Btk regulates macrophage polarization in response to lipopolysaccharide

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Gabhann, Joan Ní ^a   Hams, Emily ^b   Smith, Siobhán ^a   Wynne, Claire ^a,c   Byrne, Jennifer C ^a   Brennan, Kiva ^b   Spence, Shaun ^f   Kissenpfennig, Adrien ^f   Johnston, James A ^g   Fallon, Padraic G ^b,d,e   Jefferies, Caroline A ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c DUBLIN INSTITUTE OF TECHNOLOGY   (Ireland)

^d ST JAMES S HOSPITAL   (Ireland)

^e OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^f QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^g AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRUTON TYROSINE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN KINASE B; REGULATOR PROTEIN; SHIP1 PROTEIN; STAT1 PROTEIN; STAT6 PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; INFLAMMATION; M1 MACROPHAGE; M2 MACROPHAGE; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSCRIPTION INITIATION;

ANIMALS; CELL POLARITY; HYPERSENSITIVITY; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PHENOTYPE; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION, GENETIC;

EID: 84908193590     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085834     Document Type: Article

References (70)

1. Orme J, Mohan C (2012) Macrophage subpopulations in systemic lupus erythematosus. Discov Med 13: 151-158.
2. Shechter R, Schwartz M (2013) Harnessing monocyte-derived macrophages to control central nervous system pathologies: no longer 'if' but 'how'. J Pathol 229: 332-346.
3. Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, et al. (2012) Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012: 948098.
4. Dasgupta P, Keegan AD (2012) Contribution of alternatively activated macrophages to allergic lung inflammation: a tale of mice and men. J Innate Immun 4: 478-488.
5. Sica A, Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122: 787-795.
6. Yu H, Pardoll D, Jove R (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9: 798-809.
7. Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, et al. (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7: 148-155. (Pubitemid 43135880)
8. Pelegrin P, Surprenant A (2009) Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1beta release through pyrophosphates. EMBO J 28: 2114-2127.
9. Porta C, Rimoldi M, Raes G, Brys L, Ghezzi P, et al. (2009) Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci U S A 106: 14978-14983.
10. Mantovani A, Sica A (2010) Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 22: 231-237.
11. Pauleau AL, Rutschman R, Lang R, Pernis A, Watowich SS, et al. (2004) Enhancer-mediated control of macrophage-specific arginase I expression. J Immunol 172: 7565-7573. (Pubitemid 38747620)
12. Kortylewski M, Kujawski M, Wang T, Wei S, Zhang S, et al. (2005) Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat Med 11: 1314-1321. (Pubitemid 41752912)
13. Ostrand-Rosenberg S, Grusby MJ, Clements VK (2000) Cutting edge: STAT6-deficient mice have enhanced tumor immunity to primary and metastatic mammary carcinoma. J Immunol 165: 6015-6019.
14. Sinha P, Clements VK, Ostrand-Rosenberg S (2005) Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J Immunol 174: 636-645. (Pubitemid 40094255)
15. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, et al. (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447: 1116-1120. (Pubitemid 47014427)
16. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, et al. (2011) Kruppel-like factor 4 regulates macrophage polarization. J Clin Invest 121: 2736-2749.
17. Sly LM, Rauh MJ, Kalesnikoff J, Song CH, Krystal G (2004) LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 21: 227-239. (Pubitemid 39094052)
18. An H, Xu H, Zhang M, Zhou J, Feng T, et al. (2005) Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through a phosphatase activity- and PI-3K-independent mechanism. Blood 105: 4685-4692. (Pubitemid 40807290)
19. Gabhann JN, Higgs R, Brennan K, Thomas W, Damen JE, et al. (2010) Absence of SHIP-1 results in constitutive phosphorylation of tank-binding kinase 1 and enhanced TLR3-dependent IFN-beta production. J Immunol 184: 2314-2320.
20. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proceedings of the National Academy of Sciences 106: 7113-7118.
21. Spence S, Fitzsimons A, Boyd CR, Kessler J, Fitzgerald D, et al. (2013) Suppressors of cytokine signaling 2 and 3 diametrically control macrophage polarization. Immunity 38: 66-78.
