The SKPO-1 peroxidase functions in the hypodermis to protect Caenorhabditis Elegans from bacterial infection

Genetics

Volumn 197, Issue 2, 2014, Pages 515-526

  Tiller, George R ^a   Garsin, Danielle A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DOUBLE STRANDED RNA; HYDROGEN PEROXIDE; PEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SKPO 1 PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; SKPO-1 PROTEIN, C ELEGANS;

ARTICLE; BACTERIAL INFECTION; CAENORHABDITIS ELEGANS; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HOST RESISTANCE; IMMUNOFLUORESCENCE; IMMUNOGOLD LABELING; LONGEVITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA; RNA INTERFERENCE; SUBCUTANEOUS TISSUE; TRANSMISSION ELECTRON MICROSCOPY; VECTOR CONTROL; WILD TYPE; ANIMAL; DISEASE RESISTANCE; ENZYMOLOGY; GENETICS; GRAM POSITIVE INFECTION; IMMUNOLOGY; MICROBIOLOGY; MUTATION; PATHOGENICITY; PENETRANCE; PSEUDOMONAS INFECTION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DISEASE RESISTANCE; ENTEROCOCCUS FAECALIS; GRAM-POSITIVE BACTERIAL INFECTIONS; MUTATION; PENETRANCE; PEROXIDASE; PHENOTYPE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RNA INTERFERENCE;

EID: 84902493727     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.160606     Document Type: Article

References (53)

