Rab8a interacts directly with PI3Kγ to modulate TLR4-driven PI3K and mTOR signalling

Nature Communications

Volumn 5, Issue , 2014, Pages

  Luo, Lin ^a   Wall, Adam A ^a   Yeo, Jeremy C ^a   Condon, Nicholas D ^a   Norwood, Suzanne J ^a   Schoenwaelder, Simone ^b,c   Chen, Kaiwen W ^a   Jackson, Shaun ^b,c   Jenkins, Brendan J ^b   Hartland, Elizabeth L ^d   Schroder, Kate ^a   Collins, Brett M ^a   Sweet, Matthew J ^a   Stow, Jennifer L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PROTEIN KINASE B; RAB PROTEIN; RAB8A PROTEIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BINDING; RAB8A PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOKINE RELEASE; CYTOKINE RESPONSE; DEGRADATION; ENDOCYTOSIS; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; HUMAN; IMMUNOPRECIPITATION; LYMPHOCYTE MIGRATION; MACROPHAGE; MOLECULAR WEIGHT; NEUTROPHIL; NONHUMAN; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SURFACE PROPERTY; T LYMPHOCYTE; ANIMAL; CELL LINE RAW 264.7; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; KNOCKOUT MOUSE; MASS SPECTROMETRY; METABOLISM; MOUSE; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; MASS SPECTROMETRY; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, SCANNING; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BINDING; RAB GTP-BINDING PROTEINS; RAW 264.7 CELLS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOR SERINE-THREONINE KINASES;

EID: 84904497700     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5407     Document Type: Article

References (68)

