Genetic screen reveals link between the maternal effect sterile gene mes-1 and pseudomonas aeruginosa-induced neurodegeneration in caenorhabditis elegans

Journal of Biological Chemistry

Volumn 290, Issue 49, 2015, Pages 29231-29239

  Wu, Qiuli ^a,b   Cao, Xiou ^a   Yan, Dong ^a   Wang, Dayong ^b   Aballay, Alejandro ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANIMALS; BACTERIA; CELL PROLIFERATION; GENES; TRANSCRIPTION;

CAENORHABDITIS ELEGANS; GENETIC SCREENS; IMMUNE RESPONSE; MATERNAL EFFECTS; MICROBIAL INFECTIONS; NEURODEGENERATION; PSEUDOMONAS AERUGINOSA; RECEPTOR TYROSINE KINASE;

NEURODEGENERATIVE DISEASES;

TRANSCRIPTION FACTOR DAF 16; CAENORHABDITIS ELEGANS PROTEIN; GREEN FLUORESCENT PROTEIN; MES-1 PROTEIN, C ELEGANS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAENORHABDITIS ELEGANS; CELL SURVIVAL; CONTROLLED STUDY; GENE; GENE MUTATION; GERM LINE; MES 1 GENE; NERVE DEGENERATION; NONHUMAN; OSMOTIC STRESS; PGL 1 GENE; PRIORITY JOURNAL; PSEUDOMONAS INFECTION; SENSORY NERVE CELL; ANIMAL; CHEMOTAXIS; DEGENERATIVE DISEASE; DISEASE MODEL; GENETICS; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MUTATION; OSMOTIC PRESSURE; PHENOTYPE; PSEUDOMONAS AERUGINOSA; RNA INTERFERENCE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHEMOTAXIS; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; MUTATION; NEURODEGENERATIVE DISEASES; OSMOTIC PRESSURE; PHENOTYPE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RNA INTERFERENCE;

EID: 84946084426     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.674259     Document Type: Article

References (46)