22. Ni Gabhann J, Spence S, Wynne C, Smith S, Byrne JC, et al. (2011) Defects in acute responses to TLR4 in Btk-deficient mice result in impaired dendritic cell-induced IFN-gamma production by natural killer cells. Clin Immunol.
23. Doyle SL, Jefferies CA, O'Neill LA (2005) Bruton's tyrosine kinase is involved in p65-mediated transactivation and phosphorylation of p65 on serine 536 during NFkappaB activation by lipopolysaccharide. J Biol Chem 280: 23496-23501. (Pubitemid 40884827)
24. Doyle SL, Jefferies CA, Feighery C, O'Neill LA (2007) Signaling by Toll-like receptors 8 and 9 requires Bruton's tyrosine kinase. J Biol Chem 282: 36953-36960.
25. Horwood NJ, Mahon T, McDaid JP, Campbell J, Mano H, et al. (2003) Bruton's tyrosine kinase is required for lipopolysaccharide-induced tumor necrosis factor alpha production. J Exp Med 197: 1603-1611. (Pubitemid 36745336)
26. Horwood NJ, Page TH, McDaid JP, Palmer CD, Campbell J, et al. (2006) Bruton's tyrosine kinase is required for TLR2 and TLR4-induced TNF, but not IL-6, production. J Immunol 176: 3635-3641. (Pubitemid 43364011)
27. Lee KG, Xu S, Kang ZH, Huo J, Huang M, et al. (2012) Bruton's tyrosine kinase phosphorylates Toll-like receptor 3 to initiate antiviral response. Proc Natl Acad Sci U S A 109: 5791-5796.
28. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, et al. (2011) IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 12: 231-238.
29. Fleetwood AJ, Dinh H, Cook AD, Hertzog PJ, Hamilton JA (2009) GM-CSF-and M-CSF-dependent macrophage phenotypes display differential dependence on Type I interferon signaling. Journal of Leukocyte Biology 86: 411-421.
30. Hendriks RW, de Bruijn MF, Maas A, Dingjan GM, Karis A, et al. (1996) Inactivation of Btk by insertion of lacZ reveals defects in B cell development only past the pre-B cell stage. EMBO J 15: 4862-4872. (Pubitemid 26315797)
31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
32. Smith P, Mangan NE, Fallon PG (2009) Generation of parasite antigens for use in Toll-like receptor research. Methods Mol Biol 517: 401-413.
33. Mangan NE, Dasvarma A, McKenzie AN, Fallon PG (2007) T1/ST2 expression on Th2 cells negatively regulates allergic pulmonary inflammation. Eur J Immunol 37: 1302-1312. (Pubitemid 46925314)
34. Hams E, Saunders SP, Cummins EP, O'Connor A, Tambuwala MT, et al. (2011) The hydroxylase inhibitor dimethyloxallyl glycine attenuates endotoxic shock via alternative activation of macrophages and IL-10 production by B1 cells. Shock 36: 295-302.
35. Ghosn EE, Cassado AA, Govoni GR, Fukuhara T, Yang Y, et al. (2010) Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc Natl Acad Sci U S A 107: 2568-2573.
36. Taneichi H, Kanegane H, Sira MM, Futatani T, Agematsu K, et al. (2008) Toll-like receptor signaling is impaired in dendritic cells from patients with X-linked agammaglobulinemia. Clin Immunol 126: 148-154.
37. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3: 23-35.
38. Lin SL, Castaño AP, Nowlin BT, Lupher ML, Duffield JS (2009) Bone Marrow Ly6Chigh Monocytes Are Selectively Recruited to Injured Kidney and Differentiate into Functionally Distinct Populations. The Journal of Immunology 183: 6733-6743.
39. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686. (Pubitemid 39457982)
40. Martinez FO, Gordon S, Locati M, Mantovani A (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177: 7303-7311. (Pubitemid 44715100)
41. Porcheray F, Viaud S, Rimaniol AC, Leone C, Samah B, et al. (2005) Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol 142: 481-489. (Pubitemid 41719844)
42. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511. (Pubitemid 38931765)
43. Ramalingam TR, Reiman RM, Wynn TA (2005) Exploiting worm and allergy models to understand Th2 cytokine biology. Curr Opin Allergy Clin Immunol 5: 392-398. (Pubitemid 41345305)
44. Reese TA, Liang HE, Tager AM, Luster AD, Van Rooijen N, et al. (2007) Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature 447: 92-96. (Pubitemid 46685837)
45. Perez de Diego R, Lopez-Granados E, Pozo M, Rodriguez C, Sabina P, et al. (2006) Bruton's tyrosine kinase is not essential for LPS-induced activation of human monocytes. J Allergy Clin Immunol 117: 1462-1469. (Pubitemid 44208984)
46. Gagliardi MC, Finocchi A, Orlandi P, Cursi L, Cancrini C, et al. (2003) Bruton's tyrosine kinase defect in dendritic cells from X-linked agammaglobulinaemia patients does not influence their differentiation, maturation and antigen-presenting cell function. Clin Exp Immunol 133: 115-122. (Pubitemid 36791949)
