Role of Hyphal Formation in Interactions of Candida albicans with Endothelial Cells
Open accessAbstract
The ability to change from yeast to hyphal morphology is a major virulence determinant of Candida albicans . Mutants with defined defects in filamentation regulatory pathways have reduced virulence in mice. However, is it poorly understood why hyphal formation is critical for C. albicans to cause hematogenously disseminated infections. We used recently constructed mutants to examine the role of hyphal formation in the interactions of C. albicans with endothelial cells in vitro. These interactions included the ability of the mutants to invade and injure endothelial cells. Because the formation of hyphae may influence the host inflammatory response to C. albicans , we also investigated the capacity of these mutants to stimulate endothelial cells to express E-selectin and intercellular adhesion molecule 1. We infected endothelial cells with C. albicans strains containing homozygous null mutations in the following filamentation regulatory genes: CLA4 , CPH1 , EFG1 , and TUP1 . Whereas the wild-type strain formed true hyphae on endothelial cells, we found that neither the Δ efg1 nor the Δ cph1 Δefg1 double mutant germinated. The Δ tup1 mutant formed only pseudohyphae. We also found that the Δ efg1 , Δ cph1 Δefg1 , and Δ tup1 mutants had significantly reduced capacities to invade and injure endothelial cells. Therefore, Efg1p and Tup1p contribute to virulence by regulating hyphal formation and the factors that enable C. albicans to invade and injure endothelial cells. With the exception of the Δcph1 Δefg1 mutant, all other mutants stimulated endothelial cells to express at least one of the leukocyte adhesion molecules. Therefore, the combined activities of Cph1p and Efg1p are required for C. albicans to stimulate a proinflammatory response in endothelial cells.
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Host cell invasion and damage are likely critical virulence attributes of C. albicans because mutants with defects in these processes in vitro are highly likely to have attenuated virulence in experimental animal models of hematogenously disseminated or oropharyngeal candidiasis.
“Host cell invasion and damage are likely critical virulence attributes of C. albicans because mutants with defects in these processes in vitro are highly likely to have attenuated virulence in experimental animal models of hematogenously disseminated or oropharyngeal candidiasis [5][6][7][8].”
From Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells (2007) · cites this paper as [7]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredInduction of endocytosis is passive on the part of C. albicans because killed hyphae are endocytosed as avidly as live hyphae.
“Furthermore, studies with killed organisms indicate that induction of endocytosis is passive on the part of the organism because killed hyphae are endocytosed as avidly as are live hyphae [5,7].”
From Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells (2007) · cites this paper as [7]
The Results report that nearly 70% of methanol-fixed germ tubes were taken up by endothelial cells, and the Discussion says killed C. albicans cells can be endocytosed. This supports endocytosis without a living organism’s active participation, but the paper does not compare uptake of killed and live hyphae or establish that it is equally avid. (LLM, conf=0.85)
Experimental — accuracy not yet measuredC. albicans mutants with defects in the signal transduction pathways that govern hyphal formation have a significantly reduced capacity to invade both endothelial and oral epithelial cells in vitro.
“We have found previously that C. albicans mutants with defects in the signal transduction pathways that govern hyphal formation have a significantly reduced capacity to invade both endothelial and oral epithelial cells in vitro [5][6][7].”
From Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells (2007) · cites this paper as [7]
The Results report reduced endothelial-cell endocytosis for several filamentation mutants, with the greatest reductions in Δefg1, Δcph1 Δefg1, and Δtup1. They also state that Δcph1 was not significantly different from wild type. The paper's experiments concern endothelial cells, not oral epithelial cells, so this source does not support the oral-cell portion of the claim. (LLM, conf=0.88)
Experimental — accuracy not yet measuredC. albicans invades both endothelial cells and oral epithelial cells in vitro by inducing its own endocytosis.
“Previously, we have found that C. albicans invades both endothelial cells and oral epithelial cells in vitro by inducing its own endocytosis [4,5,7].”
From Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells (2007) · cites this paper as [7]
The Results (page not provided) state that C. albicans invades endothelial cells in vitro predominantly by inducing its own endocytosis, and report endocytosis in the endothelial-cell experiments. Our copy does not address invasion of oral epithelial cells, so it supports only the endothelial-cell part of the sentence. (LLM, conf=0.88)
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“This process is passive on the part of the organism because killed organisms are able to induce endocytosis similarly to live organisms [27,29].”
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“and the C. albicans must then respond to stimulate endothelial cell damage (Mayer et al. 1992; Filler et al. 1995; Phan et al. 2000 ).”
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“albicans, the PAK Cla4 protein is a putative transduction element that has been reported to be involved in morphogenesis and virulence in this fungus (28, 41).”
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“Effects of RIM101 and NRG1 on C. albicans morphology In several in vitro infection models, host cell damage capacity correlates with C. albicans morphology (Phan et al., 2000; Villar et al., 2004; Park et al., 2005).”
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“evade phagocytes (84), to escape from blood vessels (112), and”
BackgroundCandida albicans and Oral Carcinogenesis. A Brief Review
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“albicans is the predominant species and is associated with high concentrations of alcohol dehydrogenase enzyme and P53 that suggests a dysplastic potential factor [95].”
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“…of morphologic and sexual development often directly regulate the expression of key virulence factors (Lo et al., 1997; Lengeler et al., 2000; Phan et al., 2000; Sonneborn et al., 2000; Bahn and Sundstrom, 2001, Felk et al., 2002; Fu et al., 2002; Garcia-Sanchez et al., 2004; Sanchez et al.,…”
BackgroundSelf-citation<i>Candida albicans</i>internalization by host cells is mediated by a clathrin-dependent mechanism
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“The first steps of this process are driven by the host cell since killed hyphae are internalized as efficiently as live hyphae even though they do not cause host cell damage (Filler et al., 1995; Phan et al., 2000; Park et al., 2005).”
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“albicans in an in vitro mouse endothelial cell model (39).”
BackgroundCandida and invasive candidiasis: back to basics
Lim, C. S. Y., Rosli, R., Seow, H. F., & Chong, P. P. (2011) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-011-1273-3 · Cited by 128 · see citing works
“[89] reported that all of the null mutants had reduced invasion and injury capabilities.”
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“by using the chromium release assay described previously (43).”
BackgroundMethodSelf-citationLinking fungal morphogenesis with virulence
Rooney, P. J., & Klein, B. S. (2002) · Cellular Microbiology · doi:10.1046/j.1462-5822.2002.00179.x · Cited by 120 · see citing works
“The filamentation-deficient efg/efg cph/cph double knockout strain and the constitutively hyphal tup1/tup1 mutant demonstrated a decreased ability to induce endothelial cell injury relative to the parent strain (Phan et al., 2000).”
BackgroundCandida albicansand cancer: Can this yeast induce cancer development or progression?
Ramirez‐Garcia, A., Rementerı́a, A., Urízar, J. M. A., Moragues, M. D., Antoran, A., Pellón, A., Abad, A., & Hernando, F. L. (2014) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2014.913004 · Cited by 120 · see citing works
“…et al., 1995, 1996; Glee et al., 2001; Grubb et al., 2009; Jong et al., 2003; Kurihara et al., 2003; Lim et al., 2011; Mayer et al., 2012; Orozco et al., 2000; Park et al., 2009; Phan et al., 2000;Ramirez-Garcia et al., 2011, 2013; Sanchez et al., 2004; Seidl et al., 2012; Zhao et al., 2007).”
BackgroundAlbano, L., Bretagne, S., Mamzer, M., Kacso, I., Desnos‐Ollivier, M., Guerrini, P., Luong, T. L., Cassuto, É., Dromer, F., Lortholary, O., et al. (2008) · Clinical Infectious Diseases · doi:10.1086/595688 · Cited by 120 · see citing works
Lemar, K. M., Turner, M., & Lloyd, D. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2002.01707.x · Cited by 118 · see citing works
“The morphological forms of C. albicans (Phan et al. 2000) and the physiological state of the host are also considered to be important.”