1. Breger, J., B. B. Fuchs, G. Aperis, T. I. Moy, F. M. Ausubel et al., 2007 Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog. 3: e18.
2. Brenner, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
3. Chavez, V., A. Mohri-Shiomi, A. Maadani, L. A. Vega, and D. A. Garsin, 2007 Oxidative stress enzymes are required for DAF-16-mediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans. Genetics 176: 1567-1577.
4. Chavez, V., A. Mohri-Shiomi, and D. A. Garsin, 2009 Ce-Duox1/ BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect. Immun. 77: 4983-4989.
5. Conner, G. E., M. Salathe, and R. Forteza, 2002 Lactoperoxidase and hydrogen peroxide metabolism in the airway. Am. J. Respir. Crit. Care Med. 166: S57-S61.
6. Couillault, C., and J. J. Ewbank, 2002 Diverse bacteria are pathogens of Caenorhabditis elegans. Infect. Immun. 70: 4705-4707.
7. Cruz, M. R., C. E. Graham, B. C. Gagliano, M. C. Lorenz, and D. A. Garsin, 2013 Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect. Immun. 81: 189-200.
8. Darby, C., J. W. Hsu, N. Ghori, and S. Falkow, 2002 Caenorhabditis elegans: plague bacteria biofilm blocks food intake. Nature 417: 243-244.
9. Dunny, G. M., B. L. Brown, and D. B. Clewell, 1978 Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc. Natl. Acad. Sci. USA 75: 3479-3483.
10. Edens, W. A., L. Sharling, G. Cheng, R. Shapira, J. M. Kinkade et al., 2001 Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J. Cell Biol. 154: 879-891.
11. Engelmann, I., A. Griffon, L. Tichit, F. Montanana-Sanchis, G. Wang et al., 2011 A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. ele-gans. PLoS ONE 6: e19055.
12. Forteza, R., M. Salathe, F. Miot, R. Forteza, and G. E. Conner, 2005 Regulated hydrogen peroxide production by Duox in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 32: 462-469.
13. Fraser, A. G., R. S. Kamath, P. Zipperlen, M. Martinez-Campos, M. Sohrmann et al., 2000 Functional genomic analysis of C. ele-gans chromosome I by systematic RNA interference. Nature 408: 325-330.
14. Garigan, D., A. L. Hsu, A. G. Fraser, R. S. Kamath, J. Ahringer et al., 2002 Genetic analysis of tissue aging in Caenorhabditis ele-gans: a role for heat-shock factor and bacterial proliferation. Genetics 161: 1101-1112.
15. Garsin, D. A., C. D. Sifri, E. Mylonakis, X. Qin, K. V. Singh et al., 2001 A simple model host for identifying Gram-positive virulence factors. Proc. Natl. Acad. Sci. USA 98: 10892-10897.
16. Garsin, D. A., J. M. Villanueva, J. Begun, D. H. Kim, C. D. Sifri et al., 2003 Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300: 1921.
17. Geiszt, M., K. Lekstrom, S. Brenner, S. M. Hewitt, R. Dana et al., 2003 NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J. Immunol. 171: 299-306.
18. Ha, E. M., C. T. Oh, Y. S. Bae, and W. J. Lee, 2005a A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847-850.
19. Ha, E. M., C. T. Oh, J. H. Ryu, Y. S. Bae, S. W. Kang et al., 2005b An antioxidant system required for host protection against gut infection in Drosophila. Dev. Cell 8: 125-132.
20. Hodgkin, J., P. E. Kuwabara, and B. Corneliussen, 2000 A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr. Biol. 10: 1615-1618.
21. Hope, I. A., 1999 C. elegans: A Practical Approach, Oxford University Press, Oxford.
22. Irazoqui, J. E., A. Ng, R. J. Xavier, and F. M. Ausubel, 2008 Role for beta-catenin and HOX transcription factors in Caenorhabdi-tis elegans and mammalian host epithelial-pathogen interactions. Proc. Natl. Acad. Sci. USA 105: 17469-17474.
23. Irazoqui, J. E., E. R. Troemel, R. L. Feinbaum, L. G. Luhachack, B. O. Cezairliyan et al., 2010 Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog. 6: e1000982.
24. Jansson, H. B., A. Jeyaprakash, and B. M. Zuckerman, 1985 Differential adhesion and infection of nematodes by the endoparasitic fungus Meria coniospora (Deuteromycetes). Appl. Environ. Microbiol. 49: 552-555.
25. Kamath, R. S., A. G. Fraser, Y. Dong, G. Poulin, R. Durbin et al., 2003 Systematic functional analysis of the Caenorhabditis ele-gans genome using RNAi. Nature 421: 231-237.
26. Kennedy, S., D. Wang, and G. Ruvkun, 2004 A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427: 645-649.
27. Kim, D. H., R. Feinbaum, G. Alloing, F. E. Emerson, D. A. Garsin et al., 2002 A conserved p38 MAP kinase pathway in Caeno-rhabditis elegans innate immunity. Science 297: 623-626.
28. Klebanoff, S. J., 2005 Myeloperoxidase: friend and foe. J. Leukoc. Biol. 77: 598-625.
