Cryptococcus neoformans can form titan-like cells in vitro in response to multiple signals

Trevijano-Contador, Nuria; de Oliveira, Haroldo Cesar; García-Rodas, Rocío; Rossi, Suélen Andreia; Llorente, Irene; Zaballos, Ángel; Janbon, Guilhem; Ariño, Joaquín; Zaragoza, Óscar

doi:10.1371/journal.ppat.1007007

Cited by 124Fungal Infections and StudiesFungal and yeast genetics researchAntifungal resistance and susceptibility

Cryptococcus neoformans can form titan-like cells in vitro in response to multiple signals

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Trevijano-Contador, Nuria, de Oliveira, Haroldo Cesar, García-Rodas, Rocío, Rossi, Suélen Andreia, Llorente, Irene, Zaballos, Ángel, Janbon, Guilhem, Ariño, Joaquín +1 more·2018·PLoS Pathogens

DOI 10.1371/journal.ppat.1007007PMC PMC5959073

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Abstract

ABSTRACT Cryptococcus neoformans is an encapsulated pathogenic yeast that can change the size of the cells during infection. In particular, this process can occur by enlarging the size of the capsule without modifying the size of the cell body, or by increasing the diameter of the cell body, which is normally accompanied by an increase of the capsule too. This last process leads to the formation of cells of an abnormal enlarged size denominated titan cells. Previous works characterized titan cell formation during pulmonary infection but research on this topic has been hampered due to the difficulty to obtain them in vitro . In this work, we describe in vitro conditions (low nutrient, serum supplemented medium at neutral pH) that promote the transition from regular to titan-like cells. Moreover, addition of azide and static incubation of the cultures in a CO 2 enriched atmosphere favored cellular enlargement. This transition occurred at low cell densities, suggesting that the process was regulated by quorum sensing molecules and was independent of the cryptococcal serotype/species. Transition to titan-like cell formation was impaired by pharmacological inhibition of PKC and TOR signaling pathways. Mutants affected in capsule synthesis did not form titan-like cells. Analysis of the gene expression profile in titan-like cells indicated that they overexpressed membrane proteins and transporters, being the gene encoding the Cig1 mannoprotein involved in iron uptake from heme groups the gene most differentially expressed compared to cells of regular size. We also investigated the gene expression profile of titan-like cells isolated from mice, and observed that during infection these cells mainly overexpressed genes related to metabolism and respiration. In summary, our work provides a new alternative method to investigate titan cell formation devoid the bioethical problems that involve animal experimentation. AUTHOR SUMMARY Cryptococcus neoformans is a fungal pathogen that has a significant incidence in HIV+ patients in particular, in Subsaharian Africa, Asia and South America. This yeast poses an excellent model to investigate fungal virulence because it develops many strategies to adapt to the host and evade the immune response. One of the adaptation mechanisms involves the formation of Titan Cells, which are yeast of an abnormal large size. However, research on these cells has been limited to in vivo studies (mainly in mice) because they were not reproducibly found in vitro. In this work, we describe several conditions that induce the appearance of cells that mimic titan cells, and that we denominated as titan-like cells. The main factor that induced titan-like cells was the addition of serum to nutrient limited media. This has allowed to easily performing new approaches to characterize several signaling pathways involved in their development. We found that the formation of these cells is regulated by quorum sensing molecules, and that pathways such as PKC and TOR kinases regulate the process of cellular enlargement. We have also to perform transcriptomic analysis, which led to the identification of new genes that could be involved in the process. This work will open different research lines that will contribute to the elucidation of the role of these cells during infection and on the development of cryptococcal disease.

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The major pathway regulating titan cell formation is the cAMP/PKA/Rim101 signaling cascade.
“The major pathway regulating titan cell formation is the cAMP/PKA/Rim101 signaling cascade (Dambuza et al. 2018; Hommel et al. 2018; Trevijano-Contador et al. 2018)”
From Genetic analysis of Hsp90 function in Cryptococcus neoformans highlights key roles in stress tolerance and virulence (2022) · cites this paper as Trevijano-Contador et al. 2018

