Protection of Candida parapsilosis from neutrophil killing through internalization by human endothelial cells

References

• Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, Gillevet PM. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 2010; 6:e1000713; PMID:20072605; http://dx.doi.org/10.1371/journal.ppat.1000713.
   PubMed Web of Science ®Google Scholar
• Lionakis MS. New insights into innate immune control of systemic candidiasis. Med Mycol 2014; 52:555-64; PMID:25023483; http://dx.doi.org/10.1093/mmy/myu029.
   PubMed Web of Science ®Google Scholar
• Trofa D, Gacser A, Nosanchuk JD. Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 2008; 21:606-25; PMID:18854483; http://dx.doi.org/10.1128/CMR.00013-08.
   PubMed Web of Science ®Google Scholar
• Neu N, Malik M, Lunding A, Whittier S, Alba L, Kubin C, Saiman L. Epidemiology of candidemia at a Children's hospital, 2002 to 2006. Pediatr Infect Dis J 2009; 28:806-9; PMID:19636286; http://dx.doi.org/10.1097/INF.0b013e3181a0d78d.
   PubMed Web of Science ®Google Scholar
• Chow BD, Linden JR, Bliss JM. Candida parapsilosis and the neonate: epidemiology, virulence and host defense in a unique patient setting. Expert Rev Anti Infect Ther 2012; 10:935-46; PMID:23030332; http://dx.doi.org/10.1586/eri.12.74.
   PubMed Web of Science ®Google Scholar
• Pammi M, Holland L, Butler G, Gacser A, Bliss JM. Candida parapsilosis is a significant neonatal pathogen: a systematic review and meta-analysis. Pediatr Infect Dis J 2013; 32:e206-16; PMID:23340551; http://dx.doi.org/10.1097/INF.0b013e3182863a1c.
   PubMed Web of Science ®Google Scholar
• Ibrahim AS, Filler SG, Ghannoum MA, Edwards JE, Jr. Interferon-gamma protects endothelial cells from damage by Candida albicans. J Infect Dis 1993; 167:1467-70; PMID:8501342; http://dx.doi.org/10.1093/infdis/167.6.1467.
   PubMed Web of Science ®Google Scholar
• Filler SG, Swerdloff JN, Hobbs C, Luckett PM. Penetration and damage of endothelial cells by Candida albicans. Infect Immun 1995; 63:976-83; PMID:7868270.
   PubMed Web of Science ®Google Scholar
• Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR. Nonfilamentous C. albicans mutants are avirulent. Cell 1997; 90:939-49; PMID:9298905; http://dx.doi.org/10.1016/S0092-8674(00)80358-X.
   PubMed Web of Science ®Google Scholar
• Bendel CM, Hess DJ, Garni RM, Henry-Stanley M, Wells CL. Comparative virulence of Candida albicans yeast and filamentous forms in orally and intravenously inoculated mice. Crit Care Med 2003; 31:501-7; PMID:12576958; http://dx.doi.org/10.1097/01.CCM.0000049954.48239.A1.
   PubMed Web of Science ®Google Scholar
• Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2003; 2:1053-60; PMID:14555488; http://dx.doi.org/10.1128/EC.2.5.1053-1060.2003.
   PubMed Web of Science ®Google Scholar
• Spellberg B, Johnston D, Phan QT, Edwards JE, Jr., French SW, Ibrahim AS, Filler SG. Parenchymal organ, and not splenic, immunity correlates with host survival during disseminated candidiasis. Infect Immun 2003; 71:5756-64; PMID:14500497; http://dx.doi.org/10.1128/IAI.71.10.5756-5764.2003.
   PubMed Web of Science ®Google Scholar
• Kim SK, El Bissati K, Ben Mamoun C. Amino acids mediate colony and cell differentiation in the fungal pathogen Candida parapsilosis. Microbiology 2006; 152:2885-94; PMID:17005970; http://dx.doi.org/10.1099/mic.0.29180-0.
   PubMed Web of Science ®Google Scholar
• Sawyer RT, Moon RJ, Beneke ES. Hepatic clearance of Candida albicans in rats. Infect Immun 1976; 14:1348-55; PMID:793993.
   PubMed Web of Science ®Google Scholar
• MacCallum DM, Odds FC. Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses 2005; 48:151-61; PMID:15842329; http://dx.doi.org/10.1111/j.1439-0507.2005.01121.x.
