CARD9-Dependent Neutrophil Recruitment Protects against Fungal Invasion of the Central Nervous System

PLoS Pathogens

Volumn 11, Issue 12, 2015, Pages

  Drummond, Rebecca A ^a   Collar, Amanda L ^a   Swamydas, Muthulekha ^a   Rodriguez, Carlos A ^b   Lim, Jean K ^b   Mendez, Laura M ^c   Fink, Danielle L ^c   Hsu, Amy P ^a   Zhai, Bing ^d   Karauzum, Hatice ^a   Mikelis, Constantinos M ^e   Rose, Stacey R ^a   Ferre, Elise M N ^a   Yockey, Lynne ^a   Lemberg, Kimberly ^f   Kuehn, Hye Sun ^f   Rosenzweig, Sergio D ^f   Lin, Xin ^g   Chittiboina, Prashant ^h   Datta, Sandip K ^a   Belhorn, Thomas H ⁱ   Weimer, Eric T ⁱ   Hernandez, Michelle L ⁱ   Hohl, Tobias M ^d   Kuhns, Douglas B ^c   Lionakis, Michail S ^a   more..

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^h NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

ⁱ UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARD9 PROTEIN; CHEMOATTRACTANT; CHEMOKINE; FLUCONAZOLE; INTERLEUKIN 8; IONOMYCIN; LIPOCORTIN 5; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CARD9 PROTEIN, HUMAN; CARD9 PROTEIN, MOUSE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN;

7-AAD ASSAY; ARTICLE; CANDIDIASIS; CELL ADHESION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLUORESCENCE ACTIVATED CELL SORTING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MENINGOENCEPHALITIS; MISSENSE MUTATION; NEUTROPENIA; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OSTEOMYELITIS; PARASITE LOAD; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS INFECTION; WESTERN BLOTTING; ANIMAL; DEFICIENCY; FEMALE; FLOW CYTOMETRY; IMMUNE DEFICIENCY; IMMUNOLOGY; KNOCKOUT MOUSE; MICROBIOLOGY; MOUSE;

ANIMALS; BLOTTING, WESTERN; CANDIDIASIS; CARD SIGNALING ADAPTOR PROTEINS; CENTRAL NERVOUS SYSTEM INFECTIONS; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION;

EID: 84953220467     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005293     Document Type: Article

References (43)