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TUP1 disruption in Cryptococcus neoformans uncovers a peptide‐mediated density‐dependent growth phenomenon that mimics quorum sensing
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TOR Signaling in Fission Yeast
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UGD1 , Encoding the Cryptococcus neoformans UDP-Glucose Dehydrogenase, Is Essential for Growth at 37°C and for Capsule Biosynthesis
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Cleavage of human fibronectin and other basement membrane-associated proteins by a Cryptococcus neoformans serine proteinase
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Metabolites released by Cryptococcus neoformans var. neoformans and var. gattii differentially affect human neutrophil function
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Identification of metabolites of importance in the pathogenesis of pulmonary cryptococcoma using nuclear magnetic resonance spectroscopy
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The formation of titan cells in Cryptococcus neoformans depends on the mouse strain and correlates with induction of Th2-type responses
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The Metalloprotease, Mpr1, Engages AnnexinA2 to Promote the Transcytosis of Fungal Cells across the Blood-Brain Barrier
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Cryptococcus neoformans induces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian model Galleria mellonella
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Genetic Analyses of a Hybrid Cross Between Serotypes A and D Strains of the Human Pathogenic Fungus Cryptococcus neoformans
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Further analysis of the CAP59 locus of Cryptococcus neoformans: structure defined by forced expression and description of a new ribosomal protein-encoding gene
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The Fungal Cell Wall: Candida, Cryptococcus, and Aspergillus Species
Garcia-Rubio, R., de Oliveira, H. C., Rivera, J., & Trevijano-Contador, N. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02993 · Cited by 917 · see citing works
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The Cryptococcus neoformans Titan cell is an inducible and regulated morphotype underlying pathogenesis
Dambuza, I. M., Drake, T., Chapuis, A., Zhou, X., Correia, J., Taylor-Smith, L., LeGrave, N., Rasmussen, T., Fisher, M. C., Bicanic, T., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1006978 · Cited by 182 · see citing works
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Titan cells formation in Cryptococcus neoformans is finely tuned by environmental conditions and modulated by positive and negative genetic regulators
Hommel, B., Mukaremera, L., Cordero, R. J. B., Coelho, C., Desjardins, C. A., Sturny-Leclère, A., Janbon, G., Perfect, J. R., Fraser, J. A., Casadevall, A., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1006982 · Cited by 143 · see citing works
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Immune Response of Galleria mellonella against Human Fungal Pathogens
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The cAMP/Protein Kinase A Pathway Regulates Virulence and Adaptation to Host Conditions in Cryptococcus neoformans
Caza, M., & Kronstad, J. W. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00212 · Cited by 107 · see citing works
Quorum Sensing in Fungal Species
Tian, X., Ding, H., Ke, W., & Wang, L. (2021) · Annual Review of Microbiology · doi:10.1146/annurev-micro-060321-045510 · Cited by 91 · see citing works
A dissemination-prone morphotype enhances extrapulmonary organ entry by Cryptococcus neoformans
Denham, S. T., Brammer, B., Chung, K. Y., Wambaugh, M. A., Bednarek, J. M., Guo, L., Moreau, C. T., & Brown, J. C. S. (2022) · Cell Host & Microbe · doi:10.1016/j.chom.2022.08.017 · Cited by 80 · see citing works
A titanic drug resistance threat in Cryptococcus neoformans
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The Dynamic Fungal Genome: Polyploidy, Aneuploidy and Copy Number Variation in Response to Stress
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Studying fungal pathogens of humans and fungal infections: fungal diversity and diversity of approaches
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Phenotypic Variability Correlates with Clinical Outcome in Cryptococcus Isolates Obtained from Botswanan HIV/AIDS Patients
Fernandes, K. E., Brockway, A., Haverkamp, M. R., Cuomo, C. A., van Ogtrop, F., Perfect, J. R., & Carter, D. A. (2018) · mBio · doi:10.1128/mbio.02016-18 · Cited by 62 · see citing works
How Environmental Fungi Cause a Range of Clinical Outcomes in Susceptible Hosts
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Studying fungal pathogens of humans and fungal infections: fungal diversity and diversity of approaches
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Advances in understanding the evolution of fungal genome architecture
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Activation of Meiotic Genes Mediates Ploidy Reduction during Cryptococcal Infection
