A member of the p38 mitogen-activated protein kinase family is responsible for transcriptional induction of Dopa decarboxylase in the epidermis of Drosophila melanogaster during the innate immune response

Molecular and Cellular Biology

Volumn 28, Issue 15, 2008, Pages 4883-4895

  Davis, Monica M ^a   Primrose, David A ^a   Hodgetts, Ross B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME INDUCTION; EPIDERMIS; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL INFECTIONS; BINDING SITES; CONSERVED SEQUENCE; DOPA DECARBOXYLASE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME INDUCTION; EPIDERMIS; IMMUNITY, NATURAL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MOLECULAR SEQUENCE DATA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BINDING; SURVIVAL ANALYSIS; TIME FACTORS; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC;

DROSOPHILA MELANOGASTER; NEGIBACTERIA; POSIBACTERIA;

EID: 47949092612     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02074-07     Document Type: Article

References (88)

1. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with Image J. Biophotonics Int. 11:36-42.
2. Andersen, S. O., P. Hojrup, and P. Roepstorff. 1995. Insect cuticular proteins. Insect Biochem. Mol. Biol. 25:153-176.
3. Barolo, S., L. A. Carver, and J. W. Posakony. 2000. GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. BioTechniques 29:726-732.
4. Bidla, G., M. S. Dushay, and U. Theopold. 2007. Crystal cell rupture after injury in Drosophila requires the JNK pathway, small GTPases and the TNF homolog Eiger. J. Cell Sci. 120:1209-1215.
5. Bidla, G., M. Lindgren, U. Theopold, and M. S. Dushay. 2005. Hemolymph coagulation and phenoloxidase in Drosophila larvae. Dev. Comp. Immunol. 29:669-679.
6. Biggs, W. H., III, K. H. Zavitz, B. Dickson, A. van der Straten, D. Brunner, E. Hafen, and S. L. Zipursky. 1994. The Drosophila rolled locus encodes a MAP kinase required in the sevenless signal transduction pathway. EMBO J. 13:1628-1635.
7. Bischoff, V., C. Vignal, I. G. Boneca, T. Michel, J. A. Hoffmann, and J. Royet. 2004. Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat. Immunol. 5:1175-1180.
8. Bosch, M., F. Serras, E. Martin-Blanco, and J. Baguna. 2005. JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginai discs. Dev. Biol. 280:73-86.
9. Boutros, M., H. Agaisse, and N. Perrimon. 2002. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 3:711-722.
10. Braun, A., J. A. Hoffmann, and M. Meister. 1998. Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc. Natl. Acad. Sci. USA 95:14337-14342.
11. Busse, M. S., C. P. Arnold, P. Towb, J. Katrivesis, and S. A. Wasserman. 2007. A kappaB sequence code for pathway-specific innate immune responses. EMBO J. 26:3826-3835.
12. Corbo, J. C., and M. Levine. 1996. Characterization of an immunodeficiency mutant in Drosophila. Mech. Dev. 55:211-220.
13. Craig, C. R., J. L. Fink, Y. Yagi, Y. T. Ip, and R. L. Cagan. 2004. A Drosophila p38 orthologue is required for environmental stress responses. EMBO Rep. 5:1058-1063.
14. Davis, M. M., S. L. O'Keefe, D. A. Primrose, and R. B. Hodgetts. 2007. A neuropeptide hormone cascade controls the precise onset of post-eclosion cuticular tanning in Drosophila melanogaster. Development 134:4395-4404.
15. Davis, M. M., P. Yang, L. Chen, S. L. O'Keefe, and R. B. Hodgetts. 2007. The orphan nuclear receptor DHR38 influences transcription of the DOPA decarboxylase gene in epidermal and neural tissues of Drosophila melanogaster. Genome 50:1049-1060.
16. Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103:239-252.
17. De Gregorio, E., P. T. Spellman, G. M. Rubin, and B. Lemaitre. 2001. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 98:12590-12595.
18. Delaney, J. R., S. Stoven, H. Uvell, K. V. Anderson, Y. Engstrom, and M. Mlodzik. 2006. Cooperative control of Drosophila immune responses by the JNK and NF-kappaB signaling pathways. EMBO J. 25:3068-3077.
19. Dushay, M. S., B. Asling, and D. Hultmark. 1996. Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proc. Natl. Acad. Sci. USA 93:10343-10347.