47. Jyonouchi H, Geng L, Toruner GA, Vinekar K, Feng D, et al. (2008) Monozygous twins with a microdeletion syndrome involving BTK, DDP1, and two other genes; evidence of intact dendritic cell development and TLR responses. Eur J Pediatr 167: 317-321. (Pubitemid 351238209)
48. Amoras AL, da Silva MT, Zollner RL, Kanegane H, Miyawaki T, et al. (2007) Expression of Fc gamma and complement receptors in monocytes of X-linked agammaglobulinaemia and common variable immunodeficiency patients. Clin Exp Immunol 150: 422-428. (Pubitemid 350098735)
49. Liu X, Zhan Z, Li D, Xu L, Ma F, et al. (2011) Intracellular MHC class II molecules promote TLR-triggered innate immune responses by maintaining activation of the kinase Btk. Nat Immunol 12: 416-424.
50. Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2: 725-734.
51. Hu X, Li WP, Meng C, Ivashkiv LB (2003) Inhibition of IFN-gamma signaling by glucocorticoids. J Immunol 170: 4833-4839.
52. Li X, Tupper JC, Bannerman DD, Winn RK, Rhodes CJ, et al. (2003) Phosphoinositide 3 kinase mediates Toll-like receptor 4-induced activation of NF-kappa B in endothelial cells. Infect Immun 71: 4414-4420. (Pubitemid 36919907)
53. Kitaura J, Asai K, Maeda-Yamamoto M, Kawakami Y, Kikkawa U, et al. (2000) Akt-dependent cytokine production in mast cells. J Exp Med 192: 729-740.
54. Mohammad DK, Nore BF, Hussain A, Gustafsson MO, Mohamed AJ, et al. (2013) Dual Phosphorylation of Btk by Akt/Protein Kinase B Provides Docking for 14-3-3zeta, Regulates Shuttling, and Attenuates both Tonic and Induced Signaling in B Cells. Mol Cell Biol 33: 3214-3226.
55. Takahashi-Tezuka M, Hibi M, Fujitani Y, Fukada T, Yamaguchi T, et al. (1997) Tec tyrosine kinase links the cytokine receptors to PI-3 kinase probably through JAK. Oncogene 14: 2273-2282. (Pubitemid 27260719)
56. Uckun F, Ozer Z, Vassilev A (2007) Bruton's tyrosine kinase prevents activation of the anti-apoptotic transcription factor STAT3 and promotes apoptosis in neoplastic B-cells and B-cell precursors exposed to oxidative stress. Br J Haematol 136: 574-589. (Pubitemid 46148194)
57. Ohmori Y, Hamilton TA (2001) Requirement for STAT1 in LPS-induced gene expression in macrophages. J Leukoc Biol 69: 598-604. (Pubitemid 32294845)
58. Rauh MJ, Ho V, Pereira C, Sham A, Sly LM, et al. (2005) SHIP represses the generation of alternatively activated macrophages. Immunity 23: 361-374. (Pubitemid 41443438)
59. Antignano F, Ibaraki M, Kim C, Ruschmann J, Zhang A, et al. (2010) SHIP is required for dendritic cell maturation. J Immunol 184: 2805-2813.
60. Weisser SB, McLarren KW, Voglmaier N, van Netten-Thomas CJ, Antov A, et al. (2011) Alternative activation of macrophages by IL-4 requires SHIP degradation. Eur J Immunol 41: 1742-1753.
61. Arranz A, Doxaki C, Vergadi E, Martinez de la Torre Y, Vaporidi K, et al. (2012) Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc Natl Acad Sci U S A 109: 9517-9522.
62. Xu F, Kang Y, Zhang H, Piao Z, Yin H, et al. (2013) Akt1-Mediated Regulation of Macrophage Polarization in a Murine Model of Staphylococcus aureus Pulmonary Infection. J Infect Dis 208: 528-538.
63. Taha RA, Minshall EM, Miotto D, Shimbara A, Luster A, et al. (1999) Eotaxin and monocyte chemotactic protein-4 mRNA expression in small airways of asthmatic and nonasthmatic individuals. J Allergy Clin Immunol 103: 476-483. (Pubitemid 29136302)
64. Kawakami Y, Inagaki N, Salek-Ardakani S, Kitaura J, Tanaka H, et al. (2006) Regulation of dendritic cell maturation and function by Bruton's tyrosine kinase via IL-10 and Stat3. Proc Natl Acad Sci U S A 103: 153-158. (Pubitemid 43076120)
65. Hata D, Kawakami Y, Inagaki N, Lantz CS, Kitamura T, et al. (1998) Involvement of Bruton's tyrosine kinase in FcepsilonRI-dependent mast cell degranulation and cytokine production. J Exp Med 187: 1235-1247. (Pubitemid 28189113)
66. Shabestari MS, Rezaei N (2008) Asthma and allergic rhinitis in a patient with BTK deficiency. J Investig Allergol Clin Immunol 18: 300-304. (Pubitemid 352031576)
67. Costa-Carvalho BT, Wandalsen GF, Pulici G, Aranda CS, Sole D (2011) Pulmonary complications in patients with antibody deficiency. Allergol Immunopathol (Madr) 39: 128-132.
68. D'Cruz OJ, Uckun FM (2013) Novel Bruton's tyrosine kinase inhibitors currently in development. Onco Targets Ther 6: 161-176.
69. Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, et al. (2010) The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci U S A 107: 13075-13080.
70. Byrne JC, Ní Gabhann J, Stacey K, Coffey BM, McCarthy E, et al. (2013) Bruton's Tyrosine Kinase Is Required for Apoptotic Cell Uptake via Regulating the Phosphorylation and Localization of Calreticulin. J Immunol In press.