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Cited by 643Antifungal resistance and susceptibilityFungal and yeast genetics researchBacterial biofilms and quorum sensing

Development and regulation of single- and multi-species Candida albicans biofilms

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Lohse, Matthew B., Gulati, Megha, Johnson, Alexander D., Nobile, Clarissa J.·2018·Nature Reviews Microbiology
DOI 10.1038/nrmicro.2017.107PMC PMC5726514
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Abstract

Candida albicans is among the most prevalent fungal species of the human microbiota and asymptomatically colonizes healthy individuals. However, it is also an opportunistic pathogen that can cause severe, and often fatal, bloodstream infections. The medical impact of C. albicans typically depends on its ability to form biofilms, which are closely packed communities of cells that attach to surfaces, such as tissues and implanted medical devices. In this Review, we provide an overview of the processes involved in the formation of C. albicans biofilms and discuss the core transcriptional network that regulates biofilm development. We also consider some of the advantages that biofilms provide to C. albicans in comparison with planktonic growth and explore polymicrobial biofilms that are formed by C. albicans and certain bacterial species.

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  1. [2]Davey ME O’Toole GA Microbial biofilms: from ecology to molecular genetics Microbiol Mol Biol Rev 64 847 867 2000 11104821 PMC99016
  2. [3]Kolter R Greenberg EP Microbial sciences: The superficial life of microbes Nature 441 300 302 2006 16710410
  3. [4]Hall-Stoodley L Costerton JW Stoodley P Bacterial biofilms: from the natural environment to infectious diseases Nat Rev Microbiol 2 95 108 2004 15040259
  4. [5]Wolcott R Costerton JW Raoult D Culter SJ The polymicrobial nature of biofilm infection Clin Microbiol Infect 19 107 112 2013 22925473
  5. [6]Fox EP Nobile CJ A sticky situation: untangling the transcriptional network controlling biofilm development in Candida albicans Transcription 3 315 322 2012 23117819 PMC3630188
  6. [10]Kumamoto CA Candida biofilms Curr Opin Microbiol 5 608 611 2002 12457706
  7. [11]Kumamoto CA Inflammation and gastrointestinal Candida colonization Curr Opin Microbiol 14 386 391 2011 21802979 PMC3163673
  8. [12]Calderone RA Fonzi WA Virulence factors of Candida albicans Trends Microbiol 9 327 335 2001 11435107
  9. [13]Pappas PG Guidelines for treatment of candidiasis Clin Infect Dis 38 161 189 2004 14699449
  10. [14]Wenzel RP Nosocomial candidemia: risk factors and attributable mortality Clin Infect Dis 20 1531 1534 1995 7548504
  11. [15]Kullberg BJ Oude Lashof AM Epidemiology of opportunistic invasive mycoses Eur J Med Res 7 183 191 2002 12069910
  12. [17]Chandra J Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance J Bacteriol 183 5385 5394 2001 11514524 PMC95423
  13. [18]Ramage G Mowat E Jones B Williams C Lopez-Ribot J Our current understanding of fungal biofilms Crit Rev Microbiol 35 340 355 2009 19863383
  14. [19]Kojic EM Darouiche RO Candida infections of medical devices Clin Microbiol Rev 17 255 267 2004 15084500 PMC387407
  15. [21]Donlan RM Biofilm formation: a clinically relevant microbiological process Clin Infect Dis 33 1387 1392 2001 11565080
  16. [22]Tumbarello M Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia J Clin Microbiol 45 1843 1850 2007 17460052 PMC1933062
  17. [23]Tumbarello M Risk factors and outcomes of candidemia caused by biofilm-forming isolates in a tertiary care hospital PLoS ONE 7 e33705 2012 22479431 PMC3316499
  18. [24]Lebeaux D Ghigo JM Beloin C Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics Microbiol Mol Biol Rev 78 510 543 2014 25184564 PMC4187679
  19. [25]Fox EP Singh-Babak SD Hartooni N Nobile CJ Antifungals: From genomics to resistance and the development of Novel Agents Coste AT Vandeputte P 71 90 Caister Academic Press 2015