20. Ferrandon, D., A. C. Jung, M. Criqui, B. Lemaitre, S. Uttenweiler-Joseph, L. Michaut, J. Reichhart, and J. A. Hoffmann. 1998. A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway. EMBO J. 17:1217-1227.
21. Galko, M. J., and M. A. Krasnow. 2004. Cellular and genetic analysis of wound healing in Drosophila larvae. PLoS Biol. 2:E239.
22. Giordano, E., R. Rendina, I. Peluso, and M. Furia. 2002. RNAi triggered by symmetrically transcribed transgenes in Drosophila melanogaster. Genetics 160:637-648.
23. Glise, B., H. Bourbon, and S. Noselli. 1995. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83:451-461.
24. Gloor, G. B., J. Moretti, J. Mouyal, and K. J. Keeler. 2000. Distinct P-element excision products in somatic and gcrmline cells of Drosophila melanogaster. Genetics 155:1821-1830.
25. Gottar, M., V. Gobert, T. Michel, M. Belvin, G. Duyk, J. A. Hoffmann, D. Ferrandon, and J. Royet. 2002. The Drosophila immune response against Gram-negative bacteria is mediated by a pcptidoglycan recognition protein. Nature 416:640-644.
26. Grosshans, J., and E. Wieschaus. 2000. A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101:523-531.
27. Han, Z. S., H. Enslen, X. Hu, X. Meng, I.-H. Wu, T. Barrett, R. J. Davis, and Y. T. Ip. 1998. A conserved p38 mitogen-activated protein kinase pathway regulates Drosophila immunity gene expression. Mol. Cell. Biol. 18:3527-3539.
28. Hedengren, M., H. Asling, M. S. Dushay, I. Ando, S. Ekengren, M. Wihlborg, and D. Hultmark. 1999. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol. Cell 4:827-837.
29. Hegedus, Z., A. Czibula, and E. Kiss-Toth. 2007. Tribbles: a family of kinase-like proteins with potent signalling regulatory function. Cell. Signal. 19:238-250.
30. Hodgetts, R. B. 1972. Biochemical characterization of mutants affecting the metabolism of β-alanine in Drosophila. J. Insect Physiol. 18:937-947.
31. Hoffmann, J. A., F. C. Kafatos, C. A. Janeway, and R. A. Ezekowitz. 1999. Phylogenetic perspectives in innate immunity. Science 284:1313-1318.
32. Imler, J. L., and P. Bulet. 2005. Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem. Immunol. Allergy 86:1-21.
33. Ip, Y. T., M. Reach, Y. Engstrom, L. Kadalayil, H. Cai, S. Gonzalez-Crespo, K. Tatei, and M. Levine. 1993. Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 75:753-763.
34. Irving, P., L. Troxler, T. S. Heuer, M. Belvin, C. Kopczynski, J. M. Reichhart, J. A. Hoffmann, and C. Hetru. 2001. A genome-wide analysis of immune responses in Drosophila. Proc. Natl. Acad. Sci. USA 98:15119- 15124.
35. Kallio, J., A. Leinenen, J. Ulvila, S. Valanne, R. A. Ezekowitz, and M. Ramet. 2005. Functional analysis of immune response genes in Drosophila identifies JNK pathway as a regulator of antimicrobial peptide gene expression in S2 cells. Microbes Infect. 7:811-819.
36. Karlsson, C., A. M. Korayem, C. Scherfer, O. Loseva, M. S. Dushay, and U. Theopold. 2004. Proteomic analysis of the Drosophila larval hemolymph clot. J. Biol. Chem. 279:52033-52041.
37. Kent, W. J. 2002. BLAT - the BLAST-like alignment tool. Genome Res. 12:656-664.
38. Kim, L. K., U. Y. Choi, H. S. Cho, J. S. Lee, W. B. Lee, J. Kim, K. Jeong, J. Shim, J. Kim-Ha, and Y. J. Kim. 2007. Down-regulation of NF-kappaB target genes by the AP-1 and STAT complex during the innate immune response in Drosophila. PLoS Biol. 5:e238.
39. Kim, M. H., C. H. Joo, M. Y. Cho, T. H. Kwon, K. M. Lee, S. Natori, T. H. Lee, and B. L. Lee. 2000. Bacterial-injection-induced syntheses of N-beta-alanyldopaminc and Dopa decarboxylase in the hemolymph of eoleopteran insect, Tcnebrio molitor larvae. Eur. J. Biochem. 267:2599-2608.
40. Kockel, L., J. G. Homsy, and D. Bohmann. 2001. Drosophila AP-1: lessons from an invertebrate. Oncogene 20:2347-2364.
41. Lazareva, A. A., G. Roman, W. Mattox, P. E. Hardin, and B. Dauwalder. 2007. A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet. 3:e16.
42. Lee, Y. S., and R. W. Carthew. 2003. Making a better RNAi vector for Drosophila: use of intron spacers. Methods 30:322-329.