BackgroundLopes-Bezerra, L. M., & Filler, S. G. (2003) · Blood · doi:10.1182/blood-2003-06-2186 · Cited by 118 · see citing works
Self-citationN-cadherin Mediates Endocytosis of Candida albicans by Endothelial Cells
Phan, Q. T., Fratti, R. A., Prasadarao, N. V., Edwards, J. E., & Filler, S. G. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412592200 · Cited by 113 · see citing works
Self-citationDieterich, C., Schandar, M., Noll, M., Johannes, F., Brunner, H., Graeve, T., & Rupp, S. (2002) · Microbiology · doi:10.1099/00221287-148-2-497 · Cited by 113 · see citing works
“This strain, as well as a strain deleted for EFG1, also showed limited abilities to damage endothelial cells (Phan et al., 2000).”
BackgroundResultInfluentialLiu, H. (2002) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00215 · Cited by 111 · see citing works
Forche, A., Cromie, G., Gerstein, A. C., Solis, N. V., Pisithkul, T., Srifa, W., Jeffery, E., Abbey, D., Filler, S. G., Dudley, A. M., et al. (2018) · Genetics · doi:10.1534/genetics.118.301019 · Cited by 94 · see citing works
“Mutants with filamentation defects cause less damage to epithelial and endothelial cells in vitro (Phan et al. 2000; Tsuchimori et al. 2000; Bensen et al. 2002).”
BackgroundSelf-citationSanchez, A. A., Johnston, D. A., Myers, C., Edwards, J. E., Mitchell, A. P., & Filler, S. G. (2004) · Infection and Immunity · doi:10.1128/iai.72.1.598-601.2004 · Cited by 101 · see citing works
“with endothelial cells isolated from human umbilical cord veins, as described previously (24).”
BackgroundMethodInfluentialSelf-citationImmune Sensing of Candida albicans
Bojang, E., Ghuman, H., Kumwenda, P., & Hall, R. A. (2021) · Journal of Fungi · doi:10.3390/jof7020119 · Cited by 106 · see citing works
Mayer, F. L., Wilson, D., Jacobsen, I. D., Miramón, P., Slesiona, S., Bohovych, I., Brown, A. J. P., & Hube, B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038584 · Cited by 100 · see citing works
“albicans strains [80,81].”
Urban, C. F., Xiong, X. B., Sohn, K., Schröppel, K., Brunner, H., & Rupp, S. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04771.x · Cited by 95 · see citing works
“…hyphal development, respectively, and are required for virulence both in vivo and in vitro , for morphogenesis and for expression of adhesion proteins of the cell wall in C. albicans (Braun and Johnson, 1997; 2000; Lo et al ., 1997; Phan et al ., 2000; Dieterich et al ., 2002; Sohn et al ., 2003).”
BackgroundMechanisms of Candida albicans Trafficking to the Brain
Liu, Y., Mittal, R., Solis, N. V., Prasadarao, N. V., & Filler, S. G. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002305 · Cited by 93 · see citing works
“HUVECs were harvested from umbilical cords with collagenase and grown in M-199 medium supplemented with 10% fetal bovine serum and 10% defined bovine calf serum (Gemini Bio-Products), and containing 2 mM L-glutamine with penicillin and streptomycin (Irvine Scientific) as previously described [51].”
MethodSelf-citationInvasive Phenotype of Candida albicans Affects the Host Proinflammatory Response to Infection
Villar, C. C., Kashleva, H., Mitchell, A. P., & Dongari-Bagtzoglou, A. (2005) · Infection and Immunity · doi:10.1128/iai.73.8.4588-4595.2005 · Cited by 98 · see citing works
“Because the proinflammatory response of epithelial (47) or endothelial (38) cells to C.”
