Threonine-Rich Repeats Increase Fibronectin Binding in the Candidaalbicans Adhesin Als5p
Open accessAbstract
Commensal and pathogenic states of Candida albicans depend on cell surface-expressed adhesins, including those of the Als family. Mature Als proteins consist of a 300-residue N-terminal region predicted to have an immunoglobulin (Ig)-like fold, a 104-residue conserved Thr-rich region (T), a central domain of a variable number of tandem repeats (TR) of a 36-residue Thr-rich sequence, and a heavily glycosylated C-terminal Ser/Thr-rich stalk region, also of variable length (N. K. Gaur and S. A. Klotz, Infect. Immun. 65: 5289-5294, 1997). Domain deletions in ALS5 were expressed in Saccharomyces cerevisiae to excrete soluble protein and for surface display. Far UV circular dichroism indicated that soluble Ig-T showed a single negative peak at 212 nm, consistent with previous data indicating that this region has high beta-sheet content with very little alpha-helix. A truncation of Als5p with six tandem repeats (Ig-T-TR(6)) gave spectra with additional negative ellipticity at 200 nm and, at 227 to 240 nm, spectra characteristic of a structure with a similar fraction of beta-sheet but with additional structural elements as well. Soluble Als5p Ig-T and Ig-T-TR(6) fragments bound to fibronectin in vitro, but the inclusion of the TR region substantially increased affinity. Cellular adhesion assays with S. cerevisiae showed that the Ig-T domain mediated adherence to fibronectin and that TR repeats greatly increased cell-to-cell aggregation. Thus, the TR region of Als5p modulated the structure of the Ig-T region, augmented cell adhesion activity through increased binding to mammalian ligands, and simultaneously promoted fungal cell-cell interactions.
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The absence of tandem repeats reduced the binding affinity of Als5.
“In addition, Rauceo et al. [38] reported that the absence of tandem repeats reduced the binding affinity of Als5.”
From Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells (2007) · cites this paper as [38]
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Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells
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“However, the conserved Als tandem repeats in Als5p facilitate adhesion to fibronectin and greatly increase cell–cell aggregation (Rauceo et al., 2006).”
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Self-citationStructure and Function of Glycosylated Tandem Repeats from Candida albicans Als Adhesins
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“The Ig-like regions can interact with diverse mammalian proteins, presumably in a way analogous to antibody-antigen binding, as has been shown in the homologous protein -agglutinin from Saccharomyces cerevisiae (8, 24, 26, 35).”
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“The CRD is believed to enhance the presentation of the adhesive N-terminal region away from the cell surface (Rauceo et al., 2006; Frank et al., 2010).”
BackgroundNanoscale analysis of caspofungin-induced cell surface remodelling in Candida albicans
El-Kirat-Chatel, S., Beaussart, A., Alsteens, D., Jackson, D., Lipke, P., & Dufrêne, Y. (2012) · Nanoscale · doi:10.1039/c2nr33215a · Cited by 56 · see citing works
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“…region of about 310 aa) together with the threonine-rich region A B C D © 2011 Blackwell Publishing Ltd, Molecular Microbiology, 80, 1667–1679 (T region of about 105 aa), which has been shown previously to be necessary for proper protein folding and secretion to the medium (Rauceo et al., 2006).”
BackgroundInfluentialStudy of Candida albicans and its interactions with the host: A mini review
Tsai, P.-W., Chen, Y.-T., Hsu, P., & Lan, C. (2013) · Biomedicine · doi:10.1016/j.biomed.2012.12.004 · Cited by 53 · see citing works
“[76] Rauceo JM, De Armond R, Otoo H, Kahn PC, Klotz SA, Gaur NK, et al.”
BackgroundGenerating cell surface diversity in Candida albicans and other fungal pathogens.
Nather, K., & Munro, C. (2008) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2008.01263.x · Cited by 63 · see citing works
Unzipping a Functional Microbial Amyloid
Alsteens, D., Ramsook, C. B., Lipke, P. N., & Dufrêne, Y. F. (2012) · ACS Nano · doi:10.1021/nn3025699 · Cited by 51 · see citing works
Self-citationSingle-cell force spectroscopy of Als-mediated fungal adhesion
Alsteens, D., Beaussart, A., Derclaye, S., El‐Kirat‐Chatel, S., Park, H. R., Lipke, P. N., & Dufrêne, Y. F. (2013) · Analytical Methods · doi:10.1039/c3ay40473k · Cited by 50 · see citing works
Self-citationTkachenko, A. N., Mykhailiuk, P. K., Afonin, S., Radchenko, D. S., Kubyshkin, V., Ulrich, A. S., & Komarov, I. V. (2012) · Angewandte Chemie International Edition · doi:10.1002/anie.201208069 · Cited by 50 · see citing works
Dehullu, J., Valotteau, C., Herman-Bausier, P., Garcia-Sherman, M. C., Mittelviefhaus, M., Vorholt, J., Lipke, P., & Dufrêne, Y. (2019) · Nano letters (Print) · doi:10.1021/acs.nanolett.9b01010 · Cited by 46 · see citing works
Self-citationZhao, X.-M., Oh, S.-H., & Hoyer, L. (2007) · Microbiology · doi:10.1099/mic.0.2006/005017-0 · Cited by 48 · see citing works
“cerevisiae suggests that the tandem repeat and C-terminal domain of Als5p may have more than a structural role (Rauceo et al., 2006).”
