Insights from the worm: The C. elegans model for innate immunity

Barriere, 2007, Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations, Genetics, 176, 999, 10.1534/genetics.106.067223 Brenner, 1974, The genetics of Caenorhabditis elegans, Genetics, 77, 71, 10.1093/genetics/77.1.71 Aliyari, 2009, RNA-based viral immunity initiated by the Dicer family of host immune receptors, Immunol Rev, 227, 176, 10.1111/j.1600-065X.2008.00722.x Wilkins, 2005, RNA interference is an antiviral defence mechanism in Caenorhabditis elegans, Nature, 436, 1044, 10.1038/nature03957 Lu, 2005, Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans, Nature, 436, 1040, 10.1038/nature03870 Felix, 2011, Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses, PLoS Biol, 9, e1000586, 10.1371/journal.pbio.1000586 Guo, 2013, Homologous RIG-I-like helicase proteins direct RNAi-mediated antiviral immunity in C. elegans by distinct mechanisms, Proc Natl Acad Sci U S A, 110, 16085, 10.1073/pnas.1307453110 Ashe, 2013, A deletion polymorphism in the Caenorhabditis elegans RIG-I homolog disables viral RNA dicing and antiviral immunity, Elife, 2, e00994, 10.7554/eLife.00994 Tabara, 2002, The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans, Cell, 109, 861, 10.1016/S0092-8674(02)00793-6 Tijsterman, 2002, RNA helicase MUT-14-dependent gene silencing triggered in C. elegans by short antisense RNAs, Science, 295, 694, 10.1126/science.1067534 Makarova, 2011, Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems, Biol Direct, 6, 38, 10.1186/1745-6150-6-38 Sijen, 2003, Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi, Nature, 426, 310, 10.1038/nature02107 Horst, 2011, Viral evasion of T cell immunity: ancient mechanisms offering new applications, Curr Opin Immunol, 23, 96, 10.1016/j.coi.2010.11.005 Guo, 2013, Characterization of virus-encoded RNA interference suppressors in Caenorhabditis elegans, J Virol, 87, 5414, 10.1128/JVI.00148-13 Loo, 2011, Immune signaling by RIG-I-like receptors, Immunity, 34, 680, 10.1016/j.immuni.2011.05.003 Garsin, 2001, A simple model host for identifying Gram-positive virulence factors, Proc Natl Acad Sci U S A, 98, 10892, 10.1073/pnas.191378698 Sifri, 2003, Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis, Infect Immun, 71, 2208, 10.1128/IAI.71.4.2208-2217.2003 Tan, 1999, Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis, Proc Natl Acad Sci U S A, 96, 715, 10.1073/pnas.96.2.715 Aballay, 2000, Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans, Curr Biol, 10, 1539, 10.1016/S0960-9822(00)00830-7 Kurz, 2003, Caenorhabditis elegans: an emerging genetic model for the study of innate immunity, Nat Rev Genet, 4, 380, 10.1038/nrg1067 Mahajan-Miklos, 1999, Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model, Cell, 96, 47, 10.1016/S0092-8674(00)80958-7 Kurz, 2003, Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening, EMBO J, 22, 1451, 10.1093/emboj/cdg159 Aballay, 2001, Programmed cell death mediated by ced-3 and ced-4 protects Caenorhabditis elegans from Salmonella typhimurium-mediated killing, Proc Natl Acad Sci U S A, 98, 2735, 10.1073/pnas.041613098 Hodgkin, 2000, A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans, Curr Biol, 10, 1615, 10.1016/S0960-9822(00)00867-8 Nicholas, 2004, Responses to infection and possible recognition strategies in the innate immune system of Caenorhabditis elegans, Mol Immunol, 41, 479, 10.1016/j.molimm.2004.03.037 Tan, 2004, A movable surface: formation of Yersinia sp. biofilms on motile Caenorhabditis elegans, J Bacteriol, 186, 5087, 10.1128/JB.186.15.5087-5092.2004 Darby, 2002, Caenorhabditis elegans: plague bacteria biofilm blocks food intake, Nature, 417, 243, 10.1038/417243a Pujol, 2001, A reverse genetic analysis of components of the toll signaling pathway in Caenorhabditis elegans, Curr Biol, 11, 809, 10.1016/S0960-9822(01)00241-X Liberati, 2004, Requirement for a conserved toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response, Proc Natl Acad Sci U S A, 101, 6593, 10.1073/pnas.0308625101 Couillault, 2004, TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM, Nat Immunol, 5, 488, 10.1038/ni1060 Shivers, 2009, Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans, Cell Host Microbe, 6, 321, 10.1016/j.chom.2009.09.001 Kim, 2002, A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity, Science, 297, 623, 10.1126/science.1073759 Kim, 2004, Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase, Proc Natl Acad Sci U S A, 101, 10990, 10.1073/pnas.0403546101 O’Rourke, 2006, Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum, Genome Res, 16, 1005, 10.1101/gr.50823006 Troemel, 2006, p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans, PLoS Genet, 2, e183, 10.1371/journal.pgen.0020183 Wong, 2007, Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection, Genome Biol, 8, R194, 10.1186/gb-2007-8-9-r194 Schulenburg, 2008, Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans, Immunobiology, 213, 237, 10.1016/j.imbio.2007.12.004 Bork, 1993, The CUB domain. A widespread module in