BackgroundMaddi, A., Bowman, S. M., & Free, S. J. (2009) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.06.005 · Cited by 89 · see citing works
“, 2006), and help in the invasion of host tissues (Phan et al., 2000).”
Grubb, S. E. W., Murdoch, C., Sudbery, P. E., Saville, S. P., Lopez-Ribot, J. L., & Thornhill, M. H. (2008) · Infection and Immunity · doi:10.1128/iai.00332-08 · Cited by 87 · see citing works
“However, it is also possible that yeast forms adhere to the endothelial surface, germinate there, and then penetrate and damage the endothelium during transmigration (22) or that yeast forms adhere and are then endocytosed before germinating within the endothelial cell to cause damage (64).”
BackgroundFrank, C. F., & Hostetter, M. K. (2007) · Translational research · doi:10.1016/j.trsl.2006.11.006 · Cited by 87 · see citing works
New signaling pathways govern the host response to C. albicans infection in various nichesPreprint
Liu, Y., Shetty, A. C., Schwartz, J. A. J., Bradford, L. L., Xu, W., Phan, Q. T., Kumari, P., Mahurkar, A., Mitchell, A. P., Ravel, J., et al. (2015) · Genome Research · doi:10.1101/gr.187427.114 · Cited by 86 · see citing works
“The observation that invasion-defective C. albicans mutants display attenuated virulence in murine models of OPC and HDC is evidence of the critical importance of invasion to virulence (Phan et al. 2000; Sanchez et al. 2004; Park et al. 2005; Chiang et al. 2007).”
BackgroundSelf-citationCandida albicansactively modulates intracellular membrane trafficking in mouse macrophage phagosomes
Fernández‐Arenas, E., Bleck, C. K. E., Nombela, C., Gil, C., Griffiths, G., & Diez‐Orejas, R. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01274.x · Cited by 85 · see citing works
“In addition, this efg1D/cph1D avirulent mutant offers the possibility to study differences in the host immune response between virulent versus avirulent C. albicans strains (Lo et al., 1997; Phan et al., 2000; Dieterich et al., 2002; Gow et al., 2003; Lu et al., 2006; Chamilos et al., 2007).”
BackgroundClinical Implications of Oral Candidiasis: Host Tissue Damage and Disseminated Bacterial Disease
Kong, E. F., Kucharíková, S., Dijck, P. V., Peters, B. M., Shirtliff, M. E., & Jabra‐Rizk, M. A. (2014) · Infection and Immunity · doi:10.1128/iai.02843-14 · Cited by 84 · see citing works
“hyphae are not capable of causing mucosal infections (44, 46, 48).”
BackgroundKörting, H. C., Hube, B., Oberbauer, S., Januschke, E., Hamm, G., Albrecht, A., Borelli, C., & Schaller, M. (2003) · Journal of Medical Microbiology · doi:10.1099/jmm.0.05125-0 · Cited by 83 · see citing works
“…strains which lacked either functional Efg1, Cph1 or both factors (Brown&Gow, 1999; Stoldt et al., 1997; Bockmuhl & Ernst, 2001; Dieterich et al., 2002; Kohler & Fink, 1996; Leberer et al., 1997; Lo et al., 1997; Sonneborn et al., 1999b;Weide &Ernst, 1999; Lewis et al., 2002; Phan et al., 2000).”
BackgroundMethodInfluentialMartínez-López, R., Park, H., Myers, C., Gil, C., & Filler, S. (2006) · Eukaryotic Cell · doi:10.1128/ec.5.1.140-147.2006 · Cited by 81 · see citing works
“albicans that are endocytosed poorly and cause little damage to endothelial cells and oral epithelial cells have significantly reduced virulence in mouse models of hematogenously disseminated or oropharyngeal candidiasis (20, 21, 25).”
