EngineeredControl of Cell Morphology In Vivo Reveals Distinct Roles for Yeast andFilamentous Forms of Candida albicans duringInfection

Saville, Stephen P.; Lazzell, Anna L.; Monteagudo, Carlos; Lopez-Ribot, Jose L.

doi:10.1128/ec.2.5.1053-1060.2003

Cited by 655Antifungal resistance and susceptibilityFungal and yeast genetics researchFungal Infections and Studies

EngineeredControl of Cell Morphology In Vivo Reveals Distinct Roles for Yeast andFilamentous Forms of Candida albicans duringInfection

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Saville, Stephen P., Lazzell, Anna L., Monteagudo, Carlos, Lopez-Ribot, Jose L.·2003·Eukaryotic Cell

DOI 10.1128/ec.2.5.1053-1060.2003PMC PMC219382

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Abstract

It is widely assumed that the ability of Candida albicans to switch between different morphologies is required for pathogenesis. However, most virulence studies have used mutants that are permanently locked into either the yeast or filamentous forms which are avirulent but unsuitable for discerning the role of morphogenetic conversions at the various stages of the infectious process. We have constructed a strain in which this developmental transition can be externally modulated both in vitro and in vivo. This was achieved by placing one copy of the NRG1 gene (a negative regulator of filamentation) under the control of a tetracycline-regulatable promoter. This modified strain was then tested in an animal model of hematogenously disseminated candidiasis. Mice injected with this strain under conditions permitting hyphal development succumbed to the infection, whereas all of the animals injected under conditions that inhibited this transition survived. Importantly, fungal burdens were almost identical in both sets of animals, indicating that, whereas filament formation appears to be required for the mortality resulting from a deep-seated infection, yeast cells play an important role early in the infectious process by extravasating and disseminating to the target organs. Moreover, these infecting Candida yeast cells still retained their pathogenic potential, as demonstrated by allowing this developmental transition to occur at various time points postinfection. We demonstrate here the importance of morphogenetic conversions in C. albicans pathogenesis. This engineered strain should provide a useful tool in unraveling the individual contributions of the yeast and filamentous forms at various stages of the infectious process.

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The ability of C. albicans to reversibly change between blastospores and hyphae is a key virulence factor, and mutants that are unable to form hyphae have greatly attenuated virulence.
“The ability to reversibly change between blastospores and hyphae is a key virulence factor for this fungus, and mutants that are unable to form hyphae have greatly attenuated virulence [12,13].”
From Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells (2007) · cites this paper as [13]

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The direct cost and incidence of systemic fungal infections
Wilson, L. S., Reyes, C. M., Stolpman, M., Speckman, J., Allen, K., & Beney, J. (2002) · Value in Health · doi:10.1046/j.1524-4733.2002.51108.x · Cited by 374 · see citing works
The Impact of Candidemia on Length of Hospital Stay, Outcome, and Overall Cost of Illness
Rentz, A. M., Halpern, M. T., & Bowden, R. (1998) · Clinical Infectious Diseases · doi:10.1086/514955 · Cited by 310 · cited 1× · see citing works
“Even with aggressive drug therapy the prognosis is not good, with mortality rates ranging from 30 to 50% (36, 37); moreover, there is a significant economic burden associated with treatment (29, 38).”
Background
Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1
Murad, A. M. A., D'Enfert, C., Gaillardin, C., Tournu, H., Tekaia, F., Talibi, D., Marechal, D., Marchais, V., Cottin, J., & Brown, A. J. P. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02713.x · Cited by 208 · cited 2× · see citing works
“The NRG1 gene is transcribed maximally in yeast cells but is rapidly downregulated upon receipt of an appropriate stimulus to remove this repression and facilitate hyphal development (5, 24, 25).”
Background
Role of Hyphal Formation in Interactions of Candida albicans with Endothelial Cells
Phan, Q. T., Belanger, P. H., & Filler, S. G. (2000) · Infection and Immunity · doi:10.1128/iai.68.6.3485-3490.2000 · Cited by 181 · cited 1× · see citing works
“It has been assumed that these few infecting cells had somehow managed to form filaments in vivo through an Efg1p/Cph1p-independent mechanism, possibly through activation of the transcription factor Czf1p (8, 12), which had enabled them to extravasate and disseminate to the organs, with supporting evidence for this pr…”
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[7]7. Brown, A. J. P. 2002. Morphogenetic signaling pathways in Candida albicans , p. 95-106. In R. A. Calderone (ed.), Candida and candidiasis. ASM Press, Washington, D.C.
[9]9. Church, G. M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.
[30]30. Sherman, F., G. R. Fink, and J. Hicks. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

