Comparative genomics RNAi screen identifies eftud2 as a novel regulator of innate immunity

Genetics

Volumn 197, Issue 2, 2014, Pages 485-496

  De Arras, Lesly ^a,b   Laws, Rebecca ^c   Leach, Sonia M ^b   Pontis, Kyle ^a,b   Freedman, Jonathan H ^d   Schwartz, David A ^b,e   Alper, Scott ^a,b  

^a Integrated Department of Immunology   (United States)

^b DEPARTMENT OF MEDICINE   (United States)

^c BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EFTUD2 PROTEIN; ELONGATION FACTOR TU; MYELOID DIFFERENTIATION FACTOR 88; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; ELONGATION FACTOR; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ANIMAL GENETICS; ARTHRITIS; ARTICLE; ATHEROSCLEROSIS; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; INFECTION; INFLAMMATORY DISEASE; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA INTERFERENCE; RNA SPLICING; ALTERNATIVE RNA SPLICING; ANIMAL; CELL LINE; COMPARATIVE GENOMIC HYBRIDIZATION; CYTOLOGY; GENETICS; IMMUNOLOGY; MOUSE;

ALTERNATIVE SPLICING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; COMPARATIVE GENOMIC HYBRIDIZATION; IMMUNITY, INNATE; MACROPHAGES; MICE; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDE ELONGATION FACTORS; RIBONUCLEOPROTEIN, U5 SMALL NUCLEAR; RNA INTERFERENCE;

EID: 84902504057     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.160499     Document Type: Article

References (99)