BackgroundSelf-citationLu, Y., Su, C., Mao, X., Raniga, P. P., Liu, H., & Chen, J. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-02-0173 · Cited by 82 · see citing works
“albicans with endothelial and epithelia cells, as well as biofilm formation and catheter infection (Lo et al., 1997; Phan et al., 2000; Dieterich et al., 2002; Lewis et al., 2002; Ramage et al., 2002; Garcia-Sanchez et al., 2004).”
BackgroundVendelė, I., Willment, J. A., Silva, L. M., Palma, A. S., Chai, W., Liu, Y., Feizi, T., Spyrou, M., Stappers, M. H. T., Brown, G. D., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1007927 · Cited by 80 · see citing works
Fungal invasion of epithelial cells
Yang, W., Yan, L., Wu, C., Zhao, X., & Tang, J. (2014) · Microbiological Research · doi:10.1016/j.micres.2014.02.013 · Cited by 79 · see citing works
“Fungal-induced ndocytosis is a passive process since killed hyphae are endocyosed as avidly as living hyphae (Phan et al. 2000; Park et al. 2005).”
BackgroundPadmavathi, A. R., Sriyutha Murthy, P., Das, A., Priya, A., Sushmitha, T. J., Pandian, S. K., & Rao, T. S. (2020) · Biofouling · doi:10.1080/08927014.2020.1715371 · Cited by 78 · see citing works
“…phenotypes are virulent parameters that contribute to the invasive behaviour of C. albicans which is quintessential for adhesion and invasion into host epithelial cells (Phan et al. 2000; Zakikhany et al. 2007) and spreading infections to deep seated tissues (Lo et al. 1997; Moyes et al. 2015).”
BackgroundGil-Bona, A., Parra‐Giraldo, C. M., Hernáez, M. L., Reales‐Calderón, J. A., Solis, N. V., Filler, S. G., Monteoliva, L., & Gil, C. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2015.06.006 · Cited by 78 · see citing works
“albicans strains to the FaDu cell line was measured using a (51)Cr release assay as described previously [45].”
MethodSelf-citationJackson, S., Coulthwaite, L., Loewy, Z. G., Scallan, A., & Verran, J. (2014) · Journal of Prosthetic Dentistry · doi:10.1016/j.prosdent.2014.02.003 · Cited by 77 · see citing works
Inactivation of Kex2p Diminishes the Virulence of Candida albicans
Newport, G., Kuo, A., Flattery, A. M., Gill, C., Blake, J., Kurtz, M. B., Abruzzo, G. K., & Agabian, N. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209713200 · Cited by 77 · see citing works
Spiering, M. J., Moran, G. P., Chauvel, M., MacCallum, D. M., Higgins, J., Hokamp, K., Yeomans, T., d’Enfert, C., Coleman, D. C., & Sullivan, D. J. (2009) · Eukaryotic Cell · doi:10.1128/ec.00291-09 · Cited by 77 · see citing works
“A trait critically important for Candida virulence especially in endothelial and epithelial infection models is the ability to undergo the yeast-to-hypha transition (hyphal morphogenesis) (16, 26, 31).”
BackgroundChiang, L. Y., Sheppard, D. C., Gravelat, F. N., Patterson, T. F., & Filler, S. G. (2008) · Infection and Immunity · doi:10.1128/iai.01510-07 · Cited by 76 · see citing works
“Other fungal pathogens, such as Candida albicans, stimulate endothelial cell expression of these proinflammatory mediators (4, 16, 21).”
BackgroundSelf-citationAn RNA Transport System in Candida albicans Regulates Hyphal Morphology and Invasive Growth
Elson, S. L., Noble, S. M., Solis, N. V., Filler, S. G., & Johnson, A. D. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000664 · Cited by 76 · see citing works
“Endothelial and epithelial cell damage assays were performed as previously described [45,46].”
BackgroundMethodSelf-citationHausauer, D. L., Gerami‐Nejad, M., Kistler-Anderson, C., & Gale, C. A. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.7.1273-1286.2005 · Cited by 75 · see citing works
“albicans strains with defects in hyphal morphogenesis appear to be less virulent in animal and tissue-based models of candidiasis (9, 36, 45, 48), leading to the idea that morphogenesis is required for virulence.”