29. Meitzler, J. L., and P. R. Ortiz de Montellano, 2009 Caenorhabditis elegans and human dual oxidase 1 (DUOX1) "peroxidase" domains: insights into heme binding and catalytic activity. J. Biol. Chem. 284: 18634-18643.
30. Meitzler, J. L., and P. R. Ortiz de Montellano, 2011 Structural stability and heme binding potential of the truncated human dual oxidase 2 (DUOX2) peroxidase domain. Arch. Biochem. Biophys. 512: 197-203.
31. Meitzler, J. L., R. Brandman, and P. R. Ortiz de Montellano, 2010 Perturbed heme binding is responsible for the blistering phenotype associated with mutations in the Caenorhabditis el-egans dual oxidase 1 (DUOX1) peroxidase domain. J. Biol. Chem. 285: 40991-41000.
32. Meitzler, J. L., S. Hinde, B. Banfi, W. M. Nauseef, and P. R. Ortiz de Montellano, 2013 Conserved cysteine residues provide a protein-protein interaction surface in dual oxidase (DUOX) proteins. J. Biol. Chem. 288: 7147-7157.
33. Melo, J. A., and G. Ruvkun, 2012 Inactivation of conserved C. elegans genes engages pathogenand xenobiotic-associated defenses. Cell 149: 452-466.
34. Mohri-Shiomi, A., and D. A. Garsin, 2008 Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J. Biol. Chem. 283: 194-201.
35. Moskwa, P., D. Lorentzen, K. J. Excoffon, J. Zabner, P. B. McCray, Jr. et al., 2007 A novel host defense system of airways is defective in cystic fibrosis. Am. J. Respir. Crit. Care Med. 175: 174-183.
36. Niethammer, P., C. Grabher, A. T. Look, and T. J. Mitchison, 2009 A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459: 996-999.
37. Ortiz de Montellano, P. R., 2008 Mechanism and role of covalent heme binding in the CYP4 family of P450 enzymes and the mammalian peroxidases. Drug Metab. Rev. 40: 405-426.
38. Page, A. P., and I. L. Johnstone, 2007 The cuticle (March 19, 2007), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.138.1, http://www.wormbook.org.
39. Pujol, N., O. Zugasti, D. Wong, C. Couillault, C. L. Kurz et al., 2008 Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog. 4: e1000105.
40. Rada, B., K. Lekstrom, S. Damian, C. Dupuy, and T. L. Leto, 2008 The Pseudomonas toxin pyocyanin inhibits the dual oxidase-based antimicrobial system as it imposes oxidative stress on airway epithelial cells. J. Immunol. 181: 4883-4893.
41. Rahme, L. G., E. J. Stevens, S. F. Wolfort, J. Shao, R. G. Tompkins et al., 1995 Common virulence factors for bacterial pathoge-nicity in plants and animals. [see comments] Science 268: 1899-1902.
42. Seydoux, G., and M. A. Dunn, 1997 Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA poly-merase II in early embryos of Caenorhabditis elegans and Dro-sophila melanogaster. Development 124: 2191-2201.
43. Shapira, M., B. J. Hamlin, J. Rong, K. Chen, M. Ronen et al., 2006 A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc. Natl. Acad. Sci. USA 103: 14086-14091.
44. Simmer, F., C. Moorman, A. M. van der Linden, E. Kuijk, P. V. van den Berghe et al., 2003 Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1: E12.
45. Singh, V., and A. Aballay, 2012 Endoplasmic reticulum stress pathway required for immune homeostasis is neurally controlled by arrestin-1. J. Biol. Chem. 287: 33191-33197.
46. Soudi, M., M. Zamocky, C. Jakopitsch, P. G. Furtmuller, and C. Obinger, 2012 Molecular evolution, structure, and function of peroxidasins. Chem. Biodivers. 9: 1776-1793.
47. Sumimoto, H., 2008 Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275: 3249-3277.
48. Tenor, J. L., B. A. McCormick, F. M. Ausubel, and A. Aballay, 2004 Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr. Biol. 14: 1018-1024.
49. Thein, M. C., A. D. Winter, G. Stepek, G. McCormack, G. Stapleton et al., 2009 Combined extracellular matrix cross-linking activity of the peroxidase MLT-7 and the dual oxidase BLI-3 is critical for post-embryonic viability in Caenorhabditis elegans. J. Biol. Chem. 284: 17549-17563.
50. Tsang, S. W., C. Q. Nguyen, D. H. Hall, and K. L. Chow, 2007 Mab-7 encodes a novel transmembrane protein that orchestrates sensory ray morphogenesis in C. elegans. Dev. Biol. 312: 353-366.
51. van der Hoeven, R., K. C. McCallum, M. R. Cruz, and D. A. Garsin, 2011 Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog. 7: e1002453.
52. Wong, D., D. Bazopoulou, N. Pujol, N. Tavernarakis, and J. J. Ewbank, 2007 Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol. 8: R194.
53. Zamocky, M., C. Jakopitsch, P. G. Furtmuller, C. Dunand, and C. Obinger, 2008 The peroxidase-cyclooxygenase superfamily: reconstructed evolution of critical enzymes of the innate immune system. Proteins 72: 589-605.