JAK/STAT Pathway in Drosophila Immunity

Scandinavian Journal of Immunology

Volumn 79, Issue 6, 2014, Pages 377-385

  Myllymaki H ^a   Ramet M ^a,b,c,d  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF OULU   (Finland)

^d OULU UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN; CYTOKINE; CYTOKINE RECEPTOR; ELONGIN; ELONGIN B; ELONGIN C; HEAT SHOCK PROTEIN; JANUS KINASE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN INHIBITOR OF ACTIVATED STAT; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; UBIQUITIN PROTEIN LIGASE E3;

ANTIMICROBIAL ACTIVITY; BACTERIAL INFECTION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR IMMUNITY; DROSOPHILA; GENE EXPRESSION; HEMATOPOIESIS; INTESTINE EPITHELIUM; INTESTINE INFECTION; MUCOSAL IMMUNITY; NEGATIVE FEEDBACK; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIRUS GENE; VIRUS INFECTION;

ANIMALS; DROSOPHILA MELANOGASTER; HEMATOPOIESIS; IMMUNITY, CELLULAR; INTESTINES; JANUS KINASES; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; VIRUS DISEASES;

EID: 84901188736     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/sji.12170     Document Type: Review

References (99)

1. Stark GR, Darnell JE Jr. The JAK-STAT pathway at twenty. Immunity 2012;36:503-14.
2. O'Shea J, Plenge R. JAK and STAT signaling molecules in immunoregulation and immune-mediated disease. Immunity 2012;36:542-50.
3. Casanova J, Holland S, Notarangelo L. Inborn errors of human JAKs and STATs. Immunity 2012;36:515-28.
4. Macchi P, Villa A, Giliani S et al. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 1995;377:65-8.
5. Kiu H, Nicholson SE. Biology and significance of the JAK/STAT signalling pathways. Growth Factors 2012;30:88-106.
6. Vainchenker W, Constantinescu SN. JAK/STAT signaling in hematological malignancies. Oncogene 2013;32:2601-13.
7. Zeidler MPBN, Bausek N. The Drosophila JAK/STAT pathway. JAKSTAT 2013;2:e25353.
8. Harrison D, McCoon P, Binari R, Gilman M, Perrimon N. Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev 1998;12:3252-63.
9. Gilbert MM, Weaver BK, Gergen JP, Reich NC. A novel functional activator of the Drosophila JAK/STAT pathway, unpaired2, is revealed by an in vivo reporter of pathway activation. Mech Dev 2005;122:939-48.
10. Hombría JC, Brown S, Häder S, Zeidler MP. Characterisation of Upd2, a Drosophila JAK/STAT pathway ligand. Dev Biol 2005;288:420-33.
11. Agaisse H, Petersen U, Boutros M, Mathey-Prevot B, Perrimon N. Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev Cell 2003;5:441-50.
12. Wright VM, Vogt KL, Smythe E, Zeidler MP. Differential activities of the Drosophila JAK/STAT pathway ligands Upd, Upd2 and Upd3. Cell Signal 2011;23:920-7.
13. Pastor-Pareja JC, Wu M, Xu T. An innate immune response of blood cells to tumors and tissue damage in Drosophila. Dis Model Mech 2008;1:144-54; 153.
14. Kemp C, Mueller S, Goto A et al. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J Immunol 2013;190:650-8.
15. Brown S, Hu N, Hombría JC. Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol 2001;11:1700-5.
16. Chen H, Chen X, Oh S, Marinissen M, Gutkind J, Hou S. mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. Genes Dev 2002;16:388-98.
17. Perrimon N, Mahowald AP. l(1)hopscotch, A larval-pupal zygotic lethal with a specific maternal effect on segmentation in Drosophila. Dev Biol 1986;118:28-41.
18. Binari R, Perrimon N. Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes Dev 1994;8:300-12.
19. Hou XS, Melnick MB, Perrimon N. Marelle acts downstream of the Drosophila HOP/JAK kinase and encodes a protein similar to the mammalian STATs. Cell 1996;84:411-9.