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Martel, C. M., Parker, J. E., Bader, O., Weig, M., Gross, U., Warrilow, A. G. S., Rolley, N., Kelly, D. E., & Kelly, S. L. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00348-10 · Cited by 168 · see citing works
The metabolic basis of Candida albicans morphogenesis and quorum sensing.
Han, T.-L., Cannon, R. D., & Villas-Bôas, S. G. (2011) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2011.04.002 · Cited by 173 · see citing works
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Lewis, L. E., Bain, J. M., Lowes, C., Gillespie, C., Rudkin, F. M., Gow, N. A. R., & Erwig, L.-P. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002578 · Cited by 150 · see citing works
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Lionakis, M. S., Iliev, I. D., & Hohl, T. M. (2017) · JCI Insight · doi:10.1172/jci.insight.93156 · Cited by 153 · see citing works
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Nobile, C. J., Solis, N., Myers, C. L., Fay, A. J., Deneault, J.-S., Nantel, A., Mitchell, A. P., & Filler, S. G. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01198.x · Cited by 150 · see citing works
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Moreno-Ruiz, E., Galán-Díez, M., Zhu, W., Fernández-Ruiz, E., d'Enfert, C., Filler, S. G., Cossart, P., & Veiga, E. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01319.x · Cited by 133 · see citing works
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Hall, R. A., De Sordi, L., MacCallum, D. M., Topal, H., Eaton, R., Bloor, J. W., Robinson, G. K., Levin, L. R., Buck, J., Wang, Y., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001193 · Cited by 126 · see citing works
Yeast wall protein 1 of Candida albicans
Granger, B. L., Flenniken, M. L., Davis, D. A., Mitchell, A. P., & Cutler, J. E. (2005) · Microbiology · doi:10.1099/mic.0.27663-0 · Cited by 126 · see citing works
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Dagley, M. J., Gentle, I. E., Beilharz, T. H., Pettolino, F. A., Djordjevic, J. T., Lo, T. L., Uwamahoro, N., Rupasinghe, T., Tull, D. L., McConville, M., et al. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07503.x · Cited by 128 · see citing works
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Pierce, C. G., Chaturvedi, A. K., Lazzell, A. L., Powell, A. T., Saville, S. P., McHardy, S. F., & Lopez-Ribot, J. L. (2015) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2015.12 · Cited by 124 · see citing works
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Self-citation
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Herrero de Dios, C., Roman, E., Alonso Monge, R., & Pla, J. (2010) · Current Protein & Peptide Science · doi:10.2174/138920310794557655 · Cited by 55 · see citing works
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Ardizzoni, A., Pericolini, E., Paulone, S., Orsi, C. F., Castagnoli, A., Oliva, I., Strozzi, E., & Blasi, E. (2018) · PLoS ONE · doi:10.1371/journal.pone.0207262 · Cited by 58 · see citing works
Safeguard function of PU.1 shapes the inflammatory epigenome of neutrophils
Fischer, J., Walter, C., Tönges, A., Aleth, H., Jordão, M. J. C., Leddin, M., Gröning, V., Erdmann, T., Lenz, G., Roth, J., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0343-z · Cited by 56 · see citing works
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Koch, B., Barugahare, A. A., Lo, T. L., Huang, C., Schittenhelm, R. B., Powell, D. R., Beilharz, T. H., & Traven, A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.080 · Cited by 50 · see citing works
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Brown, A. O., Graham, C. E., Cruz, M. R., Singh, K. V., Murray, B. E., Lorenz, M. C., & Garsin, D. A. (2019) · mBio · doi:10.1128/mbio.01334-19 · Cited by 46 · see citing works
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Chen, T., Wagner, A. S., Tams, R. N., Eyer, J. E., Kauffman, S. J., Gann, E. R., Fernandez, E. J., & Reynolds, T. B. (2019) · mBio · doi:10.1128/mbio.01767-19 · Cited by 33 · see citing works
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Luna-Tapia, A., Peters, B. M., Eberle, K. E., Kerns, M. E., Foster, T. P., Marrero, L., Noverr, M. C., Fidel, P. L., & Palmer, G. E. (2015) · Eukaryotic Cell · doi:10.1128/ec.00116-15 · Cited by 35 · see citing works
Lack of Th17 Cell Generation in Patients with Severe Burn Injuries
Inatsu, A., Kogiso, M., Jeschke, M. G., Asai, A., Kobayashi, M., Herndon, D. N., & Suzuki, F. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003235 · Cited by 34 · see citing works
Regulated proteolysis of <scp>C</scp> andida albicans <scp>R</scp> as1 is involved in morphogenesis and quorum sensing regulation
Piispanen, A. E., Grahl, N., Hollomon, J. M., & Hogan, D. A. (2013) · Molecular Microbiology · doi:10.1111/mmi.12268 · Cited by 32 · see citing works
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Hossain, S., Veri, A. O., & Cowen, L. E. (2020) · mBio · doi:10.1128/mbio.00290-20 · Cited by 31 · see citing works
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Sushmitha, T. J., Rajeev, M., Kathirkaman, V., Shivam, S., Rao, T. S., & Pandian, S. K. (2023) · Scientific Reports · doi:10.1038/s41598-023-37851-1 · Cited by 30 · see citing works
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Mohammad, H., Elghazawy, N. H., Eldesouky, H. E., Hegazy, Y. A., Younis, W., Avrimova, L., Hazbun, T., Arafa, R. K., & Seleem, M. N. (2018) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.7b00215 · Cited by 29 · see citing works
Human oral keratinocyte E-cadherin degradation byCandida albicansandCandida glabrata
Pärnänen, P., Meurman, J. H., Samaranayake, L., & Virtanen, I. (2010) · Journal of Oral Pathology & Medicine · doi:10.1111/j.1600-0714.2009.00866.x · Cited by 28 · see citing works
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Chou, H., Glory, A., & Bachewich, C. (2011) · Eukaryotic Cell · doi:10.1128/ec.00263-10 · Cited by 20 · see citing works
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Schena, N. C., Baker, K. M., Stark, A. A., Thomas, D. P., & Cleary, I. A. (2026) · Folia Microbiologica · doi:10.1007/s12223-025-01288-y · Cited by 1 · see citing works