BackgroundMethodLagree, K., & Mitchell, A. P. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0024-2016 · Cited by 40 · see citing works
“Spectroscopic analysis argues that this TR function is mediated by an effect on the folding of the immunoglobulin-like domain (13).”
BackgroundInfluentialCantero, P. D., Lengsfeld, C., Prill, S. K. ‐., Subanović, M., Román, E., Plá, J., & Ernst, J. F. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05723.x · Cited by 39 · see citing works
Hashash, R. A., Younes, S., Bahnan, W., Koussa, J., Maalouf, K., Dimassi, H. I., & Khalaf, R. A. (2010) · Mycoses · doi:10.1111/j.1439-0507.2010.01883.x · Cited by 37 · see citing works
Brandhorst, T. T., Roy, R. M., Wüthrich, M., Nanjappa, S. G., Filutowicz, H. I., Galles, K., Tonelli, M., McCaslin, D. R., Satyshur, K. A., & Klein, B. S. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003464 · Cited by 36 · see citing works
“Nevertheless, reduced length is a feature known to impact the function of other adhesins [24].”
BackgroundFunctional Heterogeneity of the UpaH Autotransporter Protein from Uropathogenic Escherichia coli
Allsopp, L. P., Beloin, C., Moriel, D. G., Totsika, M., Ghigo, J., & Schembri, M. A. (2012) · Journal of Bacteriology · doi:10.1128/jb.01264-12 · Cited by 34 · see citing works
An Amyloid Core Sequence in the Major Candida albicans Adhesin Als1p Mediates Cell-Cell Adhesion
Ho, V., Herman-Bausier, P., Shaw, C., Conrad, K., Garcia-Sherman, M. C., Draghi, J., Dufrêne, Y., Lipke, P., & Rauceo, J. M. (2019) · mBio · doi:10.1128/mbio.01766-19 · Cited by 28 · see citing works
“The tandem repeats mediate hydrophobic effect binding to diverse ligands, including Als proteins themselves (i.e., homotypic binding [13, 25, 26]).”
Self-citationSharifmoghadam, M. R., & Valdivieso, M. ‐. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06375.x · Cited by 31 · see citing works
“A role of the internal repeats in adhesion has been reported for C. albicans Als5 (Rauceo et al., 2006).”
BackgroundInfluentialPeptide Detection of Fungal Functional Amyloids in Infected Tissue
Garcia, M. C., Lysak, N., Filonenko, A., Richards, H., Sobonya, R. E., Klotz, S. A., & Lipke, P. N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086067 · Cited by 29 · see citing works
“Each member of the Als family contain N-terminal Ig-like invasin domains (Ig) which define substrate specificity and a variable number of 36-amino acid tandem repeats (TR domain) that contribute to substrate binding [31–34].”
BackgroundSelf-citationMolecular Basis for Strain Variation in the Saccharomyces cerevisiae Adhesin Flo11p
Barua, S., Li, L., Lipke, P. N., & Dranginis, A. M. (2016) · mSphere · doi:10.1128/msphere.00129-16 · Cited by 28 · see citing works
“albicans adhesin Als5p, the repeats interact through a hydrophobic effect and stabilize binding to fibronectin (28).”
BackgroundSelf-citationSimón, O., Williams, T., Asensio, A. C., Ros, S., Gaya, A., Caballero, P., & Possee, R. D. (2008) · Journal of Virology · doi:10.1128/jvi.00099-08 · Cited by 28 · see citing works
“379 The presence of a threonine-rich region, that plays an important role in adhesion to cell 380 membrane glycoproteins and cell matrix proteins of bacteria (24, 43), suggests an 381 AC CE PT ED”
BackgroundParallel expansion and divergence of an adhesin family in pathogenic yeasts
Smoak, R. A., Snyder, L. F., Fassler, J. S., & He, B. Z. (2023) · GENETICS · doi:10.1093/genetics/iyad024 · Cited by 25 · see citing works
Sticking to the Subject: Multifunctionality in Microbial Adhesins
Lipke, P., & Ragonis-Bachar, P. (2023) · Journal of Fungi · doi:10.3390/jof9040419 · Cited by 25 · see citing works
“This part of the Als sequences mediates adhesion to plastic surfaces as well as to fibronectin [82,83].”