1. Adib-Conquy, M., C. Adrie, C. Fitting, O. Gattolliat, R. Beyaert et al., 2006 Up-regulation of MyD88s and SIGIRR, molecules inhibiting Toll-like receptor signaling, in monocytes from septic patients. Crit. Care Med. 34: 2377-2385.
2. Alper, S., S. J. McBride, B. Lackford, J. H. Freedman, and D. A. Schwartz, 2007 Specificity and complexity of the C. elegans innate immune response. Mol. Cell. Biol. 27: 5544-5553.
3. Alper, S., R. Laws, B. Lackford, W. A. Boyd, P. Dunlap et al., 2008 Identification of innate immunity genes and pathways using a comparative genomics approach. Proc. Natl. Acad. Sci. USA 105: 7016-7021.
4. Alper, S., M. McElwee, J. Apfeld, B. Lackford, J. Freedman et al., 2010 Germline proliferation regulates distinct signaling pathways in C. elegans to control lifespan and innate immunity. J. Biol. Chem. 285: 1822-1828.
5. An, M., and P. D. Henion, 2012 The zebrafish sf3b1b460 mutant reveals differential requirements for the sf3b1 pre-mRNA processing gene during neural crest development. Int. J. Dev. Biol. 56: 223-237.
6. Arcaroli, J., M. B. Fessler, and E. Abraham, 2005 Genetic polymorphisms and sepsis. Shock 24: 300-312.
7. Baccam, M., S. Y. Woo, C. Vinson, and G. A. Bishop, 2003 CD40mediated transcriptional regulation of the IL-6 gene in B lymphocytes: involvement of NF-kappa B, AP-1, and C/EBP. J. Immunol. 170: 3099-3108.
8. Bartels, C., C. Klatt, R. Luhrmann, and P. Fabrizio, 2002 The ribosomal translocase homologue Snu114p is involved in unwinding U4/U6 RNA during activation of the spliceosome. EMBO Rep. 3: 875-880.
9. Bartels, C., H. Urlaub, R. Luhrmann, and P. Fabrizio, 2003 Mutagenesis suggests several roles of Snu114p in premRNA splicing. J. Biol. Chem. 278: 28324-28334.
10. Bidani, A., and T. A. Heming, 1995 Effects of bafilomycin A1 on functional capabilities of LPS-activated alveolar macrophages. J. Leukoc. Biol. 57: 275-281.
11. Bolz, D. D., J. L. Tenor, and A. Aballay, 2010 A conserved PMK-1/p38 MAPK is required in C. elegans tissue-specific immune response to Y. pestis infection. J. Biol. Chem. 285: 10832-10840.
12. Brenner, T. J., and C. Guthrie, 2006 Assembly of Snu114 into U5 snRNP requires Prp8 and a functional GTPase domain. RNA 12: 862-871.
13. Burns, K., S. Janssens, B. Brissoni, N. Olivos, R. Beyaert et al., 2003 Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J. Exp. Med. 197: 263-268.
14. Calzado, M. A., S. Bacher, and M. L. Schmitz, 2007 NF-kappaB inhibitors for the treatment of inflammatory diseases and cancer. Curr. Med. Chem. 14: 367-376.
15. Chang, J. T., and J. R. Nevins, 2006 GATHER: a systems approach to interpreting genomic signatures. Bioinformatics 22: 2926-2933.
16. Collins, L. J., C. G. Kurland, P. Biggs, and D. Penny, 2009 The modern RNP world of eukaryotes. J. Hered. 100: 597-604.
17. Conboy, I. M., D. Manoli, V. Mhaiskar, and P. P. Jones, 1999 Calcineurin and vacuolar-type H+-ATPase modulate macrophage effector functions. Proc. Natl. Acad. Sci. USA 96: 6324-6329.
18. Connolly, D. J., and L. A. O'Neill, 2012 New developments in Tolllike receptor targeted therapeutics. Curr. Opin. Pharmacol. 12: 510-518.
19. Cook, D. N., D. S. Pisetsky, and D. A. Schwartz, 2004 Toll-like receptors in the pathogenesis of human disease. Nat. Immunol. 5: 975-979.
20. Corrionero, A., B. Minana, and J. Valcarcel, 2011 Reduced fidelity of branch point recognition and alternative splicing induced by the anti-tumor drug spliceostatin A. Genes Dev. 25: 445-459.
21. Couillault, C., N. Pujol, J. Reboul, L. Sabatier, J. F. Guichou et al., 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: 488-494.
22. Coux, O., K. Tanaka, and A. L. Goldberg, 1996 Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65: 801-847.
23. De Arras, L., and S. Alper, 2013 The Sf3a mRNA splicing complex mediates a MyD88-dependent negative feedback loop that limits the innate immune response. PLoS Genet. 9: e1003855.
24. De Arras, L., I. V. Yang, B. Lackford, D. W. Riches, R. Prekeris et al., 2012 Spatiotemporal Inhibition of Innate Immunity Signaling by the Tbc1d23 RAB-GAP. J. Immunol. 188: 2905-2913.
25. De Arras, L., A. Seng, B. Lackford, M. Keikhaee, B. Bowerman et al., 2013 An evolutionarily conserved innate immunity protein interaction network. J. Biol. Chem. 288: 1967-1978.
26. Dillin, A., D. K. Crawford, and C. Kenyon, 2002 Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298: 830-834.
27. Drory, O., F. Frolow, and N. Nelson, 2004 Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 5: 1148-1152.
28. Elliott, P. J., T. M. Zollner, and W. H. Boehncke, 2003 Proteasome inhibition: a new anti-inflammatory strategy. J. Mol. Med. 81: 235-245.
29. Engelmann, I., and N. Pujol, 2010 Innate immunity in C. elegans. Adv. Exp. Med. Biol. 708: 105-121.
30. Ewbank, J. J., 2006 Signaling in the immune response (January 23, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.83.1, http://www.wormbook.org.