Authors: Saville, S. P., Lazzell, A. L., Monteagudo, C., & Lopez-Ribot, J. L.
Affiliations: The University of Texas at San Antonio Health Science Center (US)
Universitat de València (ES)
Corresponding author: Saville, Stephen P.
ORCID: Monteagudo, Carlos
Lopez-Ribot, Jose L.
Venue: Eukaryotic Cell
Publisher: American Society for Microbiology
Published: 2003-10
Volume: 2
Issue: 5
Pages: 1053-1060
ISSN: 1535-9778 (ISSN-L)
1535-9786
DOI: 10.1128/ec.2.5.1053-1060.2003
PMC: PMC219382
OpenAlex: W2133183053
Cited by: 655
References: 4
Citations by year: 2026: 12 · 2025: 19 · 2024: 20 · 2023: 21 · 2022: 23 · 2021: 32 · 2020: 40 · 2019: 31 · 2018: 31 · 2017: 36 · 2016: 27 · 2015: 33 · 2014: 53 · 2013: 40 · 2012: 30
FWCI: 10.36
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Eukaryotic Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Burroughs Wellcome Fund
U.S. Public Health Service (R03 A105447)
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, yeast-to-hypha transition, morphogenesis, neuregulin-1, fungal virulence, hyphal development, yeast cells, animal models of infection
MeSH terms: Animals, Brain, Candida albicans, Candidiasis, Cell Division, Doxycycline, Female, Genetic Engineering, Kidney, Mice, Inbred BALB C, Promoter Regions, Genetic, Repressor Proteins, Spleen, Yeasts, Gene Expression Regulation, Fungal, Survival Rate, Hyphae, Mice

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EngineeredControl of Cell Morphology In Vivo Reveals Distinct Roles for Yeast andFilamentous Forms of Candida albicans duringInfection

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