developmentally regulated proteins, J Mol Biol, 231, 539, 10.1006/jmbi.1993.1305 Thomas, 2006, Concerted evolution of two novel protein families in Caenorhabditis species, Genetics, 172, 2269, 10.1534/genetics.105.052746 Shivers, 2010, Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans, PLoS Genet, 6, e1000892, 10.1371/journal.pgen.1000892 Aballay, 2003, Caenorhabditis elegans innate immune response triggered by Salmonella enterica requires intact LPS and is mediated by a MAPK signaling pathway, Curr Biol, 13, 47, 10.1016/S0960-9822(02)01396-9 Nicholas, 2004, The ERK MAP kinase cascade mediates tail swelling and a protective response to rectal infection in C. elegans, Curr Biol, 14, 1256, 10.1016/j.cub.2004.07.022 Mallo, 2002, Inducible antibacterial defense system in C. elegans, Curr Biol, 12, 1209, 10.1016/S0960-9822(02)00928-4 Garsin, 2003, Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens, Science, 300, 1921, 10.1126/science.1080147 Hsin, 1999, Signals from the reproductive system regulate the lifespan of C. elegans, Nature, 399, 362, 10.1038/20694 Libina, 2003, Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan, Cell, 115, 489, 10.1016/S0092-8674(03)00889-4 Lin, 2001, Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling, Nat Genet, 28, 139, 10.1038/88850 Evans, 2008, Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans, PLoS Pathog, 4, e1000175, 10.1371/journal.ppat.1000175 Murphy, 2003, Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans, Nature, 424, 277, 10.1038/nature01789 McElwee, 2003, Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16, Aging Cell, 2, 111, 10.1046/j.1474-9728.2003.00043.x Inoue, 2005, The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response, Genes Dev, 19, 2278, 10.1101/gad.1324805 Tullet, 2008, Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans, Cell, 132, 1025, 10.1016/j.cell.2008.01.030 Evans, 2008, The DAF-2 insulin-like signaling pathway independently regulates aging and immunity in C. elegans, Aging Cell, 7, 879, 10.1111/j.1474-9726.2008.00435.x Lakowski, 1996, Determination of life-span in Caenorhabditis elegans by four clock genes, Science, 272, 1010, 10.1126/science.272.5264.1010 Lakowski, 1998, The genetics of caloric restriction in Caenorhabditis elegans, Proc Natl Acad Sci U S A, 95, 13091, 10.1073/pnas.95.22.13091 Laws, 2004, Age influences resistance of Caenorhabditis elegans to killing by pathogenic bacteria, FEMS Microbiol Lett, 234, 281, 10.1111/j.1574-6968.2004.tb09545.x Garigan, 2002, Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation, Genetics, 161, 1101, 10.1093/genetics/161.3.1101 Gems, 2000, Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans, Genetics, 154, 1597, 10.1093/genetics/154.4.1597 Youngman, 2011, A decline in p38 MAPK signaling underlies immunosenescence in Caenorhabditis elegans, PLoS Genet, 7, e1002082, 10.1371/journal.pgen.1002082 Chávez, 2007, Oxidative stress enzymes are required for DAF-16-mediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans, Genetics, 176, 1567, 10.1534/genetics.107.072587 Hoeven, 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, 10.1371/journal.ppat.1002453 Singh, 2006, Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity, Proc Natl Acad Sci U S A, 103, 13092, 10.1073/pnas.0604050103 Richardson, 2010, An essential role for XBP-1 in host protection against immune activation in C. elegans, Nature, 463, 1092, 10.1038/nature08762 Haskins, 2008, Unfolded protein response genes regulated by CED-1 are required for Caenorhabditis elegans innate immunity, Dev Cell, 15, 87, 10.1016/j.devcel.2008.05.006 Reddy, 2009, A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans, Science, 323, 382, 10.1126/science.1166527 Styer, 2008, Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR, Science, 322, 460, 10.1126/science.1163673 Sun, 2011, Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes, Science, 332, 729, 10.1126/science.1203411 Aballay, 2013, Role of the nervous system in the control of proteostasis during innate immune activation: insights from C. elegans, PLoS Pathog, 9, e1003433, 10.1371/journal.ppat.1003433 Ermolaeva, 2013, DNA damage in germ cells induces an innate immune response that triggers systemic stress resistance, Nature, 501, 416, 10.1038/nature12452 Ermolaeva, 2014, Systemic DNA damage responses: organismal adaptations to genome instability, Trends Genet, 30, 95, 10.1016/j.tig.2013.12.001 Ermolaeva, 2013, The innate immune system as mediator of systemic DNA damage responses, Commun Integr Biol, 6, e26926, 10.4161/cib.26926 Karpac, 2011, Dynamic coordination of innate immune signaling and insulin signaling regulates systemic responses to localized DNA damage, Dev Cell, 20, 841, 10.1016/j.devcel.2011.05.011 Garinis, 2009, Persistent transcription-blocking DNA lesions trigger somatic growth attenuation associated with longevity, Nat Cell Biol, 11, 604, 10.1038/ncb1866 Schumacher, 2008, Delayed and accelerated aging share common longevity assurance mechanisms, PLoS Genet, 4, e1000161, 10.1371/journal.pgen.1000161