1. Brown GD, Denning DW, Gow NAR, Levitz SM, Netea MG, White TC, Hidden Killers: Human Fungal Infections. Sci Transl Med. 2012;4(165):165rv13. doi: 10.1126/scitranslmed.3004404 23253612
2. Lionakis MS, Netea MG, Holland SM, Mendelian Genetics of Human Susceptibility to Fungal Infection. Cold Spring Harbor Perspect Med. 2014;4(6).
3. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, et al. Multistate Point-Prevalence Survey of Health Care–Associated Infections. N Engl J Med. 2014;370(13):1198–208. doi: 10.1056/NEJMoa1306801 24670166
4. Hardison SE, Brown GD, C-type lectin receptors orchestrate antifungal immunity. Nat Immunol. 2012;13(9):817–22. doi: 10.1038/ni.2369 22910394
5. Drummond RA, Saijo S, Iwakura Y, Brown GD, The role of Syk/CARD9 coupled C-type lectins in antifungal immunity. Euro J Immunol. 2011;41(2):276–81.
6. Gross O, Gewies A, Finger K, Schafer M, Sparwasser T, Peschel C, et al. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature. 2006;442(7103):651–6. 16862125
7. Drewniak A, Gazendam RP, Tool ATJ, van Houdt M, Jansen MH, van Hamme JL, et al. Invasive fungal infection and impaired neutrophil killing in human CARD9 deficiency. Blood. 2013;121(13):2385–92. doi: 10.1182/blood-2012-08-450551 23335372
8. Glocker EO, Hennigs A, Nabavi M, Schaffer AA, Woellner C, Salzer U, et al. A Homozygous CARD9 Mutation in a Family with Susceptibility to Fungal Infections. N Engl J Med. 2009;361(18):1727–35. doi: 10.1056/NEJMoa0810719 19864672
9. Lanternier F, Mahdaviani SA, Barbati E, Chaussade H, Koumar Y, Levy R, et al. Inherited CARD9 deficiency in otherwise healthy children and adults with Candida species–induced meningoencephalitis, colitis, or both. J Allergy Clin Immunol. 2015;135(6):1558–68. doi: 10.1016/j.jaci.2014.12.1930 25702837
10. Lanternier F, Barbati E, Meinzer U, Liu L, Pedergnana V, Migaud M, et al. Inherited CARD9 Deficiency in 2 Unrelated Patients With Invasive Exophiala Infection. J Infect Dis. 2014;211(8):1241–50. doi: 10.1093/infdis/jiu412 25057046
11. Wang X, Wang W, Lin Z, Wang X, Li T, Yu J, et al. CARD9 mutations linked to subcutaneous phaeohyphomycosis and TH17 cell deficiencies. J Allergy Clin Immunol. 2014;133(3):905–8.e3. doi: 10.1016/j.jaci.2013.09.033 24231284
12. Gavino C, Cotter A, Lichtenstein D, Lejtenyi D, Fortin C, Legault C, et al. CARD9 Deficiency and Spontaneous Central Nervous System Candidiasis: Complete Clinical Remission With GM-CSF Therapy. Clin Infect Dis. 2014;59(1):81–4. doi: 10.1093/cid/ciu215 24704721
13. Lanternier F, Pathan S, Vincent QB, Liu L, Cypowyj S, Prando C, et al. Deep Dermatophytosis and Inherited CARD9 Deficiency. N Engl J Med. 2013;369(18):1704–14. doi: 10.1056/NEJMoa1208487 24131138
14. Liang P, Wang X, Wang R, Wan Z, Han W, Li R, CARD9 Deficiencies Linked to Impaired Neutrophil Functions Against Phialophora verrucosa. Mycopathologia. 2015:1–11.
15. Gazendam RP, van Hamme JL, Tool ATJ, van Houdt M, Verkuijlen PJJH, 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 24948657
16. Rieber N, Singh A, Öz H, Carevic M, Bouzani M, Amich J, et al. Pathogenic Fungi Regulate Immunity by Inducing Neutrophilic Myeloid-Derived Suppressor Cells. Cell Host Microbe. 2015;17(4):507–14. doi: 10.1016/j.chom.2015.02.007 25771792
17. Grumach A, de Queiroz-Telles F, Migaud M, Lanternier F, Filho N, Palma SU, et al. A Homozygous CARD9 Mutation in a Brazilian Patient with Deep Dermatophytosis. J Clin Immunol. 2015:1–5.
18. Herbst M, Gazendam R, Reimnitz D, Sawalle-Belohradsky J, Groll A, Schlegel P-G, et al. Chronic Candida albicans Meningitis in a 4-Year-Old Girl with a Homozygous Mutation in the CARD9 Gene (Q295X). Pediatr Infect Dis J. 2015
19. Lionakis MS, New insights into innate immune control of systemic candidiasis. Med Mycol. 2014;52(6):555–64. doi: 10.1093/mmy/myu029 25023483
20. Kircher M, Witten DM, Jain P, O'Roak BJ, Cooper GM, Shendure J, A general framework for estimating the relative pathogenicity of human genetic variants. Nat Genet. 2014;46(3):310–5. doi: 10.1038/ng.2892 24487276
21. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7(4):248–9. doi: 10.1038/nmeth0410-248 20354512
22. 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 24177428
23. Brown GD, Innate Antifungal Immunity: The Key Role of Phagocytes. Ann Review Immunol. 2010(1): doi: 10.1146/annurev-immunol-030409-101229
24. Lionakis MS, Lim JK, Lee CCR, 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 21063074
25. 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 23300452
26. Geers TA, Gordon SM, Clinical Significance of Candida Species Isolated from Cerebrospinal Fluid Following Neurosurgery. Clin Infect Dis. 1999;28(5):1139–47. 10452649
27. Nguyen MH, Yu VL, Meningitis Caused by Candida Species: An Emerging Problem in Neurosurgical Patients. Clin Infect Dis. 1995;21(2):323–7. 8562739
28. Nordstrom L, Oistamo S, Olmebring F, Candida Meningoencephalitis Treated with 5-Fluorocytosine Scand J Infect Dis. 1977;9(1):63–4. 841284
29. Sugarman B, Massanari R, Candida meningitis in patients with CSF shunts. Arch Neurol. 1980;37(3):180–1. 6766718
30. López-Cortés LF, Cruz-Ruiz M, Gómez-Mateos J, Viciana-Fernandez P, Martinez-Marcos FJ, Pachón J, Interleukin-8 in Cerebrospinal Fluid from Patients with Meningitis of Different Etiologies: Its Possible Role as Neutrophil Chemotactic Factor. J Infect Dis. 1995;172(2):581–4. 7622911
31. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE, Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol. 2008;83(1):64–70. 17884993
32. Lionakis MS, Fischer BG, Lim JK, Swamydas M, Wan W, Richard Lee C-C, 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 22916017
33. Whibley N, Jaycox JR, Reid D, Garg AV, Taylor JA, Clancy CJ, et al. Delinking CARD9 and IL-17: CARD9 Protects against Candida tropicalis Infection through a TNF-α–Dependent, IL-17–Independent Mechanism. J Immunol. 2015: doi: 10.4049/jimmunol.1500870 26566677
34. Bian Z, Guo Y, Ha B, Zen K, Liu Y, Regulation of the Inflammatory Response: Enhancing Neutrophil Infiltration under Chronic Inflammatory Conditions. J Immunol. 2012;188(2):844–53. doi: 10.4049/jimmunol.1101736 22156344
35. Lo U, Selvaraj V, Plane JM, Chechneva OV, Otsu K, Deng W, p38 alpha (MAPK14) critically regulates the immunological response and the production of specific cytokines and chemokines in astrocytes. Sci Rep. 2014;4: doi: 10.1038/srep07405 25502009
36. Kremlev SG, Roberts RL, Palmer C, Differential expression of chemokines and chemokine receptors during microglial activation and inhibition. J Neuroimmunol. 2004;149(1–2):1–9. 15020059
37. Omari KM, John GR, Sealfon SC, Raine CS, CXC chemokine receptors on human oligodendrocytes: implications for multiple sclerosis. Brain. 2005;128(5):1003–15.
38. Jhingran A, Kasahara S, Shepardson KM, Junecko BAF, Heung LJ, Kumasaka DK, et al. Compartment-Specific and Sequential Role of MyD88 and CARD9 in Chemokine Induction and Innate Defense during Respiratory Fungal Infection. PLoS Pathog. 2015;11(1):e1004589. doi: 10.1371/journal.ppat.1004589 25621893
39. del Pozo MM, Bermejo F, Molina JA, de la Fuente EC, Martinez-Martin P, Benito-Leon J, Chronic neutrophilic meningitis caused by Candida albicans. Neurologia 1998;13(7):362–6. 9810800
40. Zwijnenburg PJG, de Bie HMA, Roord JJ, van der Poll T, van Furth AM, Chemotactic activity of CXCL5 in cerebrospinal fluid of children with bacterial meningitis. J Neuroimmunol. 2003;145(1–2):148–53. 14644041
41. Hsu Y-MS, Zhang Y, You Y, Wang D, Li H, Duramad O, et al. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat Immunol. 2007;8(2):198–205. 17187069
42. Jhingran A, Mar KB, Kumasaka DK, Knoblaugh SE, Ngo LY, Segal BH, et al. Tracing Conidial Fate and Measuring Host Cell Antifungal Activity Using a Reporter of Microbial Viability in the Lung. Cell reports. 2012;2(6):1762–73. doi: 10.1016/j.celrep.2012.10.026 23200858
43. Swamydas M, Lionakis MS, Isolation, Purification and Labeling of Mouse Bone Marrow Neutrophils for Functional Studies and Adoptive Transfer Experiments. JoVE. 2013(77):e50586. doi: 10.3791/50586 23892876