elegans intestine (March 27, 2007). WormBook, ed. The C. elegans Research Community, WormBook. doi: 10.1895/wormbook.1.133.1, Available: http://www.wormbook.org
8. Van Buul VJ, Brouns FJPH. Health effects of wheat lectins: A review. J Cereal Sci. 2014; 59: 112-117. doi: 10.1016/j.jcs.2014.01.010
9. Lorenzsonn V, Olsen WA. In vivo responses of rat intestinal epithelium to intraluminal dietary lectins. Gastroenterology. 1982; 82: 838-848. PMID: 6895878
10. Schubert M, Bleuler-Martinez S, Butschi A, Wa¨lti MA, Egloff P, Stutz K, et al. Plasticity of the β-trefoil protein fold in the recognition and control of invertebrate predators and parasites by a fungal defence system. PLoS Pathog. 2012; 8. doi: 10.1371/journal.ppat.1002706
11. Sulzenbacher G, Roig-Zamboni V, Peumans WJ, Rougé P, Van Damme EJM, Bourne Y. Crystal structure of the GalNAc/Gal-specific agglutinin from the phytopathogenic ascomycete Sclerotinia sclerotiorum reveals novel adaptation of a β-trefoil domain. J Mol Biol. 2010; 400: 715-723. doi: 10.1016/j.jmb.2010.05.038 PMID: 20566411
12. Hamshou M, Smagghe G, Shahidi-Noghabi S, De Geyter E, Lannoo N, Van Damme EJM. Insecticidal properties of Sclerotinia sclerotiorum agglutinin and its interaction with insect tissues and cells. Insect Biochem Mol Biol. 2010; 40: 883-890. doi: 10.1016/j.ibmb.2010.08.008 PMID: 20826211
13. Francis F, Marty-Detraves C, Poincloux R, Baricault L, Fournier D, Paquereau L. Fungal lectin, XCL, is internalized via clathrin-dependent endocytosis and facilitates uptake of other molecules. Eur J Cell Biol. 2003; 82: 515-522. doi: 10.1078/0171-9335-00338 PMID: 14629119
14. Endo Y, Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem. 1987; 262: 8128-8130. PMID: 3036799
15. Wohlschlager T, Butschi A, Zurfluh K, Vonesch SC, Auf Dem Keller U, Gehrig P, et al. Nematotoxicity of Marasmius oreades Agglutinin (MOA) depends on glycolipid binding and cysteine protease activity. J Biol Chem. 2011; 286: 30337-30343. doi: 10.1074/jbc.M111.258202 PMID: 21757752
16. Tateno H, Goldstein IJ. Molecular Cloning, Expression, and Characterization of novel hemolytic lectins from the mushroom Laetiporus sulphureus, which show homology to bacterial toxins. J Biol Chem. 2003; 278: 40455-40463. doi: 10.1074/jbc.M306836200 PMID: 12900403
17. Darby C. Interactions with microbial pathogens (September 6, 2005). WormBook, ed. The C. elegans Research Community, WormBook. doi: 10.1895/wormbook.1.21.1, Available: http://www.wormbook.org
18. Félix MA, Ashe A, Piffaretti J, Wu G, Nuez I, Bélicard T, et al. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol. 2011; 9. doi: 10.1371/journal.pbio.1000586
19. Estes KA, Szumowski SC, Troemel ER. Non-lytic, actin-based exit of intracellular parasites from C. elegans intestinal cells. PLoS Pathog. 2011; 7. doi: 10.1371/journal.ppat.1002227
20. Sifri CD, Begun J, Ausubel FM. The worm has turned - microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol. 2005; 13: 119-127. doi: 10.1016/j.tim.2005.01.003 PMID: 15737730
21. Wei J- Z, Hale K, Carta L, Platzer E, Wong C, Fang S-C, et al. Bacillus thuringiensis crystal proteins that target nematodes. Proc Natl Acad Sci U S A. 2003; 100: 2760-2765. doi: 10.1073/pnas.0538072100 PMID: 12598644
22. Irazoqui JE, Troemel ER, Feinbaum RL, Luhachack LG, Cezairliyan BO, Ausubel FM. Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog. 2010; 6. doi: 10.1371/journal.ppat.1000982
23. Leung MCK, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M, et al. Caenorhabditis elegans: An emerging model in biomedical and environmental toxicology. Toxicol Sci. 2008; 106: 5-28. doi: 10.1093/toxsci/kfn121 PMID: 18566021
24. Varrot A, Basheer SM, Imberty A. Fungal lectins: Structure, function and potential applications. Curr Opin Struct Biol. 2013; 23: 678-685. doi: 10.1016/j.sbi.2013.07.007 PMID: 23920351
25. Yan S, Serna S, Reichardt NC, Paschinger K, Wilson IBH. Array-assisted characterization of a fucosyl-transferase required for the biosynthesis of complex core modifications of nematode N-glycans. J Biol Chem. 2013; 288: 21015-21028. doi: 10.1074/jbc.M113.479147 PMID: 23754284
26. Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature. 2007; 448: 366-369. doi: 10.1038/nature05929 PMID: 17597763
27. Carberry K, Wiesenfahrt T, Geisler F, Stocker S, Gerhardus H, Uberbach D, et al. The novel intestinal filament organizer IFO-1 contributes to epithelial integrity in concert with ERM-1 and DLG-1. J Cell Sci. 2012; 139: 1851-1862. doi: 10.1242/jcs.112854
28. Zhang H, Abraham N, Khan LA, Hall DH, Fleming JT, Göbel V. Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat Cell Biol. 2011; 13: 1189-1201. doi: 10.1038/ncb2328 PMID: 21926990
29. Khan LA, Zhang H, Abraham N, Sun L, Fleming JT, Buechner M, et al. Intracellular lumen extension requires ERM-1-dependent apical membrane expansion and AQP-8-mediated flux. Nat Cell Biol. 2013; 15: 143-156. doi: 10.1038/ncb2656 PMID: 23334498
30. Hüsken K, Wiesenfahrt T, Abraham C, Windoffer R, Bossinger O, Leube RE. Maintenance of the intestinal tube in Caenorhabditis elegans: The role of the intermediate filament protein IFC-2. Differentiation. 2008; 76: 881-896. doi: 10.1111/j.1432-0436.2008.00264.x PMID: 18452552
31. Bellier A, Chen CS, Kao CY, Cinar HN, Aroian R V. Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans. PLoS Pathog. 2009; 5. doi: 10.1371/journal.ppat.1000689
32. Los FCO, Kao CY, Smitham J, McDonald KL, Ha C, Peixoto CA, et al. RAB-5- and RAB-11-dependent vesicle-trafficking pathways are required for plasma membrane repair after attack by bacterial poreforming toxin. Cell Host Microbe. 2011; 9: 147-151. doi: 10.1016/j.chom.2011.01.005 PMID: 21320697
33. Vanfleteren JR, Braeckman BP. Mechanisms of life span determination in Caenorhabditis elegans. Neurobiol Aging. 1999; 20: 487-502. doi: 10.1016/S0197-4580(99)00087-1 PMID: 10638522
34. Zhou H, Sun L, Li J, Xu C, Yu F, Liu Y, et al. The crystal structure of human GDP-L-fucose synthase. Acta Biochim Biophys Sin. 2013; 720-725. doi: 10.1093/abbs/gmt066.Advance
35. Somers WS, Stahl ML, Sullivan FX. GDP-fucose synthetase from Escherichia coli: structure of a unique member of the short-chain dehydrogenase/reductase family that catalyzes two distinct reactions at the same active site. Structure. 1998; 6: 1601-1612. doi: 10.1016/S0969-2126(98)00157-9 PMID: 9862812
36. Fei Y, Fujita T, Lapp D, Ganapathy V, Leibach F. Two oligopeptide transporters from Caenorhabditis elegans: molecular cloning and functional expression. Biochem J. 1998; 332: 565-572. PMID: 9601088
37. Nehrke K. A Reduction in intestinal cell pHi due to loss of the Caenorhabditis elegans Na+/H+ exchanger NHX-2 increases life span. J Biol Chem. 2003; 278: 44657-44666. doi: 10.1074/jbc.M307351200 PMID: 12939266
38. Geiger O, López-Lara IM, Sohlenkamp C. Phosphatidylcholine biosynthesis and function in bacteria. Biochim Biophys Acta - Mol Cell Biol Lipids. 2013; 1831: 503-513. doi: 10.1016/j.bbalip.2012.08.009
39. Broderick NA, Raffa KF, Handelsman J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci U S A. 2006; 103: 15196-15199. doi: 10.1073/pnas.0604865103 PMID: 17005725
40. Van Dijk JE, Huisman J, Koninkx JFJG. Structural and functional aspects of a healthy gastrointestinal tract. In: Blok MC, Vahl HA, de Lange L, v.c. Braak AE, Hemke G, Hessing M, editors. Nutrition and Health of the Gastrointestinal Tract. Wageningen Academic Pub; 2002. pp. 81-83.
41. Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell. 1999; 96: 47-56. doi: 10.1016/S0092-8674(00)80958-7 PMID: 9989496
42. Sharon N. Lectins: carbohydrate-specific reagents and biological recognition molecules. J Biol Chem. 2007; 282: 2753-2764. doi: 10.1074/JBC.X600004200 PMID: 17145746
43. Miyake K, Tanaka T, McNeil PL. Lectin-based food poisoning: A new mechanism of protein toxicity. PLoS One. 2007; 2. doi: 10.1371/journal.pone.0000687
44. Ubelmann F, Chamaillard M, El-Marjou F, Simon A, Netter J, Vignjevic D, et al. Enterocyte loss of polarity and gut wound healing rely upon the F-actin-severing function of villin. Proc Natl Acad Sci U S A. 2013; 110: E1380-1389. doi: 10.1073/pnas.1218446110 PMID: 23520048
45. Engelmann I, Pujol N. Innate Immunity in C. elegans. In: Söderha¨ll K, editor. Invertebrate Immunity. XXIV. Landes Bioscience and Springer Science+Business Media; 2010. pp. 105-121.