BackgroundSelf-citationSheets, A., & Geme, J. W. S. (2010) · Journal of Bacteriology · doi:10.1128/jb.00933-10 · Cited by 25 · see citing works
“These observations parallel observations with eukaryotic microorganisms (27), suggesting that variation in peptide repeats may be a widespread mechanism among microorganisms for generating cell surface antigenic and/or functional diversity.”
BackgroundResultThe protein secretory pathway of <i>Candida albicans</i>
Fonzi, W. A. (2009) · Mycoses · doi:10.1111/j.1439-0507.2008.01673.x · Cited by 25 · see citing works
Adhesins in Opportunistic Fungal Pathogens
Zordan, R., & Cormack, B. (2012) · ASM Press eBooks · doi:10.1128/9781555817176.ch16 · Cited by 28 · see citing works
Bai, Y., Wang, J., Zhang, Z., Shi, P., Luo, H., Huang, H., Luo, C., & Yao, B. (2010) · Microbial Cell Factories · doi:10.1186/1475-2859-9-33 · Cited by 24 · see citing works
“Threonine-rich regions have been reported to be involved in fibronectin binding [ 18 ], unidirectional transport of a mineralocorticoid receptor into the nucleus [19], vanadate resistance [20], and resistance to HIV by binding to a specific receptor [21].”
Cho, T., Aoyama, T., Toyoda, M., Nakayama, H., Chibana, H., & Kaminishi, H. (2007) · Nippon Ishinkin Gakkai Zasshi · doi:10.3314/jjmm.48.159 · Cited by 22 · see citing works
Zhao, X.-M., Oh, S.-H., Coleman, D. A., & Hoyer, L. (2011) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00769.x · Cited by 22 · see citing works
“cerevisiae binding to fibronectin (Rauceo et al., 2006; Frank et al., 2010).”
BackgroundGlycoconjugate structure and function in fungal cell walls
Gonzalez, M., de Groot, P. W. J., Klis, F. M., & Lipke, P. N. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374546-0.00010-9 · Cited by 22 · see citing works
Self-citationCoding fungal tandem repeats as generators of fungal diversity
Levdansky, E., Sharon, H., & Osherov, N. (2008) · Fungal Biology Reviews · doi:10.1016/j.fbr.2008.08.001 · Cited by 20 · see citing works
“…by securely presenting the N-terminal ligand-binding domain towards the substrate (Sheppard et al., 2004) or (c) alter the spatial structure of the binding domain thereby increasing its affinity to the substrate (Rauceo et al., 2006). gal tandem repeats as generators of fungal diversity, Fungal”
BackgroundSatała, D., Satała, G., Zawrotniak, M., & Kozik, A. (2021) · BMC Microbiology · doi:10.1186/s12866-021-02235-w · Cited by 22 · see citing works
Tkachenko, A. N., Mykhailiuk, P. K., Afonin, S., Radchenko, D. S., Kubyshkin, V., Ulrich, A. S., & Komarov, I. V. (2012) · Angewandte Chemie · doi:10.1002/ange.201208069 · Cited by 19 · see citing works
Ovchinnikova, E. S., van der Mei, H. C., Krom, B. P., & Busscher, H. J. (2013) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2013.04.015 · Cited by 19 · see citing works
Structure and Conservation of Amyloid Spines From the Candida albicans Als5 Adhesin
Golan, N., Perov, S., Landau, M., & Lipke, P. N. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.926959 · Cited by 17 · see citing works
“We have also found that the T region is essential for secretion and processing in yeast (Rauceo et al., 2006).”
Self-citationAhmad, M. F., Yadav, B., Kumar, P., Puri, A., Mazumder, M., Ali, A., Gourinath, S., Muthuswami, R., & Komath, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035305 · Cited by 16 · see citing works
“The protein has also been shown to be capable of mediating endothelial cell invasion and its N-terminal domain has been shown to be important for adherence [10,11].”
BackgroundResultInfluentialPhenotypic Variability in a Coinfection With Three Independent Candida parapsilosis Lineages
Gómez-Molero, E., Willis, J. R., Dudakova, A., Carreté, L., Weig, M., Groß, U., Gácser, A., Gabaldón, T., & Bader, O. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01994 · Cited by 15 · see citing works
Homepeptide Repeats: Implications for Protein Structure, Function and Evolution
Muthukumarasamy, U., