Cell intrinsic galectin-3 attenuates neutrophil ROS-dependent killing of Candida by modulating CR3 downstream syk activation

Frontiers in Immunology

Volumn 8, Issue FEB, 2017, Pages

  Wu, Sheng Yang ^a   Huang, Juin Hua ^a   Chen, Wen Yu ^a   Chan, Yi Chen ^b   Lin, Chun Hung ^b   Chen, Yee Chun ^c   Liu, Fu Tong ^d   Wu Hsieh, Betty A ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

Candida albicans; Galectin 3; M2 macrophage; Monocyte dendritic cell recruitment; Neutrophil; Reactive oxygen species; Syk kinase; TD139

Indexed keywords

CYTOSOL RECEPTOR; GALECTIN 3; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE;

ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL ISOLATION; DOWN REGULATION; FUNGICIDAL ACTIVITY; FUNGUS ISOLATION; GENE SILENCING; HUMAN; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KIDNEY CELL; MACROPHAGE; MOUSE; MYCOSIS; NONHUMAN; PROTEIN EXPRESSION;

EID: 85014329434     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00048     Document Type: Article

References (53)

1. Dumic J, Dabelic S, Flogel M. Galectin-3: an open-ended story. Biochim Biophys Acta (2006) 1760(4):616-35. doi: 10.1016/j.bbagen.2005.12.020
2. Rabinovich GA, Toscano MA. Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol (2009) 9(5):338-52. doi:10.1038/nri2536
3. Sundblad V, Croci DO, Rabinovich GA. Regulated expression of galectin-3, a multifunctional glycan-binding protein, in haematopoietic and non-haematopoietic tissues. Histol Histopathol (2011) 26(2):247-65. doi:10.14670/HH-26.247
4. Alves CM, Silva DA, Azzolini AE, Marzocchi-Machado CM, Carvalho JV, Pajuaba AC, et al. Galectin-3 plays a modulatory role in the life span and activation of murine neutrophils during early Toxoplasma gondii infection. Immunobiology (2010) 215(6):475-85. doi:10.1016/j.imbio.2009.08.001
5. Chen HY, Fermin A, Vardhana S, Weng IC, Lo KF, Chang EY, et al. Galectin-3 negatively regulates TCR-mediated CD4+ T-cell activation at the immunological synapse. Proc Natl Acad Sci U S A (2009) 106(34):14496-501. doi:10.1073/pnas.0903497106
6. Ferraz LC, Bernardes ES, Oliveira AF, Ruas LP, Fermino ML, Soares SG, et al. Lack of galectin-3 alters the balance of innate immune cytokines and confers resistance to Rhodococcus equi infection. Eur J Immunol (2008) 38(10):2762-75. doi:10.1002/eji.200737986
7. Liu W, Hsu DK, Chen HY, Yang RY, Carraway KL III, IsseroffRR, et al. Galectin-3 regulates intracellular trafficking of EGFR through Alix and promotes keratinocyte migration. J Invest Dermatol (2012) 132(12):2828-37. doi:10.1038/jid.2012.211
8. Nakahara S, Oka N, Raz A. On the role of galectin-3 in cancer apoptosis. Apoptosis (2005) 10(2):267-75. doi:10.1007/s10495-005-0801-y
9. Esteban A, Popp MW, Vyas VK, Strijbis K, Ploegh HL, Fink GR. Fungal recognition is mediated by the association of dectin-1 and galectin-3 in macrophages. Proc Natl Acad Sci U S A (2011) 108(34):14270-5. doi:10.1073/pnas.1111415108
10. Elad-Sfadia G, Haklai R, Balan E, Kloog Y. Galectin-3 augments K-Ras activation and triggers a Ras signal that attenuates ERK but not phosphoinositide 3-kinase activity. J Biol Chem (2004) 279(33):34922-30. doi:10.1074/jbc. M312697200
11. Li Y, Liu L, Niu Y, Feng J, Sun Y, Kong X, et al. Modified apple polysaccharide prevents against tumorigenesis in a mouse model of colitis-associated colon cancer: role of galectin-3 and apoptosis in cancer prevention. Eur J Nutr (2012) 51(1):107-17. doi:10.1007/s00394-011-0194-3
12. Harazono Y, Kho DH, Balan V, Nakajima K, Zhang T, Hogan V, et al. Galectin-3 leads to attenuation of apoptosis through Bax heterodimerization in human thyroid carcinoma cells. Oncotarget (2014) 5(20):9992-10001. doi:10.18632/oncotarget.2486
13. Farnworth SL, Henderson NC, Mackinnon AC, Atkinson KM, Wilkinson T, Dhaliwal K, et al. Galectin-3 reduces the severity of pneumococcal pneumonia by augmenting neutrophil function. Am J Pathol (2008) 172(2):395-405. doi:10.2353/ajpath.2008.070870
14. Linden JR, Kunkel D, Laforce-Nesbitt SS, Bliss JM. The role of galectin-3 in phagocytosis of Candida albicans and Candida parapsilosis by human neutrophils. Cell Microbiol (2013) 15(7):1127-42. doi:10.1111/cmi.12103