1. Heneka, M. T., Carson, M. J., El Khoury, J., Landreth, G. E., Brosseron, F., Feinstein, D. L., Jacobs, A. H., Wyss-Coray, T., Vitorica, J., Ransohoff, R. M., Herrup, K., Frautschy, S. A., Finsen, B., Brown, G. C., Verkhratsky, A., Yamanaka, K., Koistinaho, J., Latz, E., Halle, A., Petzold, G. C., Town, T., Morgan, D., Shinohara, M. L., Perry, V. H., Holmes, C., Bazan, N. G., Brooks, D. J., Hunot, S., Joseph, B., Deigendesch, N., Garaschuk, O., Boddeke, E., Dinarello, C. A., Breitner, J. C., Cole, G. M., Golenbock, D. T., and Kummer, M. P. (2015) Neuroinflammation in Alzheimer's disease. Lancet Neurol. 14, 388-405
2. Heneka, M. T., Golenbock, D. T., and Latz, E. (2015) Innate immunity in Alzheimer's disease. Nat. Immunol. 16, 229-236
3. Amor, S., Puentes, F., Baker, D., and van der Valk, P. (2010) Inflammation in neurodegenerative diseases. Immunology 129, 154-169
4. Hobert, O. (2010) Neurogenesis in the nematode Caenorhabditis elegans. WormBook 10.1895/wormbook.1.12.2
5. White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314, 1-340
6. Pan, C. L., Peng, C. Y., Chen, C. H., and McIntire, S. (2011) Genetic analysis of age-dependent defects of the Caenorhabditis elegans touch receptor neurons. Proc. Natl. Acad. Sci. U.S.A. 108, 9274-9279
7. Chew, Y. L., Fan, X., Gtz, J., and Nicholas, H. R. (2013) Aging in the nervous system of Caenorhabditis elegans. Commun. Integr. Biol. 6, e25288
8. Peng, C. Y., Chen, C. H., Hsu, J. M., and Pan, C. L. (2011) C. Elegans model of neuronal aging. Commun. Integr. Biol. 4, 696-698
9. Toth, M. L., Melentijevic, I., Shah, L., Bhatia, A., Lu, K., Talwar, A., Naji, H., Ibanez-Ventoso, C., Ghose, P., Jevince, A., Xue, J., Herndon, L. A., Bhanot, G., Rongo, C., Hall, D. H., and Driscoll, M. (2012) Neurite sprouting and synapse deterioration in the aging Caenorhabditis elegans nervous system. J. Neurosci. 32, 8778-8790
10. Du, M., and Wang, D. (2009) The neurotoxic effects of heavy metal exposure on GABAergic nervous system in nematode Caenorhabditis elegans. Environ. Toxicol. Pharmacol. 27, 314-320
11. Mocko, J. B., Kern, A., Moosmann, B., Behl, C., and Hajieva, P. (2010) Phenothiazines interfere with dopaminergic neurodegeneration in Caenorhabditis elegans models of Parkinson's disease. Neurobiol. Dis. 40, 120-129
12. Negga, R., Stuart, J. A., Machen, M. L., Salva, J., Lizek, A. J., Richardson, S. J., Osborne, A. S., Mirallas, O., McVey, K. A., and Fitsanakis, V. A. (2012) Exposure to glyphosate-and/or Mn/Zn-ethylene-bis-dithiocarbamatecontaining pesticides leads to degeneration ofβ-aminobutyric acid and dopamine neurons in Caenorhabditis elegans. Neurotox. Res. 21, 281-290
13. Vanduyn, N., Settivari, R., Wong, G., and Nass, R. (2010) SKN-1/Nrf2 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of methylmercury toxicity. Toxicol. Sci. 118, 613-624
14. Benedetto, A., Au, C., Avila, D. S., Milatovic, D., and Aschner, M. (2010) Extracellular dopamine potentiates Mn-induced oxidative stress, lifespan reduction, and dopaminergic neurodegeneration in a BLI-3-dependent manner in Caenorhabditis elegans. PLoS Genet. 10.1371/journal.pgen.1001084
15. VanDuyn, N., Settivari, R., LeVora, J., Zhou, S., Unrine, J., and Nass, R. (2013) The metal transporter SMF-3/DMT-1 mediates aluminum-induced dopamine neuron degeneration. J. Neurochem. 124, 147-157
16. Harrison Brody, A., Chou, E., Gray, J. M., Pokyrwka, N. J., and Raley-Susman, K. M. (2013) Mancozeb-induced behavioral deficits precede structural neural degeneration. Neurotoxicology 34, 74-81
17. Chen, P., Martinez-Finley, E. J., Bornhorst, J., Chakraborty, S., and Aschner, M. (2013) Metal-induced neurodegeneration in C. Elegans. Front. Aging Neurosci. 5, 18
18. Sun, J., Singh, V., Kajino-Sakamoto, R., and Aballay, A. (2011) Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 332, 729-732
19. Sun, J., Liu, Y., and Aballay, A. (2012) Organismal regulation of XBP-1-mediated unfolded protein response during development and immune activation. EMBO Rep. 13, 855-860
20. Singh, V., and Aballay, A. (2012) Endoplasmic reticulum stress pathway required for immune homeostasis is neurally controlled by arrestin-1. J. Biol. Chem. 287, 33191-33197
21. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
22. Jorgensen, E. M., and Mango, S. E. (2002) The art and design of genetic screens: Caenorhabditis elegans. Nat. Rev. Genet. 3, 356-369
23. Bargmann, C. I., and Horvitz, H. R. (1991) Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. Elegans. Neuron 7, 729-742
24. Saeki, S., Yamamoto, M., and Iino, Y. (2001) Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J. Exp. Biol. 204, 1757-1764
25. O'Meara, M. M., Bigelow, H., Flibotte, S., Etchberger, J. F., Moerman, D. G., and Hobert, O. (2009) Cis-regulatory mutations in the Caenorhabditis elegans homeobox gene locus cog-1 affect neuronal development. Genetics 181, 1679-1686
26. Zheng, G., Cochella, L., Liu, J., Hobert, O., and Li, W. H. (2011) Temporal and spatial regulation of microRNA activity with photoactivatable cantimirs. ACS Chem. Biol. 6, 1332-1338
27. Doerks, T., Copley, R. R., Schultz, J., Ponting, C. P., and Bork, P. (2002) Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 12, 47-56
28. Chen, L., Fu, Y., Ren, M., Xiao, B., and Rubin, C. S. (2011) A RasGRP, C. Elegans RGEF-1b, couples external stimuli to behavior by activating LET-60 (Ras) in sensory neurons. Neuron 70, 51-65
29. Bargmann, C. I. (2006) Chemosensation in C. Elegans. WormBook 10.1895/wormbook.1.123.1
30. Styer, K. L., Singh, V., Macosko, E., Steele, S. E., Bargmann, C. I., and Aballay, A. (2008) Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 322, 460-464
31. Meisel, J. D., Panda, O., Mahanti, P., Schroeder, F. C., and Kim, D. H. (2014) Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. Elegans. Cell 159, 267-280
32. Shivers, R. P., Youngman, M. J., and Kim, D. H. (2008) Transcriptional responses to pathogens in Caenorhabditis elegans. Curr. Opin. Microbiol. 11, 251-256
33. Pepper, A. S. R., Killian, D. J., and Hubbard, E. J. A. (2003) Genetic analysis of Caenorhabditis elegans glp-1 mutants suggests receptor interaction or competition. Genetics 163, 115-132
34. Beanan, M. J., and Strome, S. (1992) Characterization of a germ-line proliferation mutation in C. Elegans. Development 116, 755-766
35. TeKippe, M., and Aballay, A. (2010) C. Elegans germline-deficient mutants respond to pathogen infection using shared and distinct mechanisms. PloS One 5, e11777
36. Sinha, A., and Rae, R. (2014) A functional genomic screen for evolutionarily conserved genes required for lifespan and immunity in germlinedeficient C. Elegans. PLoS One 9, e101970
37. Alper, S., McElwee, M. K., Apfeld, J., Lackford, B., Freedman, J. H., and Schwartz, D. A. (2010) The Caenorhabditis elegans germ line regulates distinct signaling pathways to control lifespan and innate immunity. J. Biol. Chem. 285, 1822-1828
38. Berkowitz, L. A., and Strome, S. (2000) MES-1, a protein required for unequal divisions of the germline in early C. Elegans embryos, resembles receptor tyrosine kinases and is localized to the boundary between the germline and gut cells. Development 127, 4419-4431
39. Arantes-Oliveira, N., Apfeld, J., Dillin, A., and Kenyon, C. (2002) Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295, 502-505
40. Lin, K., Dorman, J. B., Rodan, A., and Kenyon, C. (1997) daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319-1322
41. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A., and Ruvkun, G. (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. Elegans. Nature 389, 994-999
42. Chávez, V., Mohri-Shiomi, A., Maadani, A., Vega, L. A., and Garsin, D. A. (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
43. Singh, V., and Aballay, A. (2006) Heat shock and genetic activation of HSF-1 enhance immunity to bacteria. Cell Cycle 5, 2443-2446
44. Singh, V., and Aballay, A. (2009) Regulation of DAF-16-mediated innate immunity in C. Elegans. J. Biol. Chem. 284, 35580-35587
45. Berman, J. R., and Kenyon, C. (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
46. TeKippe, M., and Aballay, A. (2010) C. Elegans germ line-deficient mutants respond to pathogen infection using shared and distinct mechanisms. PLoS One 5, e11777