  20. [26]Andes DR Impact of treatment strategy on outcomes in patients with candidemia and other forms of invasive candidiasis: a patient-level quantitative review of randomized trials Clin Infect Dis 54 1110 1122 2012 22412055
  21. [28]Uppuluri P Dispersion as an important step in the Candida albicans biofilm developmental cycle PLoS Pathog 6 e1000828 2010 This work provides an examination of cell dispersion from biofilms, including regulation, nutrient dependence and the characteristics of dispersed cells 20360962 PMC2847914
  22. [29]Hawser SP Douglas LJ Biofilm formation by Candida species on the surface of catheter materials in vitro Infect Immun 62 915 921 1994 8112864 PMC186203
  23. [30]Nobile CJ Mitchell AP Genetics and genomics of Candida albicans biofilm formation Cell Microbiol 8 1382 1391 2006 16848788
  24. [34]Johnson CC Yu A Lee H Fidel PL Noverr MC Development of a contemporary animal model of Candida albicans-associated denture stomatitis using a novel intraoral denture system Infect Immun 80 1736 1743 2012 22392931 PMC3347462
  25. [37]Dongari-Bagtzoglou A Kashleva H Dwivedi P Diaz P Vasilakos J Characterization of mucosal Candida albicans biofilms PLoS ONE 4 e7967 2009 19956771 PMC2776351
  26. [38]Řičicová M Candida albicans biofilm formation in a new in vivo rat model Microbiology 156 909 919 2010 19959578
  27. [39]Schinabeck MK Rabbit model of Candida albicans biofilm infection: liposomal amphotericin B antifungal lock therapy Antimicrob Agents Chemother 48 1727 1732 2004 15105127 PMC400590
  28. [40]Shuford JA Rouse MS Piper KE Steckelberg JM Patel R Evaluation of caspofungin and amphotericin B deoxycholate against Candida albicans biofilms in an experimental intravascular catheter infection model J Infect Dis 194 710 713 2006 16897672
  29. [41]Ramage G Tomsett K Wickes BL López-Ribot JL Redding SW Denture stomatitis: a role for Candida biofilms Oral Surg Oral Med Oral Pathol Oral Radiol Endod 98 53 59 2004 15243471
  30. [42]Lazzell AL Treatment and prevention of Candida albicans biofilms with caspofungin in a novel central venous catheter murine model of candidiasis J Antimicrob Chemother 64 567 570 2009 19584104
  31. [43]Kakade P Sadhale P Sanyal K Nagaraja V ZCF32, a fungus specific Zn(II)2 Cys6 transcription factor, is a repressor of the biofilm development in the human pathogen Candida albicans Sci Rep 6 31124 2016 27498700 PMC4976313
  32. [44]Ghosh AK Wangsanut T Fonzi WA Rolfes RJ The GRF10 homeobox gene regulates filamentous growth in the human fungal pathogen Candida albicans FEMS Yeast Res 15 fov093 2015 26472755 PMC4705307
  33. [45]Chen HF Lan CY Role of SFP1 in the regulation of Candida albicans biofilm formation PLoS ONE 10 e0129903 2015 26087243 PMC4472802
  34. [46]Nobile CJ A recently evolved transcriptional network controls biofilm development in Candida albicans Cell 148 126 138 2012 This study defines the core transcriptional network regulating C. albicans biofilms 22265407 PMC3266547
  35. [47]Fox EP An expanded regulatory network temporally controls Candida albicans biofilm formation Mol Microbiol 96 1226 1239 2015 This work expands the core biofilm regulatory circuit while also providing insight into the transcriptional changes that occur temporally between different stages of biofilm development 25784162 PMC4464956
  36. [48]Nobile CJ Mitchell AP Regulation of cell-surface genes and biofilm formation by the C albicans transcription factor Bcr1p Curr Biol 15 1150 1155 2005 15964282
  37. [49]Hernday AD Structure of the transcriptional network controlling white-opaque switching in Candida albicans Mol Microbiol 90 22 35 2013 23855748 PMC3888361
  38. [50]Borneman AR Target hub proteins serve as master regulators of development in yeast Genes Dev 20 435 438 2006 16449570 PMC1369046
  39. [51]Sorrells TR Johnson AD Making sense of transcription networks Cell 161 714 723 2015 25957680 PMC4531093