43. Lemaitre, B., and J. Hoffmann. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25:697-743.
44. Lemaitre, B., E. Kromer-Metzger, L. Michaut, E. Nicolas, M. Meister, P. Georgel, J. M. Reichhart, and J. A. Hoffmann. 1995. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. USA 92:9465-9469.
45. Lemaitre, B., E. Nicolas, L. Michaut, J. M. Reichhart, and J. A. Hoffmann. 1996. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-983.
46. Levashina, E. A., S. Ohresser, B. Lemaitre, and J. L. Imler. 1998. Two distinct pathways can control expression of the gene encoding the Drosophila antimicrobial peptide metchnikowin. J. Mol. Biol. 278:515-527.
47. Lindsley, D. L., and G. G. Zimm. 1992. The genome of Drosophila melanogaster, vol. 8. Academic Press, San Diego, CA.
48. Lu, Y., L. P. Wu, and K. V. Anderson. 2001. The antibacterial arm of the Drosophila innate immune response requires an IkappaB kinase. Genes Dev. 15:104-110.
49. Mace, K. A., J. C. Pearson, and W. McGinnis. 2005. An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 308:381-385.
50. Manfruelli, P., J. M. Reichhart, R. Steward, J. A. Hoffmann, and B. Lemaitre. 1999. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J. 18:3380-3391.
51. Martin-Blanco, E. 2000. p38 MAPK signalling cascades: ancient roles and new functions. Bioessays 22:637-645.
52. Mata, J., S. Curado, A. Ephrussi, and P. Rorth. 2000. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101:511-522.
53. Meister, M. 2004. Blood cells of Drosophila: cell lineages and role in host defence. Curr. Opin. Immunol. 16:10-15.
54. Meister, M., and M. Lagueux. 2003. Drosophila blood cells. Cell. Microbiol. 5:573-580.
55. Meng, X., B. S. Khanuja, and Y. T. Ip. 1999. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev. 13:792-797.
56. Michel, T., J. M. Reichhart, J. A. Hoffmann, and J. Royet. 2001. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414:756-759.
57. Nappi, A. J., Y. Carton, and E. Vass. 1992. Reduced cellular immune competence of a temperature-sensitive Dopa decarboxylase mutant strain of Drosophila melanogaster against the parasite Leptopilina boulardi. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 101:453-460.
58. Nappi, A. J., and E. Ottaviani. 2000. Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 22:469-480.
59. Perkins, K. K., A. Admon, N. Patel, and R. Tjian. 1990. The Drosophila Fos-related AP-1 protein is a developmentally regulated transcription factor. Genes Dev. 4:822-834.
60. Perkins, K. K., G. M. Dailey, and R. Tjian. 1988. Novel Jun- and Fos-related proteins in Drosophila are functionally homologous to enhancer factor AP-1. EMBO J. 7:4265-4273.
61. Petersen, U. M., G. Bjorklund, Y. T. Ip, and Y. Engstrom. 1995, The dorsal-related immunity factor, Dif, is a sequence-specific trans-activator of Drosophila Cecropin gene expression. EMBO J. 14:3146-3158.
62. Phillips, A. M., R. Smart, R. Strauss, B. Brembs, and L. E. Kelly. 2005. The Drosophila black enigma: the molecular and behavioural characterization of the black1 mutant allele. Gene 351:131-142.
63. Ramet, M., R. Lanot, D. Zachary, and P. Manfruelli. 2002. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 241:145-156.
64. Riesgo-Escovar, J. R., M. Jenni, A. Fritz, and E. Hafen. 1996. The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev. 10:2759-2768.
65. Rizki, T. M., R. M. Rizki, and R. A. Bellotti. 1985. Genetics of a Drosophila phenoloxidase. Mol. Gen. Genet. 201:7-13.
66. Rutschmann, S., A. C. Jung, C. Hetru, J. M. Reichhart, J. A. Hoffmann, and D. Ferrandon. 2000. The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila. Immunity 12:569-580.
67. Rutschmann, S., A. C. Jung, R. Zhou, N. Silverman, J. A. Hoffmann, and D. Ferrandon. 2000. Role of Drosophila IKK gamma in a toll-independent antibacterial immune response. Nat. Immunol. 1:342-347.
68. Rutschmann, S., A. Kilinc, and D. Ferrandon. 2002. Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J. Immunol. 168:1542-1546.