31. Ewbank, J. J., and O. Zugasti, 2011 C. elegans: model host and tool for antimicrobial drug discovery. Dis. Model. Mech. 4: 300-304.
32. Fabrizio, P., B. Laggerbauer, J. Lauber, W. S. Lane, and R. Luhrmann, 1997 An evolutionarily conserved U5 snRNP-specific protein is a GTP-binding factor closely related to the ribosomal translocase EF-2. EMBO J. 16: 4092-4106.
33. Fan, L., C. Lagisetti, C. C. Edwards, T. R. Webb, and P. M. Potter, 2011 Sudemycins, novel small molecule analogues of FR901464, induce alternative gene splicing. ACS Chem. Biol. 6: 582-589.
34. Fernandez-Botran, R., and V. Větvička, 2001 Methods in Cellular Immunology, CRC Press, Boca Raton.
35. Foley, E., and P. H. O'Farrell, 2004 Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol. 2: E203.
36. Forgac, M., 1999 Structure and properties of the vacuolar (H+)-ATPases. J. Biol. Chem. 274: 12951-12954.
37. 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.
38. Goh, F. G., and K. S. Midwood, 2012 Intrinsic danger: activation of Toll-like receptors in rheumatoid arthritis. Rheumatology (Oxford) 51: 7-23.
39. Gordon, C. T., F. Petit, M. Oufadem, C. Decaestecker, A. S. Jourdain et al., 2012 EFTUD2 haploinsufficiency leads to syndromic oesophageal atresia. J. Med. Genet. 49: 737-746.
40. Ho, M. N., K. J. Hill, M. A. Lindorfer, and T. H. Stevens, 1993 Isolation of vacuolar membrane H(+)-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H(+)-ATPase. J. Biol. Chem. 268: 221-227.
41. Huffman, D. L., L. Abrami, R. Sasik, J. Corbeil, F. G. van der Goot et al., 2004 Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc. Natl. Acad. Sci. USA 101: 10995-11000.
42. Irazoqui, J., and F. Ausubel, 2010 99th Dahlem Conference on infection, inflammation, and chronic inflammatory disorders: Caenorhabditis elegans as a model to study tissues involved in host immunity and microbial pathogenesis. Clin. Exp. Immunol. 160: 48-57.
43. Iwasaki, A., and R. Medzhitov, 2010 Regulation of adaptive immunity by the innate immune system. Science 327: 291-295.
44. Janssens, S., K. Burns, J. Tschopp, and R. Beyaert, 2002 Regulation of interleukin-1-and lipopolysaccharide-in-duced NF-kappaB activation by alternative splicing of MyD88. Curr. Biol. 12: 467-471.
45. Janssens, S., K. Burns, E. Vercammen, J. Tschopp, and R. Beyaert, 2003 MyD88S, a splice variant of MyD88, differentially modulates NF-kappaB-and AP-1-dependent gene expression. FEBS Lett. 548: 103-107.
46. Kamath, R. S., and J. Ahringer, 2003 Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
47. 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.
48. Karin, M., and F. R. Greten, 2005 NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5: 749-759.
49. Kaufmann, S. H. E., R. Medzhitov, S. Gordon, 2004 The Innate Immune Response to Infection. ASM Press, Washington D.C.
50. Kawai, T., and S. Akira, 2010 The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
51. Kennedy, S., D. Wang, and G. Ruvkun, 2004 A conserved siRNAdegrading RNase negatively regulates RNA interference in C. elegans. Nature 427: 645-649.
52. 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.
53. Kramer, A., 1996 The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65: 367-409.
54. Kramer, A., F. Ferfoglia, C. J. Huang, F. Mulhaupt, D. Nesic et al., 2005 Structure-function analysis of the U2 snRNP-associated splicing factor SF3a. Biochem. Soc. Trans. 33: 439-442.
55. Lee, H. K., and A. Iwasaki, 2007 Innate control of adaptive immunity: dendritic cells and beyond. Semin. Immunol. 19: 48-55.
56. Liberati, N. T., K. A. Fitzgerald, D. H. Kim, R. Feinbaum, D. T. Golenbock et al., 2004 Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. USA 101: 6593-6598.
57. Lines, M. A., L. Huang, J. Schwartzentruber, S. L. Douglas, D. C. Lynch et al., 2012 Haploinsufficiency of a spliceosomal GTPase encoded by EFTUD2 causes mandibulofacial dysostosis with microcephaly. Am. J. Hum. Genet. 90: 369-377.
58. Luquetti, D. V., A. V. Hing, M. J. Rieder, D. A. Nickerson, E. H. Turner et al., 2013 "Mandibulofacial dysostosis with microcephaly" caused by EFTUD2 mutations: expanding the phenotype. Am. J. Med. Genet. A. 161A: 108-113.
59. 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.
60. 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.
61. Martinon, F., X. Chen, A. H. Lee, and L. H. Glimcher, 2010 TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11: 411-418.
62. Meissner, B., A. Warner, K. Wong, N. Dube, A. Lorch et al., 2009 An integrated strategy to study muscle development and myofilament structure in Caenorhabditis elegans. PLoS Genet. 5: e1000537.
63. Mendoza-Barbera, E., M. A. Corral-Rodriguez, A. Soares-Schanoski, M. Velarde, S. Macieira et al., 2009 Contribution of globular death domains and unstructured linkers to MyD88.IRAK-4 heterodimer formation: an explanation for the antagonistic activity of MyD88s. Biochem. Biophys. Res. Commun. 380: 183-187.
64. Mi, H., Q. Dong, A. Muruganujan, P. Gaudet, S. Lewis et al., 2010 PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res. 38: D204-D210.