46. Schulenburg H, Hoeppner MP, Weiner J, Bornberg-Bauer E. Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans. Immunobiology. 2008; 213: 237-250. doi: 10.1016/j.imbio.2007.12.004 PMID: 18406370
47. Barrows BD, Haslam SM, Bischof LJ, Morris HR, Dell A, Aroian R V. Resistance to Bacillus thuringiensis toxin in Caenorhabditis elegans from loss of fucose. J Biol Chem. 2007; 282: 3302-3311. doi: 10.1074/jbc.M606621200 PMID: 17135259
48. Pusztai A, Ewen SWB, Grant G, Peumans WJ, Van Damme EJM, Coates ME, et al. Lectins and also bacteria modify the glycosylation of gut surface receptors in the rat. Glycoconj J. 1995; 12: 22-35. doi: 10.1007/BF00731865 PMID: 7795410
49. MacQueen AJ, Baggett JJ, Perumov N, Bauer RA, Januszewski T, Schriefer L, et al. ACT-5 is an essential Caenorhabditis elegans actin required for intestinal microvilli formation. Mol Biol Cell. 2005; 16: 3247-3259. doi: 10.1091/mbc.E04-12-1061 PMID: 15872090
50. Croce A, Cassata G, Disanza A, Gagliani MC, Tacchetti C, Malabarba MG, et al. A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat Cell Biol. 2004; 6: 1173-1179. doi: 10.1038/ncb1198 PMID: 15558032
51. Göbel V, Barrett PL, Hall DH, Fleming JT. Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev Cell. 2004; 6: 865-873. doi: 10.1016/j.devcel.2004.05.018 PMID: 15177034
52. Walser PJ, Kües U, Aebi M, Künzler M. Ligand interactions of the Coprinopsis cinerea galectins. Fungal Genet Biol. 2005; 42: 293-305. doi: 10.1016/j.fgb.2004.12.004 PMID: 15749049
53. Stiernagle T. Maintenance of C. elegans (February 11, 2006). WormBook, ed. The C. elegans Research Community, WormBook. doi: 10.1895/wormbook.1.101.1, Available: http://www.wormbook.org
54. Castelein N, Hoogewijs D, De Vreese A, Braeckman BP, Vanfleteren JR. Dietary restriction by growth in axenic medium induces discrete changes in the transcriptional output of genes involved in energy metabolism in Caenorhabditis elegans. Biotechnol J. 2008; 3: 803-812. doi: 10.1002/biot.200800003 PMID: 18383023
55. Lowe DG. Distinctive image features from scale-invariant keypoints. Int J Comput Vis. 2004; 60: 91-110. doi: 10.1023/B:VISI.0000029664.99615.94
56. Rasband WS. ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA; 2014. Available: http://imagej.nih.gov/ij/
57. Walker AK, Jacobs RL, Watts JL, Rottiers V, Jiang K, Finnegan DM, et al. A conserved SREBP-1/phosphatidylcholine feedback circuit regulates lipogenesis in metazoans. Cell. 2011; 147: 840-852. doi: 10.1016/j.cell.2011.09.045 PMID: 22035958
58. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 2003; 100: 9440-9445. doi: 10.1073/pnas.1530509100 PMID: 12883005
59. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2001; 2: RESEARCH0002. doi: 10.1186/gb-2000-2-1-research0002 PMID: 11178279
60. Timmons L, Court DL, Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene. 2001; 263: 103-112. doi: 10.1016/S0378-1119(00)00579-5 PMID: 11223248
61. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974; 77: 71-94. doi: 10.1002/cbic.200300625 PMID: 4366476
62. Zipperlen P, Nairz K, Rimann I, Basler K, Hafen E, Hengartner M, et al. A universal method for automated gene mapping. Genome Biol. 2005; 6: R19. doi: 10.1186/gb-2005-6-2-r19 PMID: 15693948
63. Doitsidou M, Poole RJ, Sarin S, Bigelow H, Hobert O. C. elegans mutant identification with a one-step whole-genome-sequencing and SNP mapping strategy. PLoS One. 2010; 5. doi: 10.1371/journal.pone.0015435
64. Yook K. Complementation (October 06, 2005). WormBook, ed. The C. elegans Research Community, WormBook. doi: 10.1895/wormbook.1.24.1, Available: http://www.wormbook.org
65. Butschi A, Titz A, Wa¨lti MA, Olieric V, Paschinger K, Nöbauer K, et al. Caenorhabditis elegans N-glycan Core β-galactoside confers sensitivity towards nematotoxic fungal galectin CGL2. PLoS Pathog. 2010; 6. doi: 10.1371/journal.ppat.1000717
66. Praitis V, Casey E, Collar D, Austin J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics. 2001; 157: 1217-1226. PMID: 11238406
67. Kaletta T, Hengartner MO. Finding function in novel targets: C. elegans as a model organism. Nat Rev Drug Discov. 2006; 5: 387-398. doi: 10.1038/nrd2031 PMID: 16672925