DAF-16-dependent suppression of immunity during reproduction in Caenorhabditis elegans

Genetics

Volumn 178, Issue 2, 2008, Pages 903-918

  Miyata, Sachiko ^a   Begun, Jakob ^a,b   Troemel, Emily R ^a,b   Ausubel, Frederick M ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; TRANSCRIPTION FACTOR DAF 16;

ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; FEMALE; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; GENOTYPE; GRAM NEGATIVE INFECTION; IMMUNE RESPONSE; IMMUNITY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RNA INTERFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; UPREGULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMOSOME MAPPING; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION TEST; GENETIC SCREENING; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCTION; SUPPRESSION, GENETIC; TRANSCRIPTION FACTORS;

ANIMALIA; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS;

EID: 40849098017     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.083923     Document Type: Article

References (75)

1. ABALLAY, A., P. YORGEY and F. M. AUSUBEL, 2000 Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr. Biol. 10: 1539-1542.
2. AKIRA, S., S. UEMATSU and O. TAKEUCHI, 2006 Pathogen recognition and innate immunity. Cell 124: 783-801.
3. ARANTES-OLIVEIRA, N., J. APFELD, A. DILLIN and C. KENYON, 2002 Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295: 502-505.
4. ARANTES-OLIVEIRA, N., J. R. BERMAN and C. KENYON, 2003 Healthy animals with extreme longevity. Science 302: 611.
5. AUSUBEL, F. M., 2005 Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6: 973-979.
6. BAIROCH, A., and R. APWEILER, 2000 The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28: 45-48.
7. BANY, I. A., M. Q. DONG and M. R. KOELLE, 2003 Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior. J. Neurosci. 23: 8060-8069.
8. BARTON, M. K., T. B. SCHEDL and J. KIMBLE, 1987 Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 115: 107-119.
9. BERMAN, J. R., and C. KENYON, 2006 Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell 124: 1055-1068.
10. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
11. 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.
12. DAVIS, M. W., M. HAMMARLUND, T. HARRACH, P. HULLETT, S. OLSEN et al., 2005 Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics 6: 118.
13. DERNBURG, A. F., J. ZALEVSKY, M. P. COLAIACOVO and A.M. VILLENEUVE, 2000 Transgene-mediated cosuppression in the C. elegans germ line. Genes Dev. 14: 1578-1583.
14. DILLIN, A., D. K. CRAWFORD and C. KENYON, 2002 Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298: 830-834.
15. EPSTEIN, H. F. S., and D. C. SHAKES (Editors), 1995 Caenorhabditis elegans: Modern Biological Analysis of an Organism. Academic Press, New York.
16. FEDORKA, K. M., M. ZUK and T. A. MOUSSEAU, 2004 Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58: 2478-2485.
17. FIRE, A., S. XU, M. K. MONTGOMERY, S. A. KOSTAS, S. E. DRIVER et al., 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
18. FOWLER, K., and L. PARTRIDGE, 1989 A cost of mating in female fruit-flies. Nature 338: 760-761.
19. 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.
20. GOTTLIEB, S., and G. RUVKUN, 1994 daf-2, daf-16, and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics 137: 107-120.
21. GOVINDAN, J. A., H. CHENG, J. E. HARRIS and D. GREENSTEIN, 2006 Galphao/i and Galphas signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr. Biol. 16: 1257-1268.
22. GRAVATO-NOBRE, M. J., and J. HODGKIN, 2005 Caenorhabditis elegans as a model for innate immunity to pathogens. Cell Microbiol. 7: 741-751.
23. HAMILTON, B., Y. DONG, M. SHINDO, W. LIU, I. ODELL et al., 2005 A systematic RNAi screen for longevity genes in C. elegans. Genes Dev. 19: 1544-1555.
24. HANSEN, M., A. L. HSU, A. DILLIN and C. KENYON, 2005 New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet. 1: 119-128.
25. HARRIS, T. W., R. LEE, E. SCHWARZ, K. BRADNAM, D. LAWSON et al., 2003 WormBase: a cross-species database for comparative genomics. Nucleic Acids Res. 31: 133-137.
26. HAUTEKEETE, N. C., Y. PIQUOT and H. VAN DIJK, 2001 Investment in survival and reproduction along a semelparity-iteroparity gradient in the Beta species complex. J. Evol. Biol. 14: 795-804.
27. HENDERSON, S. T., and T. E. JOHNSON, 2001 daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11: 1975-1980.
28. HSIN, H., and C. KENYON, 1999 Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399: 362-366.
29. HSU, A. L., C. T. MURPHY and C. KENYON, 2003 Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300: 1142-1145.
30. KAMATH, R. S., A. G. FRASER, Y. DONG, G. POULIN, R. DURBIN et al., 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
31. KENYON, C., J. CHANG, E. GENSCH, A. RUDNER and R. TABTIANG, 1993 A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
32. KIM, D. H., and F. M. AUSUBEL, 2005 Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr. Opin. Immunol. 17: 4-10.
33. KIM, D. H., R. FEINBAUM, G. ALLOING, F. E. EMERSON, D. A. GARSIN et al., 2002 A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297: 623-626.
34. KLEIN, S. L., and R. J. NELSON, 1999 Influence of social factors on immune function and reproduction. Rev. Reprod. 4: 168-178.
35. KURZ, C. L., and J. J. EWBANK, 2003 Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nat. Rev. Genet. 4: 380-390.