   PubMed Web of Science ®Google Scholar
• Mavor AL, Thewes S, Hube B. Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr Drug Targets 2005; 6:863-74; PMID:16375670; http://dx.doi.org/10.2174/138945005774912735.
   PubMed Web of Science ®Google Scholar
• de Groot PW, Bader O, de Boer AD, Weig M, Chauhan N. Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot Cell 2013; 12:470-81; PMID:23397570; http://dx.doi.org/10.1128/EC.00364-12.
   PubMed Web of Science ®Google Scholar
• Liu Y, Filler SG. Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot Cell 2011; 10:168-73; PMID:21115738; http://dx.doi.org/10.1128/EC.00279-10.
   PubMed Web of Science ®Google Scholar
• Yang W, Yan L, Wu C, Zhao X, Tang J. Fungal invasion of epithelial cells. Microbiol Res 2014; 169:803-10; PMID:24670964; http://dx.doi.org/10.1016/j.micres.2014.02.013.
   PubMed Web of Science ®Google Scholar
• Sun JN, Solis NV, Phan QT, Bajwa JS, Kashleva H, Thompson A, Liu Y, Dongari-Bagtzoglou A, Edgerton M, Filler SG. Host cell invasion and virulence mediated by Candida albicans Ssa1. PLoS Pathog 2010; 6:e1001181; PMID:21085601; http://dx.doi.org/10.1371/journal.ppat.1001181.
   PubMed Web of Science ®Google Scholar
• Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009; 459:657-62; PMID:19465905; http://dx.doi.org/10.1038/nature08064.
   PubMed Web of Science ®Google Scholar
• Hickey MJ, Kubes P. Intravascular immunity: the host-pathogen encounter in blood vessels. Nat Rev Immunol 2009; 9:364-75; PMID:19390567; http://dx.doi.org/10.1038/nri2532.
   PubMed Web of Science ®Google Scholar
• Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, Olyaei AJ, Marr KA, Pfaller MA, Chang CH, Webster KM. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis 2009; 48:1695-703; PMID:19441981; http://dx.doi.org/10.1086/599039.
   PubMed Web of Science ®Google Scholar
• Linden JR, Maccani MA, Laforce-Nesbitt SS, Bliss JM. High efficiency opsonin-independent phagocytosis of Candida parapsilosis by human neutrophils. Med Mycol 2010; 48:355-64; PMID:19672781; http://dx.doi.org/10.3109/13693780903164566.
   PubMed Web of Science ®Google Scholar
• Gazendam RP, van Hamme JL, Tool AT, van Houdt M, Verkuijlen PJ, Herbst M, Liese JG, van de Veerdonk FL, Roos D, van den Berg TK, et al. Two independent killing mechanisms of Candida albicans by human neutrophils: evidence from innate immunity defects. Blood 2014; 124:590-7; PMID:24948657; http://dx.doi.org/10.1182/blood-2014-01-551473.
   PubMed Web of Science ®Google Scholar
• Kaloriti D, Jacobsen M, Yin Z, Patterson M, Tillmann A, Smith DA, Cook E, You T, Grimm MJ, Bohovych I, et al. Mechanisms underlying the exquisite sensitivity of Candida albicans to combinatorial cationic and oxidative stress that enhances the potent fungicidal activity of phagocytes. MBio 2014; 5:e01334-14; PMID:25028425; http://dx.doi.org/10.1128/mBio.01334-14.
   PubMed Web of Science ®Google Scholar
• Urban CF, Reichard U, Brinkmann V, Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 2006; 8:668-76; PMID:16548892; http://dx.doi.org/10.1111/j.1462-5822.2005.00659.x.
   PubMed Web of Science ®Google Scholar
• Byrd AS, O'Brien XM, Johnson CM, Lavigne LM, Reichner JS. An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J Immunol 2013; 190:4136-48; PMID:23509360; http://dx.doi.org/10.4049/jimmunol.1202671.
   PubMed Web of Science ®Google Scholar
• Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009; 114:2619-22; PMID:19541821; http://dx.doi.org/10.1182/blood-2009-05-221606.
   PubMed Web of Science ®Google Scholar
• Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5:e1000639; PMID:19876394; http://dx.doi.org/10.1371/journal.ppat.1000639.