  40. [52]Dranginis AM Rauceo JM Coronado JE Lipke PN A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions Microbiol Mol Biol Rev 71 282 294 2007 17554046 PMC1899881
  41. [53]Alves CT Effect of progesterone on Candida albicans vaginal pathogenicity Int J Med Microbiol 304 1011 1017 2014 25183575
  42. [54]Sandini S The MP65 gene is required for cell wall integrity, adherence to epithelial cells and biofilm formation in Candida albicans BMC Microbiol 11 106 2011 21575184 PMC3113926
  43. [55]Frade JP Arthington-Skaggs BA Effect of serum and surface characteristics on Candida albicans biofilm formation Mycoses 54 e154 e162 2011 20337936
  44. [56]Salgado PS Structural basis for the broad specificity to host-cell ligands by the pathogenic fungus Candida albicans Proc Natl Acad Sci USA 108 15775 15779 2011 21896717 PMC3179088
  45. [57]Li F Palecek SP Distinct domains of the Candida albicans adhesin Eap1p mediate cell-cell and cell-substrate interactions Microbiology 154 1193 1203 2008 18375812
  46. [58]Parsek MR Greenberg EP Sociomicrobiology: the connections between quorum sensing and biofilms Trends Microbiol 13 27 33 2005 15639629
  47. [59]Desai JV Mitchell AP Candida albicans biofilm development and its genetic control Microbiol Spectr http://dx.doi.org/10.1128/microbiolspec.MB-0005-2014 2015 PMC4507287 26185083 · DOI · Paper page
  48. [61]Nobile CJ Critical role of Bcr1-dependent adhesins in C albicans biofilm formation in vitro and in vivo PLoS Pathog 2 e63 2006 16839200 PMC1487173
  49. [62]Zhao X Oh SH Yeater KM Hoyer LL Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family Microbiology 151 1619 1630 2005 15870470 PMC2583123
  50. [63]Li F Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo Eukaryot Cell 6 931 939 2007 17416898 PMC1951519
  51. [65]Swidergall M Filler SG Oropharyngeal candidiasis: fungal invasion and epithelial cell responses PLoS Pathog 13 e1006056 2017 28081240 PMC5230744
  52. [66]Kempf M Disruption of Candida albicans IFF4 gene involves modifications of the cell electrical surface properties Colloids Surf B Biointerfaces 58 250 255 2007 17481864
  53. [67]Hoyer LL Cota E Candida albicans agglutinin-like sequence (Als) family vignettes: a review of Als protein structure and function Front Microbiol 7 280 2016 27014205 PMC4791367
  54. [68]Nobile CJ Nett JE Andes DR Mitchell AP Function of Candida albicans adhesin Hwp1 in biofilm formation Eukaryot Cell 5 1604 1610 2006 17030992 PMC1595337
  55. [69]Nobile CJ Complementary adhesin function in C albicans biofilm formation Curr Biol 18 1017 1024 2008 18635358 PMC2504253
  56. [71]Martins M Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms Mycopathologia 169 323 331 2010 20012895 PMC3973130
  57. [72]Nobile CJ Biofilm matrix regulation by Candida albicans Zap1 PLoS Biol 7 e1000133 2009 19529758 PMC2688839
  58. [74]Mitchell KF Community participation in biofilm matrix assembly and function Proc Natl Acad Sci USA 112 4092 4097 2015 This study examines the role of many polysaccharide components of the biofilm extracellular matrix 25770218 PMC4386410
  59. [76]Ramage G Vande Walle K López-Ribot JL Wickes BL The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans FEMS Microbiol Lett 214 95 100 2002 12204378
  60. [77]Schweizer A Rupp S Taylor BN Röllinghoff M Schröppel K The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans Mol Microbiol 38 435 445 2000 11069668
  61. [78]Konstantinidou N Morrissey JP Co-occurence of filamentation defects and impaired biofilms in Candida albicans protein kinase mutants FEMS Yeast Res 15 fov092 2015 26472756
  62. [79]Rajendran R Integrating Candida albicans metabolism with biofilm heterogeneity by transcriptome mapping Sci Rep 6 35436 2016 27765942 PMC5073228
  63. [80]Holland LM Comparative phenotypic analysis of the major fungal pathogens Candida parapsilosis and Candida albicans PLoS Pathog 10 e1004365 2014 25233198 PMC4169492
