Differential regulation of oxidative burst by distinct β-glucan- binding receptors and signaling pathways in human peripheral blood mononuclear cells

Glycobiology

Volumn 24, Issue 4, 2014, Pages 379-391

  Bose, Nandita ^a   Wurst, Lindsay R ^a   Chan, Anissa S H ^a   Dudney, Christine M ^a   Leroux, Megan L ^a   Danielson, Michael E ^a   Will, Paul M ^a   Nodland, Sonja E ^a   Patchen, Myra L ^a   Dalle Lucca, Jurandir J ^b   Lebeda, Frank J ^c   Vasilakos, John P ^a  

^a Biothera   (United States)

^b US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

^c U S ARMY MEDICAL RESEARCH AND MATERIEL COMMAND   (United States)

Author keywords

CR3; Dectin 1; human monocytes; oxidative burst; glucan

Indexed keywords

BETA GLUCAN; BETA GLUCAN BINDING RECEPTOR; CARBOHYDRATE BINDING PROTEIN; CELL SURFACE RECEPTOR; DECTIN 1; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; UNCLASSIFIED DRUG; CLEC7A PROTEIN, HUMAN; COMPLEMENT RECEPTOR; LECTIN;

ACTIN POLYMERIZATION; ARTICLE; CELL POPULATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; METABOLIC REGULATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RESPIRATORY BURST; METABOLISM; MONONUCLEAR CELL; SIGNAL TRANSDUCTION;

HUMANS; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; RECEPTORS, COMPLEMENT; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

EID: 84899013044     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwu005     Document Type: Article

References (57)

1. Adams EL, Rice PJ, Graves B, Ensley HE, Yu H, Brown GD, Gordon S, Monteiro MA, Papp-Szabo E, Lowman DW, et al. 2008. Differential highaffinity interaction of Dectin-1 with natural or synthetic glucans is dependent upon primary structure and is influenced by polymer chain length and sidechain branching. J Pharmacol Exp Ther. 325(1):115-123. (Pubitemid 351439173)
2. Berton G, Lowell CA. 1999. Integrin signalling in neutrophils and macrophages. Cell Signal. 11(9):621-635.
3. Bonvini E, Bougnoux P, Stevenson HC, Miller P, Hoffman T. 1984. Activation of the oxidative burst in human monocytes is associated with inhibition of methionine-dependent methylation of neutral lipids and phospholipids. J Clin Invest. 73(6):1629-1637. (Pubitemid 14084478)
4. Brown GD. 2005. Dectin-1: A signalling non-TLR pattern-recognition receptor. Nat Rev Immunol. 6(1):33-43.
5. Brown GD. 2006. Macrophage receptors and innate immunity: Insights from Dectin-1. Novartis Found Symp. 279:114-123.
6. Brown GD, Herre J, Williams DL, Willment JA, Marshall AS, Gordon S. 2003. Dectin-1 mediates the biological effects of β-glucans. J Exp Med. 197 (9):1119-1124. (Pubitemid 36570067)
7. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L,Wong SY, Gordon S. 2002. Dectin-1 is a major β-glucan receptor on macrophages. J Exp Med. 196(3):407-412. (Pubitemid 34875669)
8. Brown GD, Williams DL. 2009. 1,3-β-Glucans in innate immunity: Mammalian systems. In: Bacic A, Fincher GB, Stone BA, editors. Chemistry, Biochemistry, and Biology of 1-3-β-Glucans and Related Polysaccarides. New York, NY, USA: Academic Press. P. 579-619.
9. Brummer E, Morrison CJ, Stevens DA. 1985. Recombinant and natural gamma-interferon activation of macrophages in vitro: Different dose requirements for induction of killing activity against phagocytizable and nonpagocytizable fungi. Infect Immun 49(3):724-730. (Pubitemid 15021536)
10. Cain JA, Newman SL, Ross GD. 1987. Role of complement receptor type three and serum opsonins in the neutrophil response to yeast. Complement. 4 (2):75-86.
11. Calderone RA, Fonzi WA. 2001. Virulence factors of Candida albicans. Trends Microbiol. 9(7):327-335. (Pubitemid 32575277)
12. Chamilos G, Ganguly D, Lande R, Gregorio J, Meller S, Goldman WE, Gilliet M, Kontoyiannia DP. 2010. Generation of IL-23 producing dendritic cells (DCs) by airborne fungi regulates fungal pathogenicity via the induction of T (H)-17 responses. PLoS One. 5(9):e12955.
13. Deepe GS, Jr 1989. Blastomycosis. In: Immunology of the Fungal Diseases. Boca Raton, FL, USA: CRC Press. P. 139-163.
14. Dennehy KM, Ferwerda G, Faro-Trindade I, Pyz E, Willment JA, Taylor PR, Kerrigan A, Tsoni SV, Gordon S, Meyer-Wentrup F, et al. 2008. Syk kinase is required for collaborative cytokine production induced through Dectin-1 and Toll-like receptors. Eur J Immunol. 38(2):500-506.
15. Fuortes M, Melchior M, Han H, Lyon GJ, Nathan C. 1999. Role of the tyrosine kinase pyk2 in the integrin-dependent activation of human neutrophils by TNF. J Clin Invest. 104(3):327-335.
16. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM. 2003. Collaborative induction of inflammatory responses by Dectin-1 and Toll-like receptor 2. J Exp Med. 197(9):1107-1117. (Pubitemid 36570066)
17. Gantner BN, Simmons RM, Underhill DM. 2005. Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24 (6):1277-1286. (Pubitemid 40516610)
18. Geijtenbeek TB, Gringhuis SI. 2009. Signalling through C-Type lectin receptors: Shaping immune responses. Nat Rev Immunol. 9(7):465-479.
19. Goldman R, Ferber E, Meller R, Zor U. 1994. A role for reactive oxygen species in zymosan and β-glucan induced protein tyrosine phosphorylation and phospholipase A2 activation in murine macrophages. Biochim Biophys Acta. 1222(2):265-276. (Pubitemid 24213659)
20. Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, Wolf AJ, Bose N, Chan ASH, Magee AS, Danielson ME, et al. 2011. Activation of the innate immune receptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature. 472(7344):471-475.
21. Goodridge HS, Shimada T, Wolf AJ, Hsu YM, Becker CA, Lin X, Underhill DM. 2009. Differential use of CARD9 by Dectin-1 in macrophages and dendritic cells. J Immunol. 182(2):1146-1154.
22. Goodridge HS, Wolf AJ, Underhill DM. 2009. β-glucan recognition by the innate immune system. Immunol Rev. 230(1):38-50.
23. Henson PM. 1971. Interaction of cells with immune complexes: Adherence, release of constituents, and tissue injury. J Exp Med. 134(3):114-135.
24. Hernanz-Falcón P, Joffre O, Williams DL, Reis e Sousa C. 2009. Internalization of Dectin-1 terminates induction of inflammatory responses. Eur J Immunol. 39(2):507-513.5.
25. Herre J, Marshall AS, Caron E, Edwards AD, Williams DL, Schweighoffer E, Tybulewicz V, Reis e Sousa C, Gordon S, Brown GD. 2004. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood. 104 (13):4038-4045.
26. Kharazmi A, Nielsen H, Rechnitzer C, Bendtzen K. 1989. Interleukin 6 primes human neutrophil and monocyte oxidative burst response. Immunol Lett. 21 (2):177-184. (Pubitemid 19135912)
27. Lavigne LM, Albina JE, Reichner JS. 2006. β-glucan is a fungal determinant for adhesion-dependent human neutrophil functions. J Immunol. 177 (12):8667-8675. (Pubitemid 44893831)
28. Lee JS, Nauseef WM, Moeenrezakhanlou A, Sly LM, Noubir S, Leidal KG, Schlomann JM, Krystal G, Reiner NE. 2007. Monocyte p110α phosphatidylinositol 3-kinase regulates phagocytosis, the phagocyte oxidase, and cytokine production. J Leukoc Biol. 81(6):1548-1561. (Pubitemid 46827977)
29. Li B, Allendorf DJ, Hansen R, Marroquin J, Ding C, Cramer DE, Yan J. 2006. Yeast β-glucan amplifies phagocyte killing of iC3b-opsonized tumor cells via complement receptor 3-Syk-phosphatidylinositol 3-kinase pathway. J Immunol. 177(3):1661-1669. (Pubitemid 44092502)
30. Li B, Cramer D, Wagner S, Hansen R, King C, Kakar S, Ding C, Yan J. 2007. Yeast glucan particles activate murine resident macrophages to secrete proinflammatory cytokines via MyD88-And Syk kinase-dependent pathways. Clin Immunol. 124(3):170-181. (Pubitemid 47061522)
31. Li X, Hunter D, Morris J, Haskill JS, Earp HS. 1998. A calcium-dependent tyrosine kinase splice variant in human monocytes. Activation by a twostage process involving adherence and a subsequent intracellular signal. J Biol Chem. 273(16):9361-9364. (Pubitemid 28183013)
32. Liu R, Lioté F, Rose DM, Merz D, Terkeltaub R. 2004. Proline-rich tyrosine kinase 2 and Src kinase signaling transduce monosodium urate crystalinduced nitric oxide production and matrix metalloproteinase 3 expression in chondrocytes. Arthritis Rheum. 50(1):247-258. (Pubitemid 38087995)
33. Marakalala MJ, Kerrigan AM, Brown GD. 2011. Dectin-1: A role in antifungal defense and consequences of genetic polymorphisms in humans. Mamm Genome. 22(1-2):55-65.
34. Mayo LA, Curnutte JT. 1990. Kinetic microplate assay for superoxide production by neutrophils and other phagocytic cells. Methods Enzymol. 186:567-575. (Pubitemid 20279999)
35. Michalek M, Melican D, Brunke-Reese D, Langevin M, Lemerise K, Galbraith W, Patchen M, Mackin W. 1998. Activation of rat macrophages by Betafectin® PGG-glucan requires cross-linking of membrane receptors distinct from complement receptor three (CR3). J Leukoc Biol. 64 (3):337-344. (Pubitemid 28409240)
36. Mócsai A, Abram CL, Jakus Z, Hu Y, Lanier LL, Lowell CA. 2006. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nat Immunol. 7(12):1326-1333. (Pubitemid 46111254)
37. Mogensen TH. 2009. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 22(2):240-273.
38. Netea MG, Maródi L. 2010. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol. 31(9):346-353.
39. Palma AS, Feizi T, Zhang Y, Stoll MS, Lawon AM, Díaz-Rodriguez E, Campanero-Rhodes MA, Costa J, Gordon S, Brown GD, et al. 006. Ligands for the β-glucan receptor, Dectin-1, assigned using "designer" microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. J Biol Chem. 281(34):5771-5779.
40. Rogers NC, Slack EC, Edwards AD, Nolte MA, Schulz O, Schweighoffer E, Williams DL, Gordon S, Tybulewicz VL, Brown GD, et al. 2005. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity. 22(6):507-517. (Pubitemid 40545115)
41. Ross GD, Cain JA, Myones BL, Newman SL, Lachmann PJ. 1987. Specificity of membrane complement receptor type three (CR3) for β-glucans. Complement. 4(2):61-74.
42. Ross GD, Thompson RA,Walport MJ, Springer TA, Watson JV, Ward RH, Lida J, Newman SL, Harrison RA, Lachmann PJ. 1985. Characterization of patients with an increased susceptibility to bacterial infections and a genetic deficiency of leukocyte membrane complement receptor type 3 and the related membrane antigen LFA-1. Blood. 66(4):882-890. (Pubitemid 15242473)
43. Shah VB, Ozment-Skelton TR, Williams DL, Keshvara L. 2009. Vav1 and PI3K are required for phagocytosis of β-glucan and subsequent superoxide generation by microglia. Mol Immunol. 46(8-9):1845-1853.
44. Steele C, Marrero L, Swain S, Harmsen AG, Zheng M, Brown GD, Gordon S, Shellito JE, Kolls JK. 2003. Alveolar macrophage-mediated killing of Pneumocystis carinii f. sp. muris involves molecular recognition by the Dectin-1 β-glucan receptor. J Exp Med. 198(11):1677-1688. (Pubitemid 37494160)
45. Thompson IJ, Oyston PC, Williamson DE. 2010. Potential of the β-glucans to enhance innate resistance to biological agents. Expert Rev Anti Infect Ther. 8(3):339-352.
46. Thornton BP, Vetvicka V, Pitman M, Goldman RC, Ross GD. 1996. Analysis of the sugar specificity and molecular location of the β-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J Immunol. 156 (3):1235-1246.
47. Trial J, Birdsall HH, Hallum JA, Crane ML, Rodriguez-Barradas MC, de Jong AL, Krishnan B, Lacke CE, Figdor CG, Rossen RD. 1995. Phenotypic and functional changes in peripheral blood monocytes during progression of human immunodeficiency virus infection. Effects of soluble immune complexes, cytokines, subcellular particulates from apoptotic cells, and HIV-1-encoded proteins on monocytes phagocytic function, oxidative burst, transendothelial migration, and cell surface phenotype. J Clin Invest. 95 (4):1690-1701.
48. Ujita M, Nagayama H, Kanie S, Koike S, Ikeyama Y, Ozaki T, Okumura H. 2009. Carbohydrate binding specificity of recombinant human macrophage β-glucan receptor Dectin-1. Biosci Biotechnol Biochem. 73(1):237-240.
49. Underhill DM, Rossnagle E, Lowell CA, Simmons RM. 2005. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood. 106(7):2543-2550. (Pubitemid 41510832)
50. van Bruggen R, Drewniak A, Jansen M, van Houdt M, Roos D, Chapel H, Verhoeven AJ, Kulijpers TW. 2009. Complement receptor 3, not Dectin-1, is the major receptor on human neutrophils for β-glucan-bearing particles. Mol Immunol. 47(2-3):575-581.
51. Williams LM, Ridley AJ. 2000. Lipopolysaccharide induces actin reorganization and tyrosine phosphorylation of Pyk2 and paxillin in monocytes and macrophages. J Immunol. 164(4):2028-2036. (Pubitemid 30108760)
52. Willment JA, Gordon S, Brown GD. 2001. Characterization of the human β-glucan receptor and its alternatively spliced isoforms. J Biol Chem. 276 (47):43818-43823.
53. Willment JA, Marshall AS, Reid DM, Williams DL, Wong SY, Gordon S, Brown GD. 2005. The human β-glucan receptor is widely expressed and functionally equivalent to murine Dectin-1 on primary cells. Eur J Immunol. 35(5):1539-1547. (Pubitemid 40691434)
54. Xia Y, Ross GD. 1999. Generation of recombinant fragments of CD11b expressing the functional β-glucan-binding lectin site of CR3 (CD11b/CD18). J Immunol. 162(12):7285-7293. (Pubitemid 29277702)
55. Xu S, Gunawan M, Su IH, Lam KP. 2009. Activated dectin-1 localizes to lipid raft microdomains for signaling and activation of phagocytosis and cytokine production in dendritic cells. J Biol Chem. 284(33):22005-22011.
56. Xu S, Huo J, Lee KG, Kurosaki T, Lam KP. 2009. Phospholipase Cγ2 is critical for Dectin-1-mediated Ca2+ flux and cytokine production in dendritic cells. J Biol Chem. 284(11):7038-7046.
57. Yamamoto N, Takeshita K, Shichijo M, Kokubo T, Sato M, Nakashima K, Ishimori M, Nagai H, Li YF, Yura T, et al. 2003. The orally available spleen tyrosine kinase inhibitor 2-[7-(3,4-dimethoxyphenyl)-imidazo[1,2-c] pyrimidin-5-ylamino]nicotinamide dihydrochloride (BAY 61-3606) blocks antigen-induced airway inflammation in rodents. J Pharmacol Exp Ther. 306 (3):1174-1181.