Bruton's Tyrosine Kinase (BTK) and Vav1 Contribute to Dectin1-Dependent Phagocytosis of Candida albicans in Macrophages

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Strijbis, Karin ^a   Tafesse, Fikadu G ^a   Fairn, Gregory D ^b   Witte, Martin D ^a   Dougan, Stephanie K ^a   Watson, Nicki ^a   Spooner, Eric ^a   Esteban, Alexandre ^a   Vyas, Valmik K ^a   Fink, Gerald R ^a   Grinstein, Sergio ^b,c   Ploegh, Hidde L ^a  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRUTON TYROSINE KINASE; DECTIN 1; DIACYLGLYCEROL; F ACTIN; IBRUTINIB; PHOSPHATIDYLINOSITIDE; VAV PROTEIN; ZYMOSAN;

ANIMAL CELL; ARTICLE; CANDIDA ALBICANS; COLONY FORMING UNIT; CONTROLLED STUDY; ELECTRON MICROSCOPY; IMMUNE RESPONSE; IMMUNOPRECIPITATION; MACROPHAGE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; WESTERN BLOTTING;

ACTINS; ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CELL LINE; DIGLYCERIDES; HOMEODOMAIN PROTEINS; LECTINS, C-TYPE; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN-TYROSINE KINASES;

CANDIDA ALBICANS; MUS;

EID: 84879532977     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003446     Document Type: Article

References (55)

1. Cheng SC, Joosten LA, Kullberg BJ, Netea MG, (2012) Interplay between Candida albicans and the mammalian innate host defense. Infection and immunity 80: 1304-1313.
2. Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, et al. (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336: 1314-1317.
3. Herre J, Marshall AS, Caron E, Edwards AD, Williams DL, et al. (2004) Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104: 4038-4045.
4. Rogers NC, Slack EC, Edwards AD, Nolte MA, Schulz O, et al. (2005) Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22: 507-517.
5. Elsori DH, Yakubenko VP, Roome T, Thiagarajan PS, Bhattacharjee A, et al. (2011) Protein kinase Cdelta is a critical component of Dectin-1 signaling in primary human monocytes. Journal of leukocyte biology 90: 599-611.
6. Meyer-Wentrup F, Figdor CG, Ansems M, Brossart P, Wright MD, et al. (2007) Dectin-1 interaction with tetraspanin CD37 inhibits IL-6 production. Journal of immunology 178: 154-162.
7. Esteban A, Popp MW, Vyas VK, Strijbis K, Ploegh HL, et al. (2011) Fungal recognition is mediated by the association of dectin-1 and galectin-3 in macrophages. Proceedings of the National Academy of Sciences of the United States of America 108: 14270-14275.
8. Shin DM, Yang CS, Yuk JM, Lee JY, Kim KH, et al. (2008) Mycobacterium abscessus activates the macrophage innate immune response via a physical and functional interaction between TLR2 and dectin-1. Cellular microbiology 10: 1608-1621.
9. Botelho RJ, Grinstein S, (2011) Phagocytosis. Current biology: CB 21: R533-538.
10. Botelho RJ, Teruel M, Dierckman R, Anderson R, Wells A, et al. (2000) Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. The Journal of cell biology 151: 1353-1368.
11. Heinsbroek SE, Kamen LA, Taylor PR, Brown GD, Swanson J, et al. (2009) Actin and phosphoinositide recruitment to fully formed Candida albicans phagosomes in mouse macrophages. Journal of innate immunity 1: 244-253.
12. Fernandez-Arenas E, Bleck CK, Nombela C, Gil C, Griffiths G, et al. (2009) Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cellular microbiology 11: 560-589.
13. Wheeler RT, Fink GR, (2006) A drug-sensitive genetic network masks fungi from the immune system. PLoS pathogens 2: e35.
14. Grinstein S, (2010) Imaging signal transduction during phagocytosis: phospholipids, surface charge, and electrostatic interactions. American journal of physiology Cell physiology 299: C876-881.
15. Geczy T, Peach ML, El Kazzouli S, Sigano DM, Kang JH, et al. (2012) Molecular basis for failure of "atypical" C1 domain of Vav1 to bind diacylglycerol/phorbol ester. The Journal of biological chemistry 287: 13137-13158.
16. Maupin P, Pollard TD, (1983) Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation. The Journal of cell biology 96: 51-62.
17. 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. Proceedings of the National Academy of Sciences of the United States of America 107: 13075-13080.
18. Mueller H, Stadtmann A, Van Aken H, Hirsch E, Wang D, et al. (2010) Tyrosine kinase Btk regulates E-selectin-mediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) gamma2 and PI3Kgamma pathways. Blood 115: 3118-3127.
19. Ormsby T, Schlecker E, Ferdin J, Tessarz AS, Angelisova P, et al. (2011) Btk is a positive regulator in the TREM-1/DAP12 signaling pathway. Blood 118: 936-945.
20. MacCallum DM, Castillo L, Brown AJ, Gow NA, Odds FC, (2009) Early-expressed chemokines predict kidney immunopathology in experimental disseminated Candida albicans infections. PloS one 4: e6420.
21. Hornstein I, Alcover A, Katzav S, (2004) Vav proteins, masters of the world of cytoskeleton organization. Cellular signalling 16: 1-11.
22. Jongstra-Bilen J, Puig Cano A, Hasija M, Xiao H, Smith CI, et al. (2008) Dual functions of Bruton's tyrosine kinase and Tec kinase during Fcgamma receptor-induced signaling and phagocytosis. Journal of immunology 181: 288-298.
23. Olsson S, Sundler R, (2007) The macrophage beta-glucan receptor mediates arachidonate release induced by zymosan: essential role for Src family kinases. Molecular immunology 44: 1509-1515.
24. Olsson S, Sundler R, (2006) Different roles for non-receptor tyrosine kinases in arachidonate release induced by zymosan and Staphylococcus aureus in macrophages. Journal of inflammation 3: 8.
25. Li X, Utomo A, Cullere X, Choi MM, Milner DA Jr, et al. (2011) The beta-glucan receptor Dectin-1 activates the integrin Mac-1 in neutrophils via Vav protein signaling to promote Candida albicans clearance. Cell host & microbe 10: 603-615.
26. Guinamard R, Fougereau M, Seckinger P, (1997) The SH3 domain of Bruton's tyrosine kinase interacts with Vav, Sam68 and EWS. Scandinavian journal of immunology 45: 587-595.
27. Deckert M, Tartare-Deckert S, Couture C, Mustelin T, Altman A, (1996) Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product. Immunity 5: 591-604.
28. Wheeler RT, Kombe D, Agarwala SD, Fink GR, (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS pathogens 4: e1000227.
29. Gantner BN, Simmons RM, Underhill DM, (2005) Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. The EMBO journal 24: 1277-1286.
30. Bohdanowicz M, Cosio G, Backer JM, Grinstein S, (2010) Class I and class III phosphoinositide 3-kinases are required for actin polymerization that propels phagosomes. The Journal of cell biology 191: 999-1012.
31. Sakai N, Sasaki K, Ikegaki N, Shirai Y, Ono Y, et al. (1997) Direct visualization of the translocation of the gamma-subspecies of protein kinase C in living cells using fusion proteins with green fluorescent protein. The Journal of cell biology 139: 1465-1476.
32. Shirai Y, Sakai N, Saito N, (1998) Subspecies-specific targeting mechanism of protein kinase C. Japanese journal of pharmacology 78: 411-417.
33. Steinberg SF, (2008) Structural basis of protein kinase C isoform function. Physiological reviews 88: 1341-1378.
34. Larsen EC, Ueyama T, Brannock PM, Shirai Y, Saito N, et al. (2002) A role for PKC-epsilon in Fc gammaR-mediated phagocytosis by RAW 264.7 cells. The Journal of cell biology 159: 939-944.
35. Larsen EC, DiGennaro JA, Saito N, Mehta S, Loegering DJ, et al. (2000) Differential requirement for classic and novel PKC isoforms in respiratory burst and phagocytosis in RAW 264.7 cells. Journal of immunology 165: 2809-2817.
36. Khan WN, Alt FW, Gerstein RM, Malynn BA, Larsson I, et al. (1995) Defective B cell development and function in Btk-deficient mice. Immunity 3: 283-299.
37. Ellmeier W, Jung S, Sunshine MJ, Hatam F, Xu Y, et al. (2000) Severe B cell deficiency in mice lacking the tec kinase family members Tec and Btk. The Journal of experimental medicine 192: 1611-1624.
38. Tarakhovsky A, Turner M, Schaal S, Mee PJ, Duddy LP, et al. (1995) Defective antigen receptor-mediated proliferation of B and T cells in the absence of Vav. Nature 374: 467-470.
39. Turner M, Mee PJ, Walters AE, Quinn ME, Mellor AL, et al. (1997) A requirement for the Rho-family GTP exchange factor Vav in positive and negative selection of thymocytes. Immunity 7: 451-460.
40. Liao F, Shin HS, Rhee SG, (1992) Tyrosine phosphorylation of phospholipase C-gamma 1 induced by cross-linking of the high-affinity or low-affinity Fc receptor for IgG in U937 cells. Proceedings of the National Academy of Sciences of the United States of America 89: 3659-3663.
41. Hall AB, Gakidis MA, Glogauer M, Wilsbacher JL, Gao S, et al. (2006) Requirements for Vav guanine nucleotide exchange factors and Rho GTPases in FcgammaR- and complement-mediated phagocytosis. Immunity 24: 305-316.
42. Utomo A, Cullere X, Glogauer M, Swat W, Mayadas TN, (2006) Vav proteins in neutrophils are required for FcgammaR-mediated signaling to Rac GTPases and nicotinamide adenine dinucleotide phosphate oxidase component p40(phox). Journal of immunology 177: 6388-6397.
43. Shah VB, Ozment-Skelton TR, Williams DL, Keshvara L, (2009) Vav1 and PI3K are required for phagocytosis of beta-glucan and subsequent superoxide generation by microglia. Molecular immunology 46: 1845-1853.
44. Lilley BN, Ploegh HL, (2005) Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proceedings of the National Academy of Sciences of the United States of America 102: 14296-14301.
45. Tam JM, Mansour MK, Khan NS, Yoder NC, Vyas JM, (2012) Use of fungal derived polysaccharide-conjugated particles to probe Dectin-1 responses in innate immunity. Integrative biology: quantitative biosciences from nano to macro 4: 220-227.
46. Flannagan RS, Grinstein S, (2010) The application of fluorescent probes for the analysis of lipid dynamics during phagocytosis. Methods in molecular biology 591: 121-134.
47. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Canadian journal of biochemistry and physiology 37: 911-917.
48. Preiss J, Loomis CR, Bishop WR, Stein R, Niedel JE, et al. (1986) Quantitative measurement of sn-1,2-diacylglycerols present in platelets, hepatocytes, and ras- and sis-transformed normal rat kidney cells. The Journal of biological chemistry 261: 8597-8600.
49. Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, et al. (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nature immunology 8: 31-38.
50. Stauffer TP, Ahn S, Meyer T, (1998) Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Current biology: CB 8: 343-346.
51. Komander D, Fairservice A, Deak M, Kular GS, Prescott AR, et al. (2004) Structural insights into the regulation of PDK1 by phosphoinositides and inositol phosphates. The EMBO journal 23: 3918-3928.
52. Varnai P, Rother KI, Balla T, (1999) Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. The Journal of biological chemistry 274: 10983-10989.
53. Tse SM, Mason D, Botelho RJ, Chiu B, Reyland M, et al. (2005) Accumulation of diacylglycerol in the Chlamydia inclusion vacuole: possible role in the inhibition of host cell apoptosis. The Journal of biological chemistry 280: 25210-25215.
54. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nature methods 5: 605-607.
55. Shirai Y, Kashiwagi K, Yagi K, Sakai N, Saito N, (1998) Distinct effects of fatty acids on translocation of gamma- and epsilon-subspecies of protein kinase C. The Journal of cell biology 143: 511-521.