1. Stow, J. L. & Murray, R. Z. Intracellular trafficking and secretion of inflammatory cytokines. Cytokine Growth Factor Rev. 24, 227-239 (2013).
2. Zerial, M. & McBride, H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117 (2001).
3. Wang, D. et al. Ras-related protein Rab10 facilitates TLR4 signalling by promoting replenishment of TLR4 onto the plasma membrane. Proc. Natl Acad. Sci. USA 107, 13806-13811 (2010).
4. Wang, Y. Z. et al. Lysosome-associated small Rab GTPase Rab7b negatively regulates TLR4 signalling in macrophages by promoting lysosomal degradation of TLR4. Blood 110, 962-971 (2007).
5. Husebye, H. et al. The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes. Immunity 33, 583-596 (2010).
6. Smith, A. C. et al. A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J. Cell Biol. 176, 263-268 (2007).
7. Seto, S., Tsujimura, K. & Koide, Y. Rab GTPases regulating phagosome maturation are differentially recruited to mycobacterial phagosomes. Traffic 12, 407-420 (2011).
8. Rifkin, I. R., Leadbetter, E. A., Busconi, L., Viglianti, G. & Marshak-Rothstein, A. Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol. Rev. 204, 27-42 (2005).
9. Akira, S. & Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511 (2004).
10. Aksoy, E. et al. The p110 delta isoform of the kinase PI(3)K controls the subcellular compartmentalization of TLR4 signalling and protects from endotoxic shock. Nat. Immunol. 13, 1045-1054 (2012).
11. Zanoni, I. et al. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147, 868-880 (2011).
12. Kagan, J. C. et al. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 9, 361-368 (2008).
13. Kagan, J. C. & Medzhitov, R. Phosphoinositide-mediated adaptor recruitment controls toll-like receptor signalling. Cell 125, 943-955 (2006).
14. O'Neill, L. A. J. & Bowie, A. G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7, 353-364 (2007).
15. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384 (2010).
16. Weichhart, T. et al. The TSC-mTOR signalling pathway regulates the innate inflammatory response. Immunity 29, 565-577 (2008).
17. Guertin, D. A. & Sabatini, D. M. Defining the role of mTOR in cancer. Cancer Cell 12, 9-22 (2007).
18. Cook, D. N., Pisetsky, D. S. & Schwartz, D. A. Toll-like receptors in the pathogenesis of human disease. Nat. Immunol. 5, 975-979 (2004).
19. Patel, P. C. & Harrison, R. E. Membrane ruffles capture C3bi-opsonized particles in activated macrophages. Mol. Biol. Cell 19, 4628-4639 (2008).
20. Welliver, T. P., Chang, S. L., Linderman, J. J. & Swanson, J. A. Ruffles limit diffusion in the plasma membrane during macropinosome formation. J. Cell Sci. 124, 4106-4114 (2011).
21. Abella, J. V., Parachoniak, C. A., Sangwan, V. & Park, M. Dorsal ruffle microdomains potentiate met receptor tyrosine kinase signalling and downregulation. J. Biol. Chem. 285, 24956-24967 (2010).
22. Buccione, R., Orth, J. D. & McNiven, M. A. Foot and mouth: Podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5, 647-657 (2004).
23. Hattula, K. et al. Characterization of the Rab8-specific membrane traffic route linked to protrusion formation. J. Cell Sci. 119, 4866-4877 (2006).
24. Bohdanowicz, M. et al. Phosphatidic acid is required for the constitutive ruffling and macropinocytosis of phagocytes. Mol. Biol. Cell 24, 1700-1712 (2013).
25. Yoshida, S., Hoppe, A. D., Araki, N. & Swanson, J. A. Sequential signalling in plasma-membrane domains during macropinosome formation in macrophages. J. Cell Sci. 122, 3250-3261 (2009).
26. Kavran, J. M. et al. Specificity and promiscuity in phosphoinositide binding by Pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508 (1998).
27. Fukuda, M., Kanno, E., Ishibashi, K. & Itoh, T. Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol. Cell. Proteomics 7, 1031-1042 (2008).
28. Hirsch, E. et al. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287, 1049-1053 (2000).
29. Schmid, M. C. et al. Receptor tyrosine kinases and TLR/IL1 Rs unexpectedly activate myeloid cell PI3K gamma, a single convergent point promoting tumor inflammation and progression. Cancer Cell 19, 715-727 (2011).
30. Suire, S. et al. G beta gamma s and the Ras binding domain of p110 gamma are both important regulators of PI(3)K gamma signalling in neutrophils. Nat. Cell Biol. 8, 1303-1309 (2006).
31. Suire, S. et al. p84, a new G beta gamma-activated regulatory subunit of the type IB phosphoinositide 3-kinase p110 gamma. Curr. Biol. 15, 566-570 (2005).
32. Brock, C. et al. Roles of G beta gamma in membrane recruitment and activation of p110 gamma/p101 phosphoinositide 3-kinase gamma. J. Cell Biol. 160, 89-99 (2003).
33. Hou, X. M. et al. A structural basis for Lowe syndrome caused by mutations in the Rab-binding domain of OCRL1. EMBO J. 30, 1659-1670 (2011).
34. Pacold, M. E. et al. Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Cell 103, 931-943 (2000).
35. Camps, M. et al. Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat. Med 11, 936-943 (2005).
36. Swanson, J. A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9, 639-649 (2008).