65. Mitchell, D. H., J. W. Stiles, J. Santelli, and D. R. Sanadi, 1979 Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J. Gerontol. 34: 28-36.
66. Mochii, M., S. Yoshida, K. Morita, Y. Kohara, and N. Ueno, 1999 Identification of transforming growth factor-betaregulated genes in Caenorhabditis elegans by differential hybridization of arrayed cDNAs. Proc. Natl. Acad. Sci. USA 96: 15020-15025.
67. Muhammed, M., B. B. Fuchs, M. P. Wu, J. Breger, J. J. Coleman et al., 2012 The role of mycelium production and a MAPKmediated immune response in the C. elegans-Fusarium model system. Med. Mycol. 50: 488-496.
68. Mullick, A. E., P. S. Tobias, and L. K. Curtiss, 2005 Modulation of atherosclerosis in mice by Toll-like receptor 2. J. Clin. Invest. 115: 3149-3156.
69. 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.
70. Newman, A. J., 1997 The role of U5 snRNP in pre-mRNA splicing. EMBO J. 16: 5797-5800.
71. Nishi, T., and M. Forgac, 2002 The vacuolar (H+)-ATPasesnature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3: 94-103.
72. 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.
73. Picard, C., J. L. Casanova, and A. Puel, 2011 Infectious diseases in patients with IRAK-4, MyD88, NEMO, or IkappaBalpha deficiency. Clin. Microbiol. Rev. 24: 490-497.
74. Powell, J. R., and F. M. Ausubel, 2008 Models of Caenorhabditis elegans infection by bacterial and fungal pathogens. Methods Mol. Biol. 415: 403-427.
75. Pujol, N., E. M. Link, L. X. Liu, C. L. Kurz, G. Alloing et al., 2001 A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr. Biol. 11: 809-821.
76. Pukkila-Worley, R., and F. M. Ausubel, 2012 Immune defense mechanisms in the Caenorhabditis elegans intestinal epithelium. Curr. Opin. Immunol. 24: 3-9.
77. Pulverer, B., 2003 Whither RNAi? Nat Cell Biol 5: 489-90.
78. Rahme, L. G., E. J. Stevens, S. F. Wolfort, J. Shao, R. G. Tompkins et al., 1995 Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
79. Richardson, C. E., T. Kooistra, and D. H. Kim, 2010 An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463: 1092-1095.
80. Rino, J., and M. Carmo-Fonseca, 2009 The spliceosome: A selforganized macromolecular machine in the nucleus? Trends Cell Biol. 19: 375-384.
81. Sayers, E. W., T. Barrett, D. A. Benson, E. Bolton, S. H. Bryant et al., 2012 Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 40: D13-D25.
82. 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.
83. Shen J., J. Reis, D. C. Morrison, C. Papasian, S. Raghavakaimal et al., 2006 Key inflammatory signaling pathways are regulated by the proteasome. Shock 25: 472-484.
84. Small, E. C., S. R. Leggett, A. A. Winans, and J. P. Staley, 2006 The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol. Cell 23: 389-399.
85. Smith, A. N., R. C. Lovering, M. Futai, J. Takeda, D. Brown et al., 2003 Revised nomenclature for mammalian vacuolar-type H+-ATPase subunit genes. Mol. Cell 12: 801-803.
86. Sperling, J., M. Azubel, and R. Sperling, 2008 Structure and function of the Pre-mRNA splicing machine. Structure 16: 1605-1615.
87. Stevens, T. H., and M. Forgac, 1997 Structure, function and regulation of the vacuolar (H+)-ATPase. Annu. Rev. Cell Dev. Biol. 13: 779-808.
88. Takeuchi, O., and S. Akira, 2010 Pattern recognition receptors and inflammation. Cell 140: 805-820.
89. Tan, M. W., S. Mahajan-Miklos, and F. M. Ausubel, 1999 Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl. Acad. Sci. USA 96: 715-720.
90. Tenor, J. L., and A. Aballay, 2007 A conserved Toll-like receptor is required for Caenorhabditis elegans innate immunity. EMBO Rep. 9: 103-109.
91. 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.
92. Turner, I. A., C. M. Norman, M. J. Churcher, and A. J. Newman, 2004 Roles of the U5 snRNP in spliceosome dynamics and catalysis. Biochem. Soc. Trans. 32: 928-931.
93. Updike, D. L., and S. Strome, 2009 A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans. Genetics 183: 1397-1419.
94. Visconte, V., H. J. Rogers, J. Singh, J. Barnard, M. Bupathi et al., 2012 SF3B1 haploinsufficiency leads to formation of ring sideroblasts in myelodysplastic syndromes. Blood 120: 3173-3186.
95. Voigt, C., A. Megarbane, K. Neveling, J. C. Czeschik, B. Albrecht et al., 2013 Oto-facial syndrome and esophageal atresia, intellectual disability and zygomatic anomalies: expanding the phenotypes associated with EFTUD2 mutations. Orphanet J. Rare Dis. 8: 110.
96. Wahl, M. C., C. L. Will, and R. Luhrmann, 2009 The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701-718.
97. Wang, J., and M. A. Maldonado, 2006 The ubiquitin-proteasome system and its role in inflammatory and autoimmune diseases. Cell. Mol. Immunol. 3: 255-261.
98. Wood, W. B., 1988 The Nematode Caenorhabditis elegans, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
99. Yook, K., T. W. Harris, T. Bieri, A. Cabunoc, J. Chan et al., 2012 Worm Base 2012: more genomes, more data, new website. Nucleic Acids Res. 40: D735-D741.