36. LEE, R. Y., J. HENCH and G. RUVKUN, 2001 Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr. Biol. 11: 1950-1957.
37. LIBINA, N., J. R. BERMAN and C. KENYON, 2003 Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489-502.
38. LIN, K., J. B. DORMAN, A. RODAN and C. KENYON, 1997 daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319-1322.
39. LIN, K., H. HSIN, N. LIBINA and C. KENYON, 2001 Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat. Genet. 28: 139-145.
40. MAHAJAN-MIKLOS, S., M. W. TAN, L. G. RAHME and F. M. AUSUBEL, 1999 Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56.
41. MALLO, G. V., C. L. KURZ, C. COUILLAULT, N. PUJOL, S. GRANJEAUD et al., 2002 Inducible antibacterial defense system in C. elegans. Curr. Biol. 12: 1209-1214.
42. MARCHLER-BAUER, A., J. B. ANDERSON, P. F. CHERUKURI, C. DEWEESE-SCOTT, L. Y. GEER et al., 2005 CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33: D192-D196.
43. MCCARROLL, S. A., C. T. MURPHY, S. ZOU, S. D. PLETCHER, C. S. CHIN et al., 2004 Comparing genomic expression patterns across species identifies shared transcriptional profile in aging. Nat. Genet. 36: 197-204.
44. MCELWEE, J., K. BUBB and J. H. THOMAS, 2003 Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2: 111-121.
45. MCKEAN, K. A., and L. NUNNEY, 2001 Increased sexual activity reduces male immune function in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98: 7904-7909.
46. MELLO, C., and A. FIRE, 1995 DNA transformation. Methods Cell Biol. 48: 451-482.
47. MILLET, A. C., and J. J. EWBANK, 2004 Immunity in Caenorhabditis elegans. Curr. Opin. Immunol. 16: 4-9.
48. MORRIS, J. Z., H. A. TISSENBAUM and G. RUVKUN, 1996 A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382: 536-539.
49. MUKHOPADHYAY, A., S. W. OH and H. A. TISSENBAUM, 2006 Worming pathways to and from DAF-16/FOXO. Exp. Gerontol. 41: 928-934.
50. MURAKAMI, S., and T. E. JOHNSON, 1996 A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143: 1207-1218.
51. MURPHY, C. T., S. A. MCCARROLL, C. I. BARGMANN, A. FRASER, R. S. KAMATH et al., 2003 Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-283.
52. NELSON, D. W., and R. W. PADGETT, 2003 Insulin worms its way into the spotlight. Genes Dev. 17: 813-818.
53. O'QUINN, A. L., E. M. WIEGAND and J. A. JEDDELOH, 2001 Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell. Microbiol. 3: 381-393.
54. O'ROURKE, D., D. BABAN, M. DEMIDOVA, R. MOTT and J. HODGKIN, 2006 Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res. 16: 1005-1016.
55. PFAFFL, M. W., 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
56. PHELAN, P., 2005 Innexins: members of an evolutionarily conserved family of gap-junction proteins. Biochim. Biophys. Acta 1711: 225-245.
57. RUAL, J. F., J. CERON, J. KORETH, T. HAO, A. S. NICOT et al., 2004 Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14: 2162-2168.
58. RYAN, C. A., A. HUFFAKER and Y. YAMAGUCHI, 2007 New insights into innate immunity in Arabidopsis. Cell Microbiol. 9: 1902-1908.
59. SCHEDL, T., and J. KIMBLE, 1988 fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119: 43-61.
60. SCHULENBURG, H., C. L. KURZ and J. J. EWBANK, 2004 Evolution of the innate immune system: the worm perspective. Immunol. Rev. 198: 36-58.
61. 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.
62. SIFRI, C. D., J. BEGUN, F. M. AUSUBEL and S. B. CALDERWOOD, 2003 Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect. Immun. 71: 2208-2217.
63. SINGH, V., and A. ABALLAY, 2006 Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity. Proc. Natl. Acad. Sci. USA 103: 13092-13097.
64. STARICH, T., M. SHEEHAN, J. JADRICH and J. SHAW, 2001 Innexins in C. elegans. Cell Commun. Adhes. 8: 311-314.
65. STROEHER, V. L., B. P. KENNEDY, K. J. MILLEN, D. F. SCHROEDER, M.G. HAWKINS et al., 1994 DNA-protein interactions in the Caenorhabditis elegans embryo: oocyte and embryonic factors that bind to the promoter of the gut-specific ges-1 gene. Dev. Biol. 163: 367-380.
66. TAN, M. W., S. MAHAJAN-MIKLOS and F. M. AUSUBEL, 1999a Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl. Acad. Sci. USA 96: 715-720.
67. TAN, M. W., L. G. RAHME, J. A. STERNBERG, R. G. TOMPKINS and F. M. AUSUBEL, 1999b Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc. Natl. Acad. Sci. USA 96: 2408-2413.
68. TOSI, M. F., 2005 Innate immune responses to infection. J. Allergy Clin. Immunol. 116: 241-249 quiz 250.
69. TROEMEL, E. R., S. W. CHU, V. REINKE, S. S. LEE, F. M. AUSUBEL et al., 2006 p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2: e183.
70. VAN DEN BERG, M. C., J. Z. WOERLEE, H. MA and R. C. MAY, 2006 Sex-dependent resistance to the pathogenic fungus Cryptococcus neoformans. Genetics 173: 677-683.
71. WESTENDORP, R. G., and T. B. KIRKWOOD, 1998 Human longevity at the cost of reproductive success. Nature 396: 743-746.
72. WHITTEN, S. J., and M. A. MILLER, 2007 The role of gap junctions in Caenorhabditis elegans oocyte maturation and fertilization. Dev. Biol. 301: 432-446.
73. WOLFF, S., H. MA, D. BURCH, G. A. MACIEL, T. HUNTER et al., 2006 SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 124: 1039-1053.
74. WOLKOW, C. A., K. D. KIMURA, M. S. LEE and G. RUVKUN, 2000 Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290: 147-150.
75. YOCHEM, J., T. GU and M. HAN, 1998 A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 149: 1323-1334.