  64. [87]Blankenship JR Mitchell AP How to build a biofilm: a fungal perspective Curr Opin Microbiol 9 588 594 2006 17055772
  65. [88]Sellam A A Candida albicans early stage biofilm detachment event in rich medium BMC Microbiol 9 25 2009 19187560 PMC2647545
  66. [90]Richard ML Nobile CJ Bruno VM Mitchell AP Candida albicans biofilm-defective mutants Eukaryot Cell 4 1493 1502 2005 16087754 PMC1214533
  67. [91]Winter MB Global identification of biofilm-specific proteolysis in Candida albicans mBio 7 e01514 16 2016 27624133 PMC5021810
  68. [93]Fiori B In vitro activities of anidulafungin and other antifungal agents against biofilms formed by clinical isolates of different Candida and Aspergillus species Antimicrob Agents Chemother 55 3031 3035 2011 21422210 PMC3101406
  69. [94]Jacobson MJ Steckelberg KE Piper KE Steckelberg JM Patel R In vitro activity of micafungin against planktonic and sessile Candida albicans isolates Antimicrob Agents Chemother 53 2638 2639 2009 19307371 PMC2687220
  70. [96]Cowen LE The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype Nat Rev Microbiol 6 187 198 2008 18246082
  71. [97]Anderson JB Evolution of antifungal-drug resistance: mechanisms and pathogen fitness Nat Rev Microbiol 3 547 556 2005 15953931
  72. [98]Ramage G Bachmann S Patterson TF Wickes BL Lopez-Ribot JL Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms J Antimicrob Chemother 49 973 980 2002 12039889
  73. [99]Mukherjee PK Chandra J Kuhn DM Ghannoum MA Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols Infect Immun 71 4333 4340 2003 12874310 PMC165995
  74. [100]Prasad R Shah AH Rawal MK Antifungals: mechanism of action and drug resistance Adv Exp Med Biol 892 327 349 2016 26721281
  75. [103]Yeater KM Temporal analysis of Candida albicans gene expression during biofilm development Microbiology 153 2373 2385 2007 17660402
  76. [104]Nett J Putative role of β-1,3 glucans in Candida albicans biofilm resistance Antimicrob Agents Chemother 51 510 520 2007 17130296 PMC1797745
  77. [107]Vediyappan G Rossignol T D’Enfert C Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans Antimicrob Agents Chemother 54 2096 2111 2010 20194705 PMC2863626
  78. [110]Mathe L Van Dijck P Recent insights into Candida albicans biofilm resistance mechanisms Curr Genet 59 251 264 2013 23974350 PMC3824241
  79. [114]Gropp K The yeast Candida albicans evades human complement attack by secretion of aspartic proteases Mol Immunol 47 465 475 2009 19880183
  80. [115]Szafranski-Schneider E Msb2 shedding protects Candida albicans against antimicrobial peptides PLoS Pathog 8 e1002501 2012 22319443 PMC3271078
  81. [116]Swidergall M Ernst AM Ernst JF Candida albicans mucin Msb2 is a broad-range protectant against antimicrobial peptides Antimicrob Agents Chemother 57 3917 3922 2013 23733470 PMC3719696
  82. [117]Hirschfeld J Dynamic interactions of neutrophils and biofilms J Oral Microbiol 6 26102 2014 25523872 PMC4270880
  83. [118]Xie Z Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing J Infect Dis 206 1936 1945 2012 23033146 PMC3502374
  84. [119]Johnson CJ The extracellular matrix of Candida albicans biofilms impairs formation of neutrophil extracellular traps PLoS Pathog 12 e1005884 2016 27622514 PMC5021349
  85. [120]Peters BM Jabra-Rizk MA O’May GA Costerton JW Shirtliff ME Polymicrobial interactions: impact on pathogenesis and human disease Clin Microbiol Rev 25 193 213 2012 22232376 PMC3255964
  86. [122]Pammi M Zhong D Johnson Y Revell P Versalovic J Polymicrobial bloodstream infections in the neonatal intensive care unit are associated with increased mortality: a case-control study BMC Infect Dis 14 390 2014 25022748 PMC4226990
  87. [123]Peters BM Noverr MC Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity Infect Immun 81 2178 2189 2013 This study demonstrates that the combination of C. albicans and S. aureus results in dramatic increases in microbial burden and mortality in a mouse model of peritonitis 23545303 PMC3676024