20. Yan R, Small S, Desplan C, Dearolf CR, Darnell JE Jr. Identification of a Stat gene that functions in Drosophila development. Cell 1996;84:421-30.
21. Parganas E, Wang D, Stravopodis D et al. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 1998;93:385-95.
22. Brown S, Hu N, Hombría J. Novel level of signalling control in the JAK/STAT pathway revealed by in situ visualisation of protein-protein interaction during Drosophila development. Development 2003;130:3077-84.
23. Agaisse H, Perrimon N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 2004;198:72-82.
24. Baeg G, Zhou R, Perrimon N. Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev 2005;19:1861-70.
25. Bach E, Vincent S, Zeidler M, Perrimon N. A sensitized genetic screen to identify novel regulators of the janus kinase/signal transducer and activator of transcription pathway. Genetics 2003;165:1149-66.
26. Müller P, Kuttenkeuler D, Gesellchen V, Zeidler M, Boutros M. Identification of JAK/STAT signalling components by genome-wide RNA interference. Nature 2005;436:871-5.
27. Kallio J, Myllymäki H, Grönholm J et al. Eye transformer is a negative regulator of Drosophila JAK/STAT signaling. FASEB J 2010;24:4467-79.
28. Grönholm J, Kaustio M, Myllymäki H et al. Not4 enhances JAK/STAT pathway-dependent gene expression in Drosophila and in human cells. FASEB J 2012;26:1239-50.
29. Narazaki M, Yasukawa K, Saito T et al. Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 1993;82:1120-6.
30. Makki R, Meister M, Pennetier D et al. A short receptor downregulates JAK/STAT signalling to control the Drosophila cellular immune response. PLoS Biol 2010;8:e1000441.
31. Starr R, Willson TA, Viney EM et al. A family of cytokine-inducible inhibitors of signalling. Nature 1997;387:917-21.
32. Inagaki-Ohara K, Kondo T, Ito M, Yoshimura A. SOCS, inflammation, and cancer. JAKSTAT 2013;2:e24053.
33. Rawlings J, Rennebeck G, Harrison S, Xi R, Harrison D. Two Drosophila suppressors of cytokine signaling (SOCS) differentially regulate JAK and EGFR pathway activities. BMC Cell Biol 2004;5:38.
34. Stec W, Zeidler M. Drosophila SOCS Proteins. J Signal Transduct 2011;2011:894510.
35. Callus B, Mathey-Prevot B. SOCS36E, a novel Drosophila SOCS protein, suppresses JAK/STAT and EGF-R signalling in the imaginal wing disc. Oncogene 2002;21:4812-21.
36. Karsten P, Häder S, Zeidler MP. Cloning and expression of Drosophila SOCS36E and its potential regulation by the JAK/STAT pathway. Mech Dev 2002;117:343-6.
37. Stec W, Vidal O, Zeidler MP. Drosophila SOCS36E negatively regulates JAK/STAT pathway signaling via two separable mechanisms. Mol Biol Cell 2013;24:3000-9.
38. Vidal OM, Stec W, Bausek N, Smythe E, Zeidler MP. Negative regulation of Drosophila JAK-STAT signalling by endocytic trafficking. J Cell Sci 2010;123:3457-66.
39. Chung C, Liao J, Liu B et al. Specific inhibition of Stat3 signal transduction by PIAS3. Science 1997;278:1803-5.
40. Betz A, Lampen N, Martinek S, Young M, Darnell JJ. A Drosophila PIAS homologue negatively regulates stat92E. Proc Natl Acad Sci USA 2001;98:9563-8.
41. Ungureanu D, Vanhatupa S, Kotaja N et al. PIAS proteins promote SUMO-1 conjugation to STAT1. Blood 2003;102:3311-3.
42. Grönholm J, Ungureanu D, Vanhatupa S, Rämet M, Silvennoinen O. Sumoylation of Drosophila transcription factor Stat92E. J Innate Immun 2010;2:618-24.
43. Harris M, Mostecki J, Rothman P. Repression of an interleukin-4-responsive promoter requires cooperative BCL-6 function. J Biol Chem 2005;280:13114-21.
44. Arbouzova NI, Bach EA, Zeidler MP. Ken & barbie selectively regulates the expression of a subset of JAK/STAT pathway target genes. Curr Biol 2006;16:80-8.