   PubMed Web of Science ®Google Scholar
• Cline MJ, Lehrer RI. Phagocytosis by human monocytes. Blood 1968; 32:423-35; PMID:4877597.
   PubMed Web of Science ®Google Scholar
• Seider K, Brunke S, Schild L, Jablonowski N, Wilson D, Majer O, Barz D, Haas A, Kuchler K, Schaller M, et al. The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 2011; 187:3072-86; PMID:21849684; http://dx.doi.org/10.4049/jimmunol.1003730.
   PubMed Web of Science ®Google Scholar
• Seider K, Gerwien F, Kasper L, Allert S, Brunke S, Jablonowski N, Schwarzmuller T, Barz D, Rupp S, Kuchler K, et al. Immune evasion, stress resistance, and efficient nutrient acquisition are crucial for intracellular survival of Candida glabrata within macrophages. Eukaryot Cell 2014; 13:170-83; PMID:24363366; http://dx.doi.org/10.1128/EC.00262-13.
   PubMed Web of Science ®Google Scholar
• Kasper L, Seider K, Gerwien F, Allert S, Brunke S, Schwarzmuller T, Ames L, Zubiria-Barrera C, Mansour MK, Becken U, et al. Identification of Candida glabrata genes involved in pH modulation and modification of the phagosomal environment in macrophages. PLoS One 2014; 9:e96015; PMID:24789333; http://dx.doi.org/10.1371/journal.pone.0096015.
   PubMed Web of Science ®Google Scholar
• Shintaku T, Glass KA, Hirakawa MP, Longley SJ, Bennett RJ, Bliss JM, Shaw SK. Human endothelial cells internalize Candida parapsilosis via N-WASP-mediated endocytosis. Infect Immun 2013; 81:2777-87; PMID:23690407; http://dx.doi.org/10.1128/IAI.00535-13.
   PubMed Web of Science ®Google Scholar
• Benjamin DK, Jr., Stoll BJ, Gantz MG, Walsh MC, Sanchez PJ, Das A, Shankaran S, Higgins RD, Auten KJ, Miller NA, et al. Neonatal candidiasis: epidemiology, risk factors, and clinical judgment. Pediatrics 2010; 126:e865-73; PMID:20876174; http://dx.doi.org/10.1542/peds.2009-3412.
   PubMed Web of Science ®Google Scholar
• Boyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl 1968; 97:77-89; PMID:4179068.
   PubMedGoogle Scholar
• Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S A 2007; 104:7628-33; PMID:17456602; http://dx.doi.org/10.1073/pnas.0611195104.
   PubMed Web of Science ®Google Scholar
• Otto V, Howard DH. Further studies on the intracellular behavior of Torulopsis glabrata. Infect Immun 1976; 14:433-8; PMID:987021.
   PubMed Web of Science ®Google Scholar
• Roetzer A, Gratz N, Kovarik P, Schuller C. Autophagy supports Candida glabrata survival during phagocytosis. Cell Microbiol 2010; 12:199-216; PMID:19811500; http://dx.doi.org/10.1111/j.1462-5822.2009.01391.x.
   PubMed Web of Science ®Google Scholar
• Sheppard DC, Filler SG. Host Cell Invasion by Medically Important Fungi. Cold Spring Harb Perspect Med 2014; 5:a019687; PMID:25367974.
   PubMed Web of Science ®Google Scholar
• Toth R, Toth A, Papp C, Jankovics F, Vagvolgyi C, Alonso MF, Bain JM, Erwig LP, Gacser A. Kinetic studies of Candida parapsilosis phagocytosis by macrophages and detection of intracellular survival mechanisms. Front Microbiol 2014; 5:633; PMID:25477874.
   PubMed Web of Science ®Google Scholar
• Edwards JE, Jr., Rotrosen D, Fontaine JW, Haudenschild CC, Diamond RD. Neutrophil-mediated protection of cultured human vascular endothelial cells from damage by growing Candida albicans hyphae. Blood 1987; 69:1450-7; PMID:3552077.
   PubMed Web of Science ®Google Scholar
• Martin CJ, Peters KN, Behar SM. Macrophages clean up: efferocytosis and microbial control. Curr Opin Microbiol 2014; 17:17-23; PMID:24581688; http://dx.doi.org/10.1016/j.mib.2013.10.007.
   PubMed Web of Science ®Google Scholar
• Stukes SA, Cohen HW, Casadevall A. Temporal kinetics and quantitative analysis of Cryptococcus neoformans nonlytic exocytosis. Infect Immun 2014; 82:2059-67; PMID:24595144; http://dx.doi.org/10.1128/IAI.01503-14.
   PubMed Web of Science ®Google Scholar
• Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007; 317:666-70; PMID:17673663; http://dx.doi.org/10.1126/science.1142883.
   PubMed Web of Science ®Google Scholar
• Lionakis MS, Swamydas M, Fischer BG, Plantinga TS, Johnson MD, Jaeger M, Green NM, Masedunskas A, Weigert R, Mikelis C, et al. CX3CR1-dependent renal macrophage survival promotes Candida control and host survival. J Clin Invest 2013; 123:5035-51; PMID:24177428; http://dx.doi.org/10.1172/JCI71307.
   PubMed Web of Science ®Google Scholar
• Lee WY, Moriarty TJ, Wong CH, Zhou H, Strieter RM, van Rooijen N, Chaconas G, Kubes P. An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat Immunol 2010; 11:295-302; PMID:20228796; http://dx.doi.org/10.1038/ni.1855.
   PubMed Web of Science ®Google Scholar
• Fratti RA, Ghannoum MA, Edwards JE, Jr., Filler SG. Gamma interferon protects endothelial cells from damage by Candida albicans by inhibiting endothelial cell phagocytosis. Infect Immun 1996; 64:4714-8; PMID:8890230.
   PubMed Web of Science ®Google Scholar
• de Fougerolles AR, Stacker SA, Schwarting R, Springer TA. Characterization of ICAM-2 and evidence for a third counter-receptor for LFA-1. J Exp Med 1991; 174:253-67; PMID:1676048; http://dx.doi.org/10.1084/jem.174.1.253.
   PubMed Web of Science ®Google Scholar
• Schenkel AR, Mamdouh Z, Muller WA. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol 2004; 5:393-400; PMID:15021878; http://dx.doi.org/10.1038/ni1051.
   PubMed Web of Science ®Google Scholar
• Halai K, Whiteford J, Ma B, Nourshargh S, Woodfin A. ICAM-2 facilitates luminal interactions between neutrophils and endothelial cells in vivo. J Cell Sci 2014; 127:620-9; PMID:24317296; http://dx.doi.org/10.1242/jcs.137463.
   PubMed Web of Science ®Google Scholar
• Wojciechowski JC, Sarelius IH. Preferential binding of leukocytes to the endothelial junction region in venules in situ. Microcirculation 2005; 12:349-59; PMID:16020081; http://dx.doi.org/10.1080/10739680590934763.
   PubMed Web of Science ®Google Scholar
• Phillipson M, Heit B, Colarusso P, Liu L, Ballantyne CM, Kubes P. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J Exp Med 2006; 203:2569-75; PMID:17116736; http://dx.doi.org/10.1084/jem.20060925.
   PubMed Web of Science ®Google Scholar
• Sumagin R, Prizant H, Lomakina E, Waugh RE, Sarelius IH. LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J Immunol 2010; 185:7057-66; PMID:21037096; http://dx.doi.org/10.4049/jimmunol.1001638.
   PubMed Web of Science ®Google Scholar
• Patel KD. Mechanisms of selective leukocyte recruitment from whole blood on cytokine-activated endothelial cells under flow conditions. J Immunol 1999; 162:6209-16; PMID:10229866.
   PubMed Web of Science ®Google Scholar
• Migliorini C, Qian Y, Chen H, Brown EB, Jain RK, Munn LL. Red blood cells augment leukocyte rolling in a virtual blood vessel. Biophys J 2002; 83:1834-41; PMID:12324405; http://dx.doi.org/10.1016/S0006-3495(02)73948-9.
   PubMed Web of Science ®Google Scholar
• Branzk N, Lubojemska A, Hardison SE, Wang Q, Gutierrez MG, Brown GD, Papayannopoulos V. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 2014; 15:1017-25; PMID:25217981; http://dx.doi.org/10.1038/ni.2987.
   PubMed Web of Science ®Google Scholar