BackgroundBrand, A., Vacharaksa, A., Bendel, C. M., Norton, J., Haynes, P. R., Henry‐Stanley, M. J., Wells, C. L., Ross, K., Gow, N. A. R., & Gale, C. A. (2008) · Eukaryotic Cell · doi:10.1128/ec.00453-07 · Cited by 71 · see citing works
“The ability to form hyphae strongly correlates with the ability to injure host cells (44), and many of the C.”
BackgroundToenjes, K. A., Munsee, S. M., Ibrahim, A. S., Jeffrey, R., Edwards, J. E., & Johnson, D. I. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.3.963-972.2005 · Cited by 72 · see citing works
“assay in 96-well tissue culture plates described previously (32).”
MethodMogavero, S., Sauer, F. M., Brunke, S., Allert, S., Schulz, D., Wisgott, S., Jablonowski, N., Elshafee, O., Krüger, T., Kniemeyer, O., et al. (2021) · Cellular Microbiology · doi:10.1111/cmi.13378 · Cited by 69 · see citing works
“Als3, which acts as both an adhesin and invasin (Phan et al., 2000; Wachtler et al., 2011).”
BackgroundSpellberg, B. J., Johnston, D. A., Phan, Q. T., Edwards, J. E., French, S. W., Ibrahim, A. S., & Filler, S. G. (2003) · Infection and Immunity · doi:10.1128/iai.71.10.5756-5764.2003 · Cited by 68 · see citing works
“The hyphadeficient mutant strain is defective in its ability to injure host cells in vitro (12, 24), and it is therefore likely that this mutant strain causes less damage to the renal parenchyma and is a weaker stimulus for IL-10 production than the wild-type strain.”
BackgroundSelf-citationFungal Infection of the Radicular Dentin
SIQUEIRAJR, J., Rôças, I. N., LOPES, H., Elias, C. N., & DEUZEDA, M. (2002) · Journal of Endodontics · doi:10.1097/00004770-200211000-00006 · Cited by 67 · see citing works
Adhesion of Candida albicans to Endothelial Cells under Physiological Conditions of Flow
Grubb, S. E. W., Murdoch, C., Sudbery, P. E., Saville, S. P., Lopez-Ribot, J. L., & Thornhill, M. H. (2009) · Infection and Immunity · doi:10.1128/iai.00518-09 · Cited by 66 · see citing works
“Previous in vitro studies showed that yeast forms adhere to the endothelial cell surface before undergoing germination and causing endothelial damage (6, 19).”
BackgroundAspartic proteinases of Candida spp.: role in pathogenicity and antifungal resistance
Silva, N. C., Nery, J. M., & Dias, A. (2014) · Mycoses (Berlin) · doi:10.1111/myc.12095 · Cited by 76 · see citing works
Ura-status-dependent adhesion of Candida albicans mutants
Bain, J. M., Stubberfield, C. R., & Gow, N. A. R. (2001) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2001.tb10905.x · Cited by 63 · see citing works
The Novel Candida albicans Transporter Dur31 Is a Multi-Stage Pathogenicity Factor
Mayer, F. L., Wilson, D., Jacobsen, I. D., Miramón, P., Große, K., & Hube, B. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002592 · Cited by 61 · see citing works
“albicans strains for 15 hours and the degree of oral epithelial cell damage was quantified by measuring lactate dehydrogenase (LDH) activity [29,30].”
BackgroundMethodBernhardt, J., Herman, D., Sheridan, M. J., & Calderone, R. (2001) · The Journal of Infectious Diseases · doi:10.1086/323807 · Cited by 62 · see citing works
Małagocka, J., Grell, M. N., Lange, L., Eilenberg, J., & Jensen, A. B. (2015) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2015.05.001 · Cited by 60 · see citing works
“Pld1 plays a role in transition from yeast to hyphal type of growth in Candida, a process that is essential for invasion of host cells (Hube et al., 2001; Phan et al., 2000).”