15. Nieminen J, St-Pierre C, Sato S. Galectin-3 interacts with naive and primed neutrophils, inducing innate immune responses. J Leukoc Biol (2005) 78(5):1127-35. doi:10.1189/jlb.1204702
16. Gow NA, van de Veerdonk FL, Brown AJ, Netea MG. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol (2012) 10(2):112-22. doi:10.1038/nrmicro2711
17. Antachopoulos C, Walsh TJ, Roilides E. Fungal infections in primary immunodeficiencies. Eur J Pediatr (2007) 166(11):1099-117. doi:10.1007/s00431-007-0527-7
18. Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, Olyaei AJ, et al. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis (2009) 48(12):1695-703. doi:10.1086/599039
19. Lionakis MS, Netea MG. Candida and host determinants of susceptibility to invasive candidiasis. PLoS Pathog (2013) 9(1):e1003079. doi:10.1371/journal.ppat.1003079
20. Kullberg BJ, Arendrup MC. Invasive candidiasis. N Engl J Med (2015) 373(15):1445-56. doi:10.1056/NEJMra1315399
21. Chen PY, Chuang YC, Wang JT, Sheng WH, Yu CJ, Chu CC, et al. Comparison of epidemiology and treatment outcome of patients with candidemia at a teaching hospital in Northern Taiwan, in 2002 and 2010. J Microbiol Immunol Infect (2014) 47(2):95-103. doi:10.1016/j.jmii.2012.08.025
22. Lionakis MS, Lim JK, Lee CC, Murphy PM. Organ-specific innate immune responses in a mouse model of invasive candidiasis. J Innate Immun (2011) 3(2):180-99. doi:10.1159/000321157
23. Aratani Y, Kura F, Watanabe H, Akagawa H, Takano Y, Suzuki K, et al. Critical role of myeloperoxidase and nicotinamide adenine dinucleotide phosphate-oxidase in high-burden systemic infection of mice with Candida albicans. J Infect Dis (2002) 185(12):1833-7. doi:10.1086/340635
24. Koh AY, Kohler JR, Coggshall KT, Van Rooijen N, Pier GB. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog (2008) 4(2):e35. doi:10.1371/journal.ppat.0040035
25. Chao CC, Hsu PC, Jen CF, Chen IH, Wang CH, Chan HC, et al. Zebrafish as a model host for Candida albicans infection. Infect Immun (2010) 78(6):2512-21. doi:10.1128/IAI.01293-09
26. Maqbool M, Vidyadaran S, George E, Ramasamy R. Optimisation of laboratory procedures for isolating human peripheral blood derived neutrophils. Med J Malaysia (2011) 66(4):296-9.
27. Hsieh TJ, Lin HY, Tu Z, Lin TC, Wu SC, Tseng YY, et al. Dual thio-digalactoside-binding modes of human galectins as the structural basis for the design of potent and selective inhibitors. Sci Rep (2016) 6:29457. doi:10.1038/srep29457
28. Vonk AG, Netea MG, Kullberg BJ. Phagocytosis and intracellular killing of Candida albicans by murine polymorphonuclear neutrophils. Methods Mol Biol (2012) 845:277-87. doi:10.1007/978-1-61779-539-8_18
29. Novak R, Dabelic S, Dumic J. Galectin-1 and galectin-3 expression profiles in classically and alternatively activated human macrophages. Biochim Biophys Acta (2012) 1820(9):1383-90. doi:10.1016/j.bbagen.2011.11.014
30. Shan M, Gentile M, Yeiser JR, Walland AC, Bornstein VU, Chen K, et al. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science (2013) 342(6157):447-53. doi:10.1126/science.1237910
31. Gazendam RP, van Hamme JL, Tool AT, van Houdt M, Verkuijlen PJ, Herbst M, et al. Two independent killing mechanisms of Candida albicans by human neutrophils: evidence from innate immunity defects. Blood (2014) 124(4):590-7. doi:10.1182/blood-2014-01-551473
32. James RE, Hillis J, Adorjan I, Gration B, Mundim MV, Iqbal AJ, et al. Loss of galectin-3 decreases the number of immune cells in the subventricular zone and restores proliferation in a viral model of multiple sclerosis. Glia (2016) 64(1):105-21. doi:10.1002/glia.22906
33. Nieminen J, St-Pierre C, Bhaumik P, Poirier F, Sato S. Role of galectin-3 in leukocyte recruitment in a murine model of lung infection by Streptococcus pneumoniae. J Immunol (2008) 180(4):2466-73. doi:10.4049/jimmunol.180.4.2466
34. Lionakis MS, Swamydas M, Fischer BG, Plantinga TS, Johnson MD, Jaeger M, et al. CX3CR1-dependent renal macrophage survival promotes Candida control and host survival. J Clin Invest (2013) 123(12):5035-51. doi:10.1172/JCI71307
35. Chen Y, Mendoza S, Davis-Gorman G, Cohen Z, Gonzales R, Tuttle H, et al. Neutrophil activation by murine retroviral infection during chronic ethanol consumption. Alcohol Alcohol (2003) 38(2):109-14. doi:10.1093/alcalc/agg049
36. Bain JM, Louw J, Lewis LE, Okai B, Walls CA, Ballou ER, et al. Candida albicans hypha formation and mannan masking of beta-glucan inhibit macrophage phagosome maturation. MBio (2014) 5(6):e01874. doi:10.1128/mBio.01874-14
37. ten Oever J, Giamarellos-Bourboulis EJ, van de Veerdonk FL, Stelma FF, Simon A, Janssen M, et al. Circulating galectin-3 in infections and non-infectious inflammatory diseases. Eur J Clin Microbiol Infect Dis (2013) 32(12):1605-10. doi:10.1007/s10096-013-1919-4
38. Mocsai A, Ruland J, Tybulewicz VL. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol (2010) 10(6):387-402. doi:10.1038/nri2765
39. Pineda MA, Cuervo H, Fresno M, Soto M, Bonay P. Lack of galectin-3 prevents cardiac fibrosis and effective immune responses in a murine model of Trypanosoma cruzi infection. J Infect Dis (2015) 212(7):1160-71. doi:10.1093/infdis/jiv185
40. Lionakis MS, Fischer BG, Lim JK, Swamydas M, Wan W, Richard Lee CC, et al. Chemokine receptor Ccr1 drives neutrophil-mediated kidney immunopathology and mortality in invasive candidiasis. PLoS Pathog (2012) 8(8):e1002865. doi:10.1371/journal.ppat.1002865
41. Majer O, Bourgeois C, Zwolanek F, Lassnig C, Kerjaschki D, Mack M, et al. Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during Candida infections. PLoS Pathog (2012) 8(7):e1002811. doi:10.1371/journal.ppat.1002811
42. Qian Q, Jutila MA, Van Rooijen N, Cutler JE. Elimination of mouse splenic macrophages correlates with increased susceptibility to experimental disseminated candidiasis. J Immunol (1994) 152(10):5000-8.
43. Ngo LY, Kasahara S, Kumasaka DK, Knoblaugh SE, Jhingran A, Hohl TM. Inflammatory monocytes mediate early and organ-specific innate defense during systemic candidiasis. J Infect Dis (2014) 209(1):109-19. doi:10.1093/infdis/jit413
44. Wirnsberger G, Zwolanek F, Asaoka T, Kozieradzki I, Tortola L, Wimmer RA, et al. Inhibition of CBLB protects from lethal Candida albicans sepsis. Nat Med (2016) 22(8):915-23. doi:10.1038/nm.4134
45. Whitney PG, Bar E, Osorio F, Rogers NC, Schraml BU, Deddouche S, et al. Syk signaling in dendritic cells orchestrates innate resistance to systemic fungal infection. PLoS Pathog (2014) 10(7):e1004276. doi:10.1371/journal.ppat.1004276
46. Bar E, Whitney PG, Moor K, Reis e Sousa C, LeibundGut-Landmann S. IL-17 regulates systemic fungal immunity by controlling the functional competence of NK cells. Immunity (2014) 40(1):117-27. doi:10.1016/j.immuni.2013.12.002
47. MacKinnon AC, Farnworth SL, Hodkinson PS, Henderson NC, Atkinson KM, Leffler H, et al. Regulation of alternative macrophage activation by galectin-3. J Immunol (2008) 180(4):2650-8. doi:10.4049/jimmunol.180.4.2650
48. Corna G, Campana L, Pignatti E, Castiglioni A, Tagliafico E, Bosurgi L, et al. Polarization dictates iron handling by inflammatory and alternatively activated macrophages. Haematologica (2010) 95(11):1814-22. doi:10.3324/haematol.2010.023879
49. Linden JR, De Paepe ME, Laforce-Nesbitt SS, Bliss JM. Galectin-3 plays an important role in protection against disseminated candidiasis. Med Mycol (2013) 51(6):641-51. doi:10.3109/13693786.2013.770607
50. Nilsson U, Leffler H, Mukhopadhyay B, Rajput V, Inventor; Galecto Biotech Ab, Assignee. Galectoside Inhibitors of Galectins. US patent 9353141 (2016).
51. Mackinnon AC, Gibbons MA, Farnworth SL, Leffler H, Nilsson UJ, Delaine T, et al. Regulation of transforming growth factor-beta1-driven lung fibrosis by galectin-3. Am J Respir Crit Care Med (2012) 185(5):537-46. doi:10.1164/rccm.201106-0965OC
52. Volarevic V, Milovanovic M, Ljujic B, Pejnovic N, Arsenijevic N, Nilsson U, et al. Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology (2012) 55(6):1954-64. doi:10.1002/hep.25542
53. Saksida T, Nikolic I, Vujicic M, Nilsson UJ, Leffler H, Lukic ML, et al. Galectin-3 deficiency protects pancreatic islet cells from cytokine-triggered apoptosis in vitro. J Cell Physiol (2013) 228(7):1568-76. doi:10.1002/jcp.24318