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The Evolution of Sexual Reproduction and the Mating-Type Locus: Links to Pathogenesis of Cryptococcus Human Pathogenic Fungi
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Intranasal Inoculation of Cryptococcus neoformans in Mice Produces Nasal Infection with Rapid Brain Dissemination
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Macrophage Mediated Immunomodulation During Cryptococcus Pulmonary Infection
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The population genetics of ploidy change in unicellular fungi
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Genomic Variation across a Clinical Cryptococcus Population Linked to Disease Outcome
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Animal Models of Cryptococcus neoformans in Identifying Immune Parameters Associated With Primary Infection and Reactivation of Latent Infection
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The Cyclin Cln1 Controls Polyploid Titan Cell Formation following a Stress-Induced G2 Arrest in Cryptococcus
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Mitotic Recombination and Adaptive Genomic Changes in Human Pathogenic Fungi
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Cryptococcus escapes host immunity: What do we know?
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Fungal resilience and host–pathogen interactions: Future perspectives and opportunities
Brown, A. J. P. (2022) · Parasite Immunology · doi:10.1111/pim.12946 · Cited by 40 · see citing works
The Transcription Factor Pdr802 Regulates Titan Cell Formation and Pathogenicity of Cryptococcus neoformans
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Dangerous Liaisons: Interactions of Cryptococcus neoformans with Host Phagocytes
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Cell wall composition in Cryptococcus neoformans is media dependent and alters host response, inducing protective immunity
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Cryptococcus neoforman s rapidly invades the murine brain by sequential breaching of airway and endothelial tissues barriers, followed by engulfment by microglia
Francis, V. I., Liddle, C., Camacho, E., Kulkarni, M., Santos, S. R. D., Harvey, J. A., Ballou, E. R., Thomson, D. D., Brown, G. D., Hardwick, J. M., et al. (2024) · mBio · doi:10.1128/mbio.03078-23 · Cited by 30 · see citing works
The Cryptococcus neoformans Titan Cell: From In Vivo Phenomenon to In Vitro Model
Zhou, X., & Ballou, E. R. (2018) · Current Clinical Microbiology Reports · doi:10.1007/s40588-018-0107-9 · Cited by 30 · see citing works
Landscape of gene expression variation of natural isolates of Cryptococcus neoformans in response to biologically relevant stresses
Yu, C.-H. A., Chen, Y., Desjardins, C. A., Tenor, J. L., Toffaletti, D. L., Giamberardino, C. D., Litvintseva, A. P., Perfect, J. R., & Cuomo, C. A. (2019) · Microbial Genomics · doi:10.1099/mgen.0.000319 · Cited by 32 · see citing works
Cryptococcal Titan Cells: When Yeast Cells Are All Grown up
García‐Rodas, R., de Oliveira, H. C., Trevijano‐Contador, N., & Zaragoza, Ó. (2018) · Current topics in microbiology and immunology · doi:10.1007/82_2018_145 · Cited by 32 · see citing works
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Chromatin-Mediated Regulation of Genome Plasticity in Human Fungal Pathogens
Buscaino, A. (2019) · Genes · doi:10.3390/genes10110855 · Cited by 32 · see citing works
Titan cell formation is unique to Cryptococcus species complex
Dyląg, M., Colón-Reyes, R. J., & Kozubowski, L. (2020) · Virulence · doi:10.1080/21505594.2020.1772657 · Cited by 31 · see citing works
Genetic analysis of Hsp90 function in Cryptococcus neoformans highlights key roles in stress tolerance and virulence
Fu, C., Beattie, S. R., Jezewski, A. J., Robbins, N., Whitesell, L., Krysan, D. J., & Cowen, L. E. (2022) · Genetics · doi:10.1093/genetics/iyab164 · Cited by 31 · see citing works
Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
Araújo, G. R. D. S., Alcantara, C. D. L., Rodrigues, N., de Souza, W., Pontes, B., & Frasés, S. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.609244 · Cited by 27 · see citing works
Titan Cells and Yeast Forms of Cryptococcus neoformans and Cryptococcus gattii Are Recognized by GXMR-CAR
dos Santos, M. H., Machado, M. P., Kumaresan, P. R., & da Silva, T. A. (2021) · Microorganisms · doi:10.3390/microorganisms9091886 · Cited by 27 · see citing works
Analysis of Cryptococcal Extracellular Vesicles: Experimental Approaches for Studying Their Diversity Among Multiple Isolates, Kinetics of Production, Methods of Separation, and Detection in Cultures of Titan Cells
Reis, F. C. G., Gimenez, B., Jozefowicz, L. J., Castelli, R. F., Martins, S. T., Alves, L. R., de Oliveira, H. C., & Rodrigues, M. L. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.00125-21 · Cited by 26 · see citing works
Cell Wall Integrity Pathway Involved in Morphogenesis, Virulence and Antifungal Susceptibility in Cryptococcus neoformans