BackgroundRole of Candida albicans polymorphism in interactions with oral epithelial cells
Villar, C. C., Kashleva, H., & Dongari‐Bagtzoglou, A. I. (2004) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.2004.00150.x · Cited by 60 · see citing works
Transcriptional Responses of Candida albicans to Epithelial and Endothelial Cells
Park, H., Liu, Y., Solis, N. V., Spotkov, J., Hamaker, J. J., Blankenship, J. R., Yeaman, M. R., Mitchell, A. P., Liu, H., & Filler, S. G. (2009) · Eukaryotic Cell · doi:10.1128/ec.00165-09 · Cited by 58 · see citing works
“Prior studies indicate that mutant germination defects are invariably associated with endothelial cell damage defects (48, 59), so the yck2/yck2 mutant is novel in separating these two phenotypes.”
BackgroundMethodSelf-citationExposure of Candida albicans β (1,3)-glucan is promoted by activation of the Cek1 pathway
Chen, T., Jackson, J. W., Tams, R. N., Davis, S. E., Sparer, T. E., & Reynolds, T. B. (2019) · PLOS Genetics · doi:10.1371/journal.pgen.1007892 · Cited by 56 · see citing works
Candida albicans protein kinase CK2 governs virulence during oropharyngeal candidiasis
Chiang, L. Y., Sheppard, D. C., Bruno, V. M., Mitchell, A. P., Edwards, J. E., & Filler, S. G. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00784.x · Cited by 59 · see citing works
“They were cultured as previously described (Phan et al., 2000) in M-199 medium supplemented with 10% fetal bovine serum and 10% defined bovine calf serum (both from Gemini Bio-Products), and containing 2 mM L-glutamine with penicillin and streptomycin (Irvine Scientific).”
BackgroundMethodInfluentialSelf-citationVonk, A. G., Netea, M. G., van der Meer, J. W. M., & Kullberg, B. J. (2006) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.6.9.891 · Cited by 54 · see citing works
“albicans can escape from the endothelial cell by phagosome fusion with the abluminal plasma membrane, or by damaging the endothelial cell by germination (Figure 1) [18,20,21].”
BackgroundPathogenesis I: interactions of host cells and fungi
Clemons, K. V., Calich, V. L. G., Burger, E., Filler, S. G., Graziuttit, M., Murphy, J. W., Roilides, E., Čampa, A., Dias, M. R., Edwards, J. E., et al. (2000) · Medical Mycology · doi:10.1080/mmy.38.s1.99.111 · Cited by 54 · see citing works
Self-citationZhang, L., Chang, W., Sun, B., Groh, M., Speicher, A., & Lou, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028953 · Cited by 52 · see citing works
“Studies have demonstrated that filamentation plays a crucial role in the pathogenic process [3,4,5].”
BackgroundTherapeutic Potential of Thiazolidinedione-8 as an Antibiofilm Agent against Candida albicans
Feldman, M., Al-Quntar, A., Polacheck, I., Friedman, M., & Steinberg, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093225 · Cited by 51 · see citing works
“albicans to evade macrophages [32], escape from blood vessels [33], and colonize medical devices by forming biofilms [9,34].”
BackgroundBertolini, M., Xu, H., Sobue, T., Nobile, C. J., Cury, A. A. D. B., & Dongari‐Bagtzoglou, A. I. (2015) · Molecular Oral Microbiology · doi:10.1111/omi.12095 · Cited by 49 · see citing works
“Germination of fungal cells to form true hyphae is a pre-requisite for epithelial invasion and damage in several experimental systems (Phan et al., 2000; Schlecht et al., 2014; Villar et al., 2004).”
BackgroundLu, Q., Jayatilake, J. A. M. S., Samaranayake, L. P., & Jin, L. (2006) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700346 · Cited by 49 · see citing works
“albicans efg1/efg1 cph1/ cph1 mutant is unable to form hyphae under any conditions and is lowly virulent in animal or cell based systems (Lo et al., 1997; Phan et al., 2000).”