37. Jean, S. & Kiger, A. A. Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat. Rev. Mol. Cell Biol. 13, 463-470 (2012).
38. Katholnig, K., Linke, M., Pham, H., Hengstschlager, M. & Weichhart, T. Immune responses of macrophages and dendritic cells regulated by mTOR signalling. Biochem. Soc. Trans. 41, 927-933 (2013).
39. Ivanov, S. S. & Roy, C. R. Pathogen signatures activate a ubiquitination pathway that modulates the function of the metabolic checkpoint kinase mTOR. Nat. Immunol. 14, 1219-1228 (2013).
40. Peranen, J. Rab8 GTPase as a regulator of cell shape. Cytoskeleton 68, 527-539 (2011).
41. Knodler, A. et al. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl Acad. Sci. USA 107, 6346-6351 (2010).
42. Honda, A. et al. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99, 521-532 (1999).
43. Hokanson, D. E. & Bretscher, A. P. EPI64 interacts with Slp1/JFC1 to coordinate Rab8a and Arf6 membrane trafficking. Mol. Biol. Cell 23, 701-715 (2012).
44. Christoforidis, S. et al. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1, 249-252 (1999).
45. Vadas, O. et al. Molecular determinants of PI3Kgamma-mediated activation downstream of G-protein-coupled receptors (GPCRs). Proc. Natl Acad. Sci. USA 110, 18862-18867 (2013).
46. Fritsch, R. et al. RAS and RHO Families of GTPases Directly Regulate Distinct Phosphoinositide 3-Kinase Isoforms. Cell 153, 1050-1063 (2013).
47. Laffargue, M. et al. Phosphoinositide 3-kinase gamma is an essential amplifier of mast cell function. Immunity 16, 441-451 (2002).
48. Weichhart, T. & Saemann, M. D. The multiple facets of mTOR in immunity. Trends Immunol. 30, 218-226 (2009).
49. Kim, J. H., Yoon, M. S. & Chen, J. Signal transducer and activator of transcription 3 (STAT3) mediates amino acid inhibition of insulin signalling through Serine 727 phosphorylation. J. Biol. Chem. 284, 35425-35432 (2009).
50. Ruckle, T., Schwarz, M. K. & Rommel, C. PI3K gamma inhibition: towards an 'aspirin of the 21st century'? Nat. Rev. Drug Discovery 5, 903-918 (2006).
51. Kobayashi, N. et al. Blockade of class IB phosphoinositide-3 kinase ameliorates obesity-induced inflammation and insulin resistance. Proc. Natl Acad. Sci. USA 108, 5753-5758 (2011).
52. Wymann, M. P. & Solinas, G. Inhibition of phosphoinositide 3-kinase gamma attenuates inflammation, obesity, and cardiovascular risk factors. Ann. N Y Acad. Sci. 1280, 44-47 (2013).
53. Bakowski, M. A. et al. The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell. Host. Microbe. 7, 453-462 (2010).
54. Heo, W. D. et al. PI(3,4,5)P-3 and PI(4,5)P-2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461 (2006).
55. Collins, B. M., Skinner, C. F., Watson, P. J., Seaman, M. N. J. & Owen, D. J. Vps29 has a phosphoesterase fold that acts as a protein interaction scaffold for retromer assembly. Nat. Struct. Mol. Biol. 12, 594-602 (2005).
56. Tushinski, R. J. et al. Survival of mononuclear phagocytes depends on a lineagespecific growth-factor that the differentiated cells selectively destroy. Cell 28, 71-81 (1982).
57. Hume, D. A. & Gordon, S. Regulation of Bone-Marrow Macrophage Proliferation. Adv. Exp. Med. Biol. 155, 261-266 (1982).
58. Shurety, W., Merino-Trigo, A., Brown, D., Hume, D. A. & Stow, J. L. Localization and post-Golgi trafficking of tumor necrosis factor-alpha in macrophages. J. Interferon Cytokine Res. 20, 427-438 (2000).
59. Rubinson, D. A. et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference (vol 33, pg 401, 2003). Nat. Genet 39, 803-803 (2007).
60. Vitriol, E. A., Uetrecht, A. C., Shen, F. M., Jacobson, K. & Bear, J. E. Enhanced EGFP-chromophore-assisted laser inactivation using deficient cells rescued with functional EGFP-fusion proteins. Proc. Natl Acad. Sci. USA 104, 6702-6707 (2007).
61. Rubinson, D. A. et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33, 401-406 (2003).
62. Kutner, R. H., Zhang, X. Y. & Reiser, J. Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat. Protoc. 4, 495-505 (2009).
63. Yeo, J. C., Wall, A. A., Stow, J. L. & Hamilton, N. A. High-throughput quantification of early stages of phagocytosis. BioTechniques 55, 24-32 (2013).
64. Pagan, J. K. et al. The t-SNARE syntaxin 4 is regulated during macrophage activation to function in membrane traffic and cytokine secretion. Curr. Biol. 13, 156-160 (2003).
65. Murray, R. Z., Wylie, F. G., Khromykh, T., Hume, D. A. & Stow, J. L. Syntaxin 6 and Vti1b form a novel SNARE complex, which is up-regulated in activated macrophages to facilitate exocytosis of tumor necrosis Factor-alpha. J. Biol. Chem. 280, 10478-10483 (2005).
66. Schroder, K. et al. Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages. Proc. Natl Acad. Sci. USA 109, E944-E953 (2012).
67. Luo, L., King, N. P., Yeo, C. J., Jones, A. & Stow, J. L. Single-step protease cleavage elution for identification of protein-protein interactions from GST pull-down and mass spectrometry. Proteomics 14, 19-23 (2014).
68. Simon, I., Zerial, M. & Goody, R. S. Kinetics of interaction of Rab5 and Rab7 with nucleotides and magnesium ions. J. Biol. Chem. 271, 20470-20478 (1996).