  88. [124]Jarosz LM Deng DM van der Mei HC Crielaard W Krom BP Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation Eukaryot Cell 8 1658 1664 2009 19717744 PMC2772401
  89. [125]Bamford CV Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication Infect Immun 77 3696 3704 2009 19528215 PMC2737996
  90. [128]Bamford CV Nobbs AH Barbour ME Lamont RJ Jenkinson HF Functional regions of Candida albicans hyphal cell wall protein Als3 that determine interaction with the oral bacterium Streptococcus gordonii Microbiology 161 18 29 2015 25332379 PMC4274786
  91. [130]Hoyer LL Oh SH Jones R Cota E A proposed mechanism for the interaction between the Candida albicans Als3 adhesin and streptococcal cell wall proteins Front Microbiol 5 564 2014 25408685 PMC4219490
  92. [131]Peters BM Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p Microbiology 158 2975 2986 2012 22918893 PMC4083660
  93. [132]Schlecht LM Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue Microbiology 161 168 181 2015 25332378 PMC4274785
  94. [133]Förster TM Enemies and brothers in arms: Candida albicans and gram-positive bacteria Cell Microbiol 28 1709 1715 2016 27552083
  95. [134]Harriott MM Noverr MC Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance Antimicrob Agents Chemother 53 3914 3922 2009 This work shows that co-incubation of C. albicans and S. aureus results in increased biofilm formation and vancomycin resistance in S. aureus. 19564370 PMC2737866
  96. [135]Harriott MM Noverr MC Ability of Candida albicans mutants to induce Staphylococcus aureus vancomycin resistance during polymicrobial biofilm formation Antimicrob Agents Chemother 54 3746 3755 2010 20566760 PMC2934986
  97. [136]Kong EF Commensal protection of Staphylococcus aureus against antimicrobials by Candida albicans biofilm matrix mBio 7 e01365 16 2016 This study identifies the component of the C. albicans extracellular matrix that protects S. aureus from vancomycin 27729510 PMC5061872
  98. [138]Hogan DA Kolter R Pseudomonas-Candida interactions: an ecological role for virulence factors Science 296 2229 2232 2002 This is a foundational study of interactions between C. albicans and bacterial species 12077418
  99. [139]Strus M The in vitro activity of vaginal Lactobacillus with probiotic properties against Candida Infect Dis Obstet Gynecol 13 69 75 2005 16011996 PMC1784560
  100. [140]Hogan DA Vik A Kolter RA Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology Mol Microbiol 54 1212 1223 2004 15554963
  101. [141]McAlester G O’Gara F Morrissey JP Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans J Med Microbiol 57 563 569 2008 18436588
  102. [143]Seth EC Taga ME Nutrient cross-feeding in the microbial world Front Microbiol 5 350 2014 25071756 PMC4086397
  103. [144]Shrestha PM Rotaru AE Plugging in or going wireless: strategies for interspecies electron transfer Front Microbiol 5 237 2014 24904551 PMC4032928
  104. [145]Stams AJ Plugge CM Electron transfer in syntrophic communities of anaerobic bacteria and archaea Nat Rev Microbiol 7 568 577 2009 19609258
  105. [146]Morales DK Control of Candida albicans metabolism and biofilm formation by Pseudomonas aeruginosa phenazines mBio 4 e00526 12 2013 23362320 PMC3560528
  106. [147]Chen AI Candida albicans ethanol stimulates Pseudomonas aeruginosa WspR-controlled biofilm formation as part of a cyclic relationship involving phenazines PLoS Pathog 10 e1004480 2014 25340349 PMC4207824
  107. [149]Vande Velde G Kucharíková S Schrevens S Himmelreich U Van Dijck P Towards non-invasive monitoring of pathogen-host interactions during Candida albicans biofilm formation using in vivo bioluminescence Cell Microbiol 16 115 130 2014 This study describes an in vivo live-animal imaging model of infection 23962311 PMC4204156
  108. [150]Vande Velde G Kucharíková S Van Dijck P Himmelreich U Bioluminescence imaging of fungal biofilm development in live animals Methods Mol Biol 1098 153 167 2014 24166376