de Oliveira, H. C., Rossi, S. A., García-Barbazán, I., Zaragoza, Ó., & Trevijano‐Contador, N. (2021) · Journal of Fungi · doi:10.3390/jof7100831 · Cited by 25 · see citing works
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Human IgM Inhibits the Formation of Titan-Like Cells in Cryptococcus neoformans
Trevijano‐Contador, N., Pianalto, K. M., Nichols, C. B., Zaragoza, Ó., Alspaugh, J. A., & Pirofski, L. (2020) · Infection and Immunity · doi:10.1128/iai.00046-20 · Cited by 24 · see citing works
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The COMPASS Complex Regulates Fungal Development and Virulence through Histone Crosstalk in the Fungal Pathogen Cryptococcus neoformans
Liu, R., Chen, X., Zhao, F., Jiang, Y., Lu, Z., Ji, H., Feng, Y., Li, J., Zhang, H., Zheng, J., et al. (2023) · Journal of Fungi · doi:10.3390/jof9060672 · Cited by 24 · see citing works
The role of Toll-like receptor 9 in a murine model of Cryptococcus gattii infection
da Silva-Júnior, E. B., Firmino-Cruz, L., Guimarães-de-Oliveira, J. C., De-Medeiros, J. V. R., Nascimento, D. D. O., Freire-de-Lima, M., de Brito‐Gitirana, L., Morrot, A., Previato, J. O., Mendonça‐Previato, L., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-80959-5 · Cited by 23 · see citing works
An in vitro method for inducing titan cells reveals novel features of yeast-to-titan switching in the human fungal pathogen Cryptococcus gattii
Saidykhan, L., Correia, J., Romanyuk, A. V., Peacock, A. F. A., Desanti, G. E., Taylor-Smith, L. M., Makarova, M., Ballou, E. R., & May, R. C. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010321 · Cited by 21 · see citing works
A Glucuronoxylomannan Epitope Exhibits Serotype-Specific Accessibility and Redistributes towards the Capsule Surface during Titanization of the Fungal Pathogen Cryptococcus neoformans
Probert, M. A., Zhou, X., Goodall, M. D., Johnston, S. A., Bielska, E., Ballou, E. R., & May, R. C. (2019) · Infection and Immunity · doi:10.1128/iai.00731-18 · Cited by 23 · see citing works
Dynamic genome plasticity during unisexual reproduction in the human fungal pathogen Cryptococcus deneoformans
Fu, C., Davy, A., Holmes, S., Sun, S., Yadav, V., Gusa, A. A., Coelho, M. A., & Heitman, J. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009935 · Cited by 21 · see citing works
Epistatic genetic interactions govern morphogenesis during sexual reproduction and infection in a global human fungal pathogen
Sun, S., Roth, C., Averette, A. F., Magwene, P. M., & Heitman, J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122293119 · Cited by 22 · see citing works
Similar evolutionary trajectories in an environmental Cryptococcus neoformans isolate after human and murine infection
Sephton-Clark, P., McConnell, S. A., Grossman, N. T., Baker, R. P., Dragotakes, Q., Fan, Y., Fu, M. S., Gerbig, G. R., Greengo, S. D., Hardwick, J. M., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2217111120 · Cited by 21 · see citing works
Importance of Clinical Isolates in Cryptococcus neoformans Research
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Authors: Trevijano-Contador, N., de Oliveira, H. C., García-Rodas, R., Rossi, S. A., Llorente, I., Zaballos, Á., Janbon, G., Ariño, J., & Zaragoza, Ó.
Affiliations: Instituto de Salud Carlos III (ES)
Institut Pasteur (FR)
Corresponding author: Zaragoza, Óscar
ORCID: de Oliveira, Haroldo Cesar
Rossi, Suélen Andreia
Llorente, Irene
Zaballos, Ángel
Janbon, Guilhem
Ariño, Joaquín
Zaragoza, Óscar
Venue: PLoS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2018-05-18
Volume: 14
Issue: 5
Pages: e1007007
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.1007007
PMC: PMC5959073
OpenAlex: W2803592889
Cited by: 124
References: 109
Citations by year: 2026: 20 · 2025: 11 · 2024: 9 · 2023: 8 · 2022: 16 · 2021: 18 · 2020: 15 · 2019: 18 · 2018: 9
FWCI: 11.71
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: PLoS Pathogens (publishedVersion, cc-by)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
HAL (submittedVersion, cc-by)
Americanae (AECID Library) (submittedVersion, other-oa)
Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
Funders: Secretaría de Estado de Investigación, Desarrollo e Innovación (SAF2014-54336-R, BFU2014-54591-C2-1-P)
Agència de Gestió d’Ajuts Universitaris i de Recerca (Ajut 2014SGR-4)
Dirección General de Investigación Científica y Técnica (SAF2017-86192-R, BFU2017-82574-P)
Topics: Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Keywords: Cryptococcus neoformans, titan cells, quorum sensing, PKC signaling, iron limitation, calnexin, coatomer complex, carbohydrate metabolism, azide, elevated CO2, in vitro cell culture
MeSH terms: RAW 264.7 Cells, Animals, Cryptococcosis, Cryptococcus neoformans, Genes, Fungal, Humans, Macrophages, Male, Mice, Inbred C57BL, Models, Biological, Phagocytosis, Phenotype, Signal Transduction, Gene Expression Profiling, Mice, Quorum Sensing, Host-Pathogen Interactions

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Cryptococcus neoformans can form titan-like cells in vitro in response to multiple signals

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