69. Ryu, J. H., E. M. Ha, C. T. Oh, J. H. Seol, P. T. Brey, I. Jin, D. G. Lee, J. Kim, D. Lee, and W. J. Lee. 2006. An essential complementary role of NF-kappaB pathway to microbicidal oxidants in Drosophila gut immunity. EMBO J. 25:3693-3701.
70. Schachter, J., M. M. Perez, and L. A. Quesada-Allue. 2007. The role of N-beta-alanyldopamine synthase in the innate immune response of two insects. J. Insect Physiol. 53:1188-1197.
71. Scherfer, C., C. Karlsson, O. Loseva, G. Bidla, A. Goto, J. Havemann, M. S. Dushay, and U. Theopold. 2004. Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr. Biol. 14:625-629.
72. Schug, J. 2003. Using TESS to predict transcription factor binding sites in DNA sequence, chapter 2.6. In A. D. Baxevanis (ed.), Current protocols in bioinformatics. J. Wiley and Sons, Hoboken, NJ.
73. Silverman, N., R. Zhou, R. L. Erlich, M. Hunter, E. Bernstein, D. Schneider, and T. Maniatis. 2003. Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J. Biol. Chem. 278:48928-48934.
74. Silverman, N., R. Zhou, S. Stoven, N. Pandey, D. Hultmark, and T. Maniatis. 2000. A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity. Genes Dev. 14:2461-2471.
75. Stathopoulos, A., and M. Levine. 2002. Dorsal gradient networks in the Drosophila embryo. Dev. Biol. 246:57-67.
76. Staveley, B. E., T. R. Heslip, R. B. Hodgetts, and J. B. Bell. 1995. Protected P-elemcnt termini suggest a role for inverted-repeat-binding protein in transposase-induced gap repair in Drosophila melanogaster. Genetics 139: 1321-1329.
77. Takasu-Ishikawa, E., M. Yoshihara, and Y. Hotta. 1992. Extra sequences found at P element excision sites in Drosophila melanogaster. Mol. Gen. Genet. 232:17-23.
78. Takehana, A., T. Yano, S. Mita, A. Kotani, Y. Oshima, and S. Kurata. 2004. Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J. 23:4690-4700.
79. Tzou, P., S. Ohresser, D. Ferrandon, M. Capovilla, J. M. Reichhart, B. Lemaitre, J. A. Hoffmann, and J. L. Imler. 2000. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13:737-748.
80. Vidal, S., R. S. Khush, F. Leulier, P. Tzou, M. Nakamura, and B. Lemaitre. 2001. Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-kappaB-dependent innate immune responses. Genes Dev. 15:1900-1912.
81. Walter, M. F., L. L. Zeineh, B. C. Black, W. E. McIvor, T. R. Wright, and H. Biessmann. 1996. Catecholamine metabolism and in vitro induction of premature cuticle melanization in wild type and pigmentation mutants of Drosophila melanogaster. Arch. Insect Biochem. Physiol. 31:219-233.
82. Weber, J. P., R. J. Bolin, M. S. Hixon, and A. F. Sherald. 1992. Beta-alanine transaminase activity in black and suppressor of black mutations of Drosophila melanogaster. Bioehim. Biophys. Acta 1115:181-186.
83. Wright, T. R. 1987. The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv. Genet. 24:127-222.
84. Wright, T. R., G. C. Bewley, and A. F. Sherald. 1976. The genetics of dopa decarboxylase in Drosophila melanogaster. II. Isolation and characterization of dopa-decarboxylase-deficient mutants and their relationship to the a-methyl-dopa-hypersensitivc mutants. Genetics 84:287-310.
85. Wright, T. R., R. Steward, K. W. Bentley, and P. N. Adler. 1981. The genetics of Dopa decarboxylase in Drosophila melanogaster. III. Effect of a temperature sensitive Dopa decarboxylase deficient mutation of female fertility. Dev. Genet. 2:223-235.
86. Zettervall, C. J., I. Anderl, M. J. Williams, R. Palmer, E. Kurucz, I. Ando, and D. Hultmark. 2004. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101:14192-14197.
87. Zhang, K., J. R. Chaillet, L. A. Perkins, T. D. Halazonetis, and N. Perrimon. 1990. Drosophila homolog of the mammalian jun oncogene is expressed during embryonic development and activates transcription in mammalian cells. Proc. Natl. Acad. Sci. USA 87:6281-6285.
88. Zhuang, Z. H., Y. Zhou, M. C. Yu, N. Silverman, and B. X. Ge. 2006. Regulation of Drosophila p38 activation by specific MAP2 kinase and MAP3 kinase in response to different stimuli. Cell. Signal. 18:441-448.