  109. [151]Tournu H Van Dijck P Candida biofilms and the host: models and new concepts for eradication Int J Microbiol 2012 845352 2012 22164167 PMC3227478
  110. [152]Lohse MB Assessment and optimizations of Candida albicans in vitro biofilm assays Antimicrob Agents Chemother 61 e02749 16 2017 28289028 PMC5404589
  111. [153]Ramage G Vande Walle K Wickes BL López-Ribot JL Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms Antimicrob Agents Chemother 45 2475 2479 2001 11502517 PMC90680
  112. [154]Nett JE Cain MT Crawford K Andes DR Optimizing a Candida biofilm microtiter plate model for measurement of antifungal susceptibility by tetrazolium salt assay J Clin Microbiol 49 1426 1433 2011 21227984 PMC3122839
  113. [155]Jin Y Yip HK Samaranayake YH Yau JY Samaranayake LP Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage in cases of human immunodeficiency virus infection J Clin Microbiol 41 2961 2967 2003 12843027 PMC165379
  114. [156]Nett JE Marchillo K Spiegel CA Andes DR Development and validation of an in vivo Candida albicans biofilm denture model Infect Immun 78 3650 3659 2010 20605982 PMC2937450
  115. [157]Wang X Fries BC A murine model for catheter-associated candiduria J Med Microbiol 60 1523 1529 2011 21596904 PMC3347865
  116. [158]Doyle TC Nawotka KA Kawahara CB Francis KP Contag PR Visualizing fungal infections in living mice using bioluminescent pathogenic Candida albicans strains transformed with the firefly luciferase gene Microb Pathog 40 82 90 2006 16426810
  117. [159]Kelly MT The Candida albicans CaACE2 gene affects morphogenesis, adherence and virulence Mol Microbiol 53 969 983 2004 15255906
  118. [160]Askew C The zinc cluster transcription factor Ahr1p directs Mcm1p regulation of Candida albicans adhesion Mol Microbiol 79 940 953 2011 21299649 PMC4092010
  119. [161]García-Sánchez S Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns Eukaryot Cell 3 536 545 2004 15075282 PMC387656
  120. [162]Tsai PW The role of Mss11 in Candida albicans biofilm formation Mol Genet Genom 289 807 819 2014 24752399
  121. [163]Sellam A Role of transcription factor CaNdt80p in cell separation, hyphal growth, and virulence in Candida albicans Eukaryot Cell 9 634 644 2010 20097739 PMC2863402
  122. [164]Bonhomme J Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans Mol Microbiol 80 995 1013 2011 21414038
  123. [165]Ganguly S Zap1 control of cell-cell signaling in Candida albicans biofilms Eukaryot Cell 10 1448 1454 2011 21890817 PMC3209068

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Authors
Lohse, M. B., Gulati, M., Johnson, A. D., & Nobile, C. J.
Affiliations
  • University of California, San Francisco (US)
  • University of California, Merced (US)
Corresponding author
  • Johnson, Alexander D.
  • Nobile, Clarissa J.
ORCID
Venue
Nature Reviews Microbiology
Publisher
Springer Science and Business Media LLC
Published
2017-10-03
Volume
16
Issue
1
Pages
19-31
ISSN
  • 1740-1526 (ISSN-L)
  • 1740-1534
DOI
10.1038/nrmicro.2017.107
PMC
PMC5726514
OpenAlex
W2761420273
Cited by
643
References
41
Citations by year
2026: 56 · 2025: 85 · 2024: 79 · 2023: 83 · 2022: 98 · 2021: 83 · 2020: 77 · 2019: 56 · 2018: 25
FWCI
6.64
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature Reviews Microbiology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institutes of Health
  • National Institute of Allergy and Infectious Diseases (R41AI112038, R01AI083311)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Keywords
Candida albicans, biofilm formation, polymicrobial biofilms, transcriptional regulation, bloodstream infection, opportunistic fungal pathogens, planktonic versus biofilm growth, fungal-bacterial interactions, biomedical implants, fungal colonization
MeSH terms
Antifungal Agents, Candida albicans, Humans, Gene Expression Regulation, Fungal, Biofilms, Drug Resistance, Fungal, Gene Regulatory Networks

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