BackgroundResultSohn, K., rek, I. S. ⁄., Fertey, J., Königsdorfer, A., Joffroy, C. M., Hauser, N., Zelt, G., Brunner, H., & Rupp, S. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00130.x · Cited by 50 · see citing works
Rottmann, M., Dieter, S., Brunner, H., & Rupp, S. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03358.x · Cited by 47 · see citing works
“As the ability to switch between a yeast and a hyphal form is essential for virulence in C. albicans (Lo et al ., 1997; Phan et al ., 2000), the components required for this differentiation could be potential virulence factors.”
BackgroundNisin Z inhibits the growth ofCandida albicansand its transition from blastospore to hyphal form
Lay, C., Akerey, B., Fliss, I., Subirade, M., & Rouabhia, M. (2008) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2008.03908.x · Cited by 47 · see citing works
“Host cell invasion and damage are likely critical virulence attributes of C. albicans (Phan et al. 2000; Sanchez et al. 2004; Park et al. 2005; Chiang et al. 2007).”
BackgroundSeman, B. G., Moore, J. L., Scherer, A. K., Blair, B. A., Manandhar, S., Jones, J. M., & Wheeler, R. T. (2018) · Infection and Immunity · doi:10.1128/iai.00415-18 · Cited by 44 · see citing works
vandenBerg, A. L., Ibrahim, A. S., Edwards, J. E., Toenjes, K. A., & Johnson, D. I. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.3.724-734.2004 · Cited by 46 · see citing works
“ously (37), using human umbilical vein ECs incubated for 3 h in the presence of 5 10(5) of C.”
Mao, X., Cao, F., Nie, X., Liu, H., & Chen, J. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.04.009 · Cited by 45 · see citing works
The role of diclofenac sodium in the dimorphic transition in Candida albicans.
Ghalehnoo, Z. R., Rashki, A., Najimi, M., & Domínguez, Á. (2010) · Microbial Pathogenesis · doi:10.1016/j.micpath.2009.12.003 · Cited by 42 · see citing works
Role of Endothelial Cell Septin 7 in the Endocytosis of Candida albicans
Phan, Q., Eng, D., Mostowy, S., Park, H., Cossart, P., & Filler, S. (2013) · mBio · doi:10.1128/mbio.00542-13 · Cited by 42 · see citing works
Self-citationShareck, J., Nantel, A., & Belhumeur, P. (2011) · Eukaryotic Cell · doi:10.1128/ec.00305-10 · Cited by 41 · see citing works
- Authors
- Phan, Q. T., Belanger, P. H., & Filler, S. G.
- Affiliations
- University of California, Los Angeles (US)
- ORCID
- Filler, Scott G.
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2000-06
- Volume
- 68
- Issue
- 6
- Pages
- 3485-3490
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC97632
- OpenAlex
- W2134152581
- Cited by
- 181
- References
- 31
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 4 · 2020: 6 · 2019: 2 · 2018: 8 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 13 · 2013: 7 · 2012: 7
- FWCI
- 6.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Infection and Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Burroughs Wellcome Fund
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (P01 AI-37194, R29AI040636, R01AI019990, R01-AI19990, P01AI037194)
- National Center for Research Resources (M01RR000425)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Candida albicans, hyphal development, filamentation, endothelial cells, pseudohyphae, endothelial cell invasion, leukocyte adhesion molecules, E-selectin, ICAM-1, inflammation, virulence, yeast-to-hypha transition
- MeSH terms
- Candida albicans, DNA-Binding Proteins, Endocytosis, Endothelium, Vascular, Fungal Proteins, Genes, Fungal, Humans, Morphogenesis, Mutation, Nuclear Proteins, Repressor Proteins, Transcription Factors, Protein Serine-Threonine Kinases, Intercellular Adhesion Molecule-1, E-Selectin, Saccharomyces cerevisiae Proteins
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