A UPR-independent infection-specific role for a BiP/GRP78 protein in the control of antimicrobial peptide expression in C. elegans epidermis

Virulence

Volumn 3, Issue 3, 2012, Pages 299-308

  Couillault, Carole ^a,b   Fourquet, Patrick ^a,b   Pophillat, Matthieu ^a,b   Ewbank, Jonathan J ^a,b  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b INSERM   (France)

Author keywords

Drechmeria coniospora; Gene regulation; MAPK; Proteomics; Signal transduction

Indexed keywords

GLUCOSE REGULATED PROTEIN 78; POLYPEPTIDE ANTIBIOTIC AGENT;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CORRELATION ANALYSIS; ENDOPLASMIC RETICULUM; EPISTASIS; INNATE IMMUNITY; NONHUMAN; PROTEIN PROCESSING; PROTEOMICS; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UNFOLDED PROTEIN RESPONSE;

CAENORHABDITIS ELEGANS; DRECHMERIA CONIOSPORA; FUNGI;

EID: 84862895021     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.20384     Document Type: Article

References (49)

1. Engelmann I, Pujol N. Innate immunity in C. elegans. Adv Exp Med Biol 2010; 708:105-21; PMID: 21528695; DOI: 10.1007/978-1-4419-8059-5_6.
2. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou JF, Kohara Y, et al. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 2004; 5:488-94; PMID: 15048112; DOI: 10.1038/ni1060.
3. Pujol N, Zugasti O, Wong D, Couillault C, Kurz CL, Schulenburg H, et al. Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 2008; 4:e1000105; PMID: 18636113; DOI: 10.1371/journal.ppat.1000105.
4. Engelmann I, Griffon A, Tichit L, Montañana-Sanchis F, Wang G, Reinke V, et al. A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans. PLoS One 2011; 6:e19055; PMID: 21602919; DOI: 10.1371/journal.pone.0019055.
5. Pujol N, Cypowyj S, Ziegler K, Millet A, Astrain A, Goncharov A, et al. Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr Biol 2008; 18:481-9; PMID: 18394898; DOI: 10.1016/j.cub.2008.02.079.
6. Dierking K, Polanowska J, Omi S, Engelmann I, Gut M, Lembo F, et al. Unusual regulation of a STAT protein by an SLC6 family transporter in C. elegans epidermal innate immunity. Cell Host Microbe 2011; 9:425-35; PMID: 21575913; DOI: 10.1016/j.chom.2011.04.011.
7. Ziegler K, Kurz CL, Cypowyj S, Couillault C, Pophillat M, Pujol N, et al. Antifungal innate immunity in C. elegans: PKCdelta links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 2009; 5:341-52; PMID: 19380113; DOI: 10.1016/j.chom.2009.03.006.
8. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, Inoue H, et al. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002; 297:623-6; PMID: 12142542; DOI: 10.1126/science.1073759.
9. Kurz CL, Shapira M, Chen K, Baillie DL, Tan MW. Caenorhabditis elegans pgp-5 is involved in resistance to bacterial infection and heavy metal and its regulation requires TIR-1 and a p38 map kinase cascade. Biochem Biophys Res Commun 2007; 363:438-43; PMID: 17888400; DOI: 10.1016/j.bbrc.2007.08.190.
10. Liberati NT, Fitzgerald KA, Kim DH, Feinbaum R, Golenbock DT, Ausubel FM. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc Natl Acad Sci U S A 2004; 101:6593-8; PMID: 15123841; DOI: 10.1073/pnas.0308625101.
11. Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, Aroian RV. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A 2004; 101:10995-1000; PMID: 15256590; DOI: 10.1073/pnas.0404073101.
12. Ren M, Feng H, Fu Y, Land M, Rubin CS. Protein kinase D is an essential regulator of C. elegans innate immunity. Immunity 2009; 30:521-32; PMID: 19371715; DOI: 10.1016/j.immuni.2009.03.007.