45. Coste F, Kemp C, Bobezeau V et al. Crystal structure of Diedel, a marker of the immune response of Drosophila melanogaster. PLoS ONE 2012;7:e33416.
46. Small S, Blair A, Levine M. Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. Dev Biol 1996;175:314-24.
47. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 2001;294:2542-5.
48. Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 2001;294:2546-9.
49. Wang W, Li Y, Zhou L, Yue H, Luo H. Role of JAK/STAT signaling in neuroepithelial stem cell maintenance and proliferation in the Drosophila optic lobe. Biochem Biophys Res Commun 2011;410:714-20.
50. Boutros M, Agaisse H, Perrimon N. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev Cell 2002;3:711-22.
51. Valanne S, Wang JH, Rämet M. The Drosophila Toll signaling pathway. J Immunol 2011;186:649-56.
52. Myllymäki H, Valanne S, Rämet M. The Drosophila Imd signaling pathway. J Immunol 2014;192:3455-62.
53. Ekengren S, Tryselius Y, Dushay MS, Liu G, Steiner H, Hultmark D. A humoral stress response in Drosophila. Curr Biol 2001;11:1479.
54. Ekengren S, Hultmark D. A Family of Turandot-related genes in the humoral stress response of Drosophila. Biochem Biophys Res Commun 2001;284:998-1003.
55. Luo H, Hanratty WP, Dearolf CR. An amino acid substitution in the Drosophila hopTum-l Jak kinase causes leukemia-like hematopoietic defects. EMBO J 1995;14:1412-20.
56. Sorrentino R, Melk J, Govind S. Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 2004;166:1343-56.
57. Honti V, Csordás G, Kurucz É, Márkus R, Andó I. The cell-mediated immunity of Drosophila melanogaster: hemocyte lineages, immune compartments, microanatomy and regulation. Dev Comp Immunol 2014;42:47-56.
58. Ulvila J, Vanha-Aho L, Rämet M. Drosophila phagocytosis - still many unknowns under the surface. APMIS 2011;119:651-62.
59. Sorrentino RP, Carton Y, Govind S. Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev Biol 2002;243:65-80.
60. Crozatier M, Meister M. Drosophila haematopoiesis. Cell Microbiol 2007;9:1117-26.
61. Minakhina S, Steward R. Hematopoietic stem cells in Drosophila. Development 2010;137:27-31.
62. Krzemień J, Dubois L, Makki R, Meister M, Vincent A, Crozatier M. Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 2007;446:325-8.
63. Lanot R, Zachary D, Holder F, Meister M. Postembryonic hematopoiesis in Drosophila. Dev Biol 2001;230:243-57.
64. Stofanko M, Kwon SY, Badenhorst P. Lineage tracing of lamellocytes demonstrates Drosophila macrophage plasticity. PLoS ONE 2010;5:e14051.
65. Honti V, Csordas G, Markus R, Kurucz E, Jankovics F, Ando I. Cell lineage tracing reveals the plasticity of the hemocyte lineages and of the hematopoietic compartments in Drosophila melanogaster. Mol Immunol 2010;47:1997-2004.
66. Sinenko SA, Shim J, Banerjee U. Oxidative stress in the haematopoietic niche regulates the cellular immune response in Drosophila. EMBO Rep 2011;13:83-9.
67. Markus R, Laurinyecz B, Kurucz E et al. Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci USA 2009;106:4805-9.
68. Rizki T, Rizki R, Carton Y. Leptopilina heterotoma and L. boulardi: strategies to avoid cellular defense responses of Drosophila melanogaster. Exp Parasitol 1990;70:466-75.
69. Wertheim B, Kraaijeveld AR, Schuster E et al. Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 2005;6:R94.
70. Harrison D, Binari R, Nahreini T, Gilman M, Perrimon N. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J 1995;14:2857-65.
71. Ekas LA, Cardozo TJ, Flaherty MS, McMillan EA, Gonsalves FC, Bach EA. Characterization of a dominant-active STAT that promotes tumorigenesis in Drosophila. Dev Biol 2010;344:621-36.
72. Bangi E. Drosophila at the intersection of infection, inflammation, and cancer. Front Cell Infect Microbiol 2013;3:103.
73. Wu M, Pastor-Pareja JC, Xu T. Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature 2010;463:545-8.
74. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006;6:24-37.
75. Galiana-Arnoux D, Dostert C, Schneemann A, Hoffmann J, Imler J. Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat Immunol 2006;7:590-7.
76. Habayeb M, Ekengren S, Hultmark D. Nora virus, a persistent virus in Drosophila, defines a new picorna-like virus family. J Gen Virol 2006;87:3045-51.
77. Merkling SH, van Rij RP. Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. J Insect Physiol 2013;59:159-70.
78. Wang J, Valanne S, Rämet M. Drosophila as a model for antiviral immunity. World J Biol Chem 2010;1:151-9.
79. Ulvila J, Hultmark D, Rämet M. RNA silencing in the antiviral innate immune defence-role of DEAD-box RNA helicases. Scand J Immunol 2010;71:146-58.
80. Avadhanula V, Weasner BP, Hardy GG, Kumar JP, Hardy RW. A novel system for the launch of alphavirus RNA synthesis reveals a role for the Imd pathway in arthropod antiviral response. PLoS Pathog 2009;5:e1000582.
81. Zambon RA, Nandakumar M, Vakharia VN, Wu LP. The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci USA 2005;102:7257-62.
82. Costa A, Jan E, Sarnow P, Schneider D. The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 2009;4:e7436.
83. Dostert C, Jouanguy E, Irving P et al. The JAK/STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat Immunol 2005;6:946-53.
84. Souza-Neto JA, Sim S, Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 2009;106:17841-6.
85. Paradkar P, Trinidad L, Voysey R, Duchemin J, Walker P. Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proc Natl Acad Sci USA 2012;109:18915-20.
86. Deddouche S, Matt N, Budd A et al. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat Immunol 2008;9:1425-32.
87. Lee KA, Lee WJ. Drosophila as a model for intestinal dysbiosis and chronic inflammatory diseases. Dev Comp Immunol 2014;42:102-10.
88. Lhocine N, Ribeiro PS, Buchon N et al. PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 2008;4:147-58.
89. Ha EM, Oh CT, Ryu JH et al. An antioxidant system required for host protection against gut infection in Drosophila. Dev Cell 2005;8:125-32.
90. Valanne S, Ramet M. Uracil debases pathogenic but not commensal bacteria. Cell Host Microbe 2013;13:505-6.
91. Ryu JH, Kim SH, Lee HY et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 2008;319:777-82.
92. Ryu JH, Nam KB, Oh CT et al. The homeobox gene Caudal regulates constitutive local expression of antimicrobial peptide genes in Drosophila epithelia. Mol Cell Biol 2004;24:172-85.
93. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 2009;5:200-11.
94. Cronin S, Nehme N, Limmer S et al. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 2009;325:340-3.
95. Buchon N, Broderick N, Chakrabarti S, Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 2009;23:2333-44.
96. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009;137:1343-55.
97. Mukherjee T, Schäfer U, Zeidler M. Identification of Drosophila genes modulating Janus kinase/signal transducer and activator of transcription signal transduction. Genetics 2006;172:1683-97.
98. Fisher KH, Wright VM, Taylor A, Zeidler MP, Brown S. Advances in genome-wide RNAi cellular screens: a case study using the Drosophila JAK/STAT pathway. BMC Genomics 2012;13:506.
99. Lucchetta EM, Ohlstein B. The Drosophila midgut: a model for stem cell driven tissue regeneration. Wiley Interdiscip Rev Dev Biol 2012;1:781-8.