13. Shivers RP, Pagano DJ, Kooistra T, Richardson CE, Reddy KC, Whitney JK, et al. Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans. PLoS Genet 2010; 6:e1000892; PMID: 20369020; DOI: 10.1371/journal.pgen.1000892.
14. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2006; 2:e183; PMID: 17096597; DOI: 10.1371/journal.pgen.0020183.
15. Partridge FA, Gravato-Nobre MJ, Hodgkin J. Signal transduction pathways that function in both development and innate immunity. Dev Dyn 2010; 239:1330-6; PMID: 20131356.
16. Coleman JJ, Mylonakis E. The tangled web of signaling in innate immunity. Cell Host Microbe 2009; 5:313-5; PMID: 19380109; DOI: 10.1016/j.chom.2009.04.002.
17. Bischof LJ, Kao CY, Los FC, Gonzalez MR, Shen Z, Briggs SP, et al. Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS Pathog 2008; 4:e1000176; PMID: 18846208; DOI: 10.1371/journal.ppat.1000176.
18. Richardson CE, Kooistra T, Kim DH. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 2010; 463:1092-5; PMID: 20182512; DOI: 10.1038/nature08762.
19. Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, et al. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 2001; 107:893-903; PMID: 11779465; DOI: 10.1016/S0092-8674(01)00612-2.
20. Shen X, Ellis RE, Sakaki K, Kaufman RJ. Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet 2005; 1:e37; PMID: 16184190; DOI: 10.1371/journal.pgen.0010037.
21. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002; 415:92-6; PMID: 11780124; DOI: 10.1038/415092a.
22. Ewbank JJ, Pujol N. Cellular homeostasis: coping with ER overload during an immune response. Curr Biol 2010; 20:R452-5; PMID: 20504757; DOI: 10.1016/j.cub.2010.03.023.
23. Bogaerts A, Beets I, Temmerman L, Schoofs L, Verleyen P. Proteome changes of Caenorhabditis elegans upon a Staphylococcus aureus infection. Biol Direct 2010; 5:11; PMID: 20163716; DOI: 10.1186/1745-6150-5-11.
24. Bogaerts A, Temmerman L, Boerjan B, Husson SJ, Schoofs L, Verleyen P. A differential proteomics study of Caenorhabditis elegans infected with Aeromonas hydrophila. Dev Comp Immunol 2010; 34:690-8; PMID: 20149819; DOI: 10.1016/j.dci.2010.02.003.
25. Simonsen KT, Møller-Jensen J, Kristensen AR, Andersen JS, Riddle DL, Kallipolitis BH. Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence 2011; 2:120-30; PMID: 21389771; DOI: 10.4161/viru.2.2.15270.
26. Zugasti O, Ewbank JJ. Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat Immunol 2009; 10:249-56; PMID: 19198592; DOI: 10.1038/ni.1700.
27. Schwarz EM, Antoshechkin I, Bastiani C, Bieri T, Blasiar D, Canaran P, et al. WormBase: better software, richer content. Nucleic Acids Res 2006; 34:D475-8; PMID: 16381915; DOI: 10.1093/nar/gkj061.
28. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 2010; 38:D355-60; PMID: 19880382; DOI: 10.1093/nar/gkp896.
29. Hosack DA, Dennis G, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE. Genome Biol 2003; 4:R70; PMID: 14519205; DOI: 10.1186/gb-2003-4-10-r70.
30. Haskins KA, Russell JF, Gaddis N, Dressman HK, Aballay A. Unfolded protein response genes regulated by CED-1 are required for Caenorhabditis elegans innate immunity. Dev Cell 2008; 15:87-97; PMID: 18606143; DOI: 10.1016/j.devcel.2008.05.006.
31. Sun J, Singh V, Kajino-Sakamoto R, Aballay A. Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 2011; 332:729-32; PMID: 21474712; DOI: 10.1126/science.1203411.
32. Caruso ME, Jenna S, Bouchecareilh M, Baillie DL, Boismenu D, Halawani D, et al. GTPase-mediated regulation of the unfolded protein response in Caenorhabditis elegans is dependent on the AAA+ ATPase CDC-48. Mol Cell Biol 2008; 28:4261-74; PMID: 18458060; DOI: 10.1128/MCB.02252-07.
33. Rohlfing AK, Miteva Y, Hannenhalli S, Lamitina T. Genetic and physiological activation of osmosensitive gene expression mimics transcriptional signatures of pathogen infection in C. elegans. PLoS One 2010; 5:e9010; PMID: 20126308; DOI: 10.1371/journal.pone.0009010.
34. Kapulkin WJ, Hiester BG, Link CD. Compensatory regulation among ER chaperones in C. elegans. FEBS Lett 2005; 579:3063-8; PMID: 15907843; DOI: 10.1016/j.febslet.2005.04.062.
35. TeKippe M, Aballay A. C. elegans germline-deficient mutants respond to pathogen infection using shared and distinct mechanisms. PLoS One 2010; 5:e11777; PMID: 20668681; DOI: 10.1371/journal.pone.0011777.
36. Miyata S, Begun J, Troemel ER, Ausubel FM. DAF-16-dependent suppression of immunity during reproduction in Caenorhabditis elegans. Genetics 2008; 178:903-18; PMID: 18245330; DOI: 10.1534/genetics.107.083923.
37. Henis-Korenblit S, Zhang P, Hansen M, McCormick M, Lee SJ, Cary M, et al. Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc Natl Acad Sci U S A 2010; 107:9730-5; PMID: 20460307; DOI: 10.1073/pnas.1002575107.
38. De Gregorio E, Spellman PT, Rubin GM, Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S A 2001; 98:12590-5; PMID: 11606746; DOI: 10.1073/pnas.221458698.
39. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 2002; 21:2568-79; PMID: 12032070; DOI: 10.1093/emboj/21.11.2568.
40. Lee W, Kim KR, Singaravelu G, Park BJ, Kim DH, Ahnn J, et al. Alternative chaperone machinery may compensate for calreticulin/calnexin deficiency in Caenorhabditis elegans. Proteomics 2006; 6:1329-39; PMID: 16404716; DOI: 10.1002/pmic.200500320.
41. Jeong PY, Na K, Jeong MJ, Chitwood D, Shim YH, Paik YK. Proteomic analysis of Caenorhabditis elegans. Methods Mol Biol 2009; 519:145-69; PMID: 19381582; DOI: 10.1007/978-1-59745-281-6_10.
42. Urano F, Calfon M, Yoneda T, Yun C, Kiraly M, Clark SG, et al. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J Cell Biol 2002; 158:639-46; PMID: 12186849; DOI: 10.1083/jcb.200203086.
43. Osterloh A, Breloer M. Heat shock proteins: linking danger and pathogen recognition. Med Microbiol Immunol 2008; 197:1-8; PMID: 17638015; DOI: 10.1007/s00430-007-0055-0.
44. Kadota Y, Shirasu K, Guerois R. NLR sensors meet at the SGT1-HSP90 crossroad. Trends Biochem Sci 2010; 35:199-207; PMID: 20096590; DOI: 10.1016/j.tibs.2009.12.005.
45. Stiernagle T. Maintenance of C. elegans. WormBook. http://www.wormbook.org: The C. elegans Research Community ed, 2006:1551-8507.
46. Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, Kohara Y, et al. Inducible antibacterial defense system in C. elegans. Curr Biol 2002; 12:1209-14; PMID: 12176330; DOI: 10.1016/S0960-9822(02)00928-4.
47. Timmons L, Court DL, Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001; 263:103-12; PMID: 11223248; DOI: 10.1016/S0378-1119(00)00579-5.
48. Lee KZ, Kniazeva M, Han M, Pujol N, Ewbank JJ. The fatty acid synthase fasn-1 acts upstream of WNK and Ste20/GCK-VI kinases to modulate antimicrobial peptide expression in C. elegans epidermis. Virulence 2010; 1:113-22; PMID: 21178429; DOI: 10.4161/viru.1.3.10974.
49. Labed SA, Omi S, Gut M, Ewbank JJ, Pujol N. The Pseudokinase NIPI-4 Is a Novel Regulator of Antimicrobial Peptide Gene Expression. PLoS One 2012; 7:e33887; PMID: 22470487; DOI: 10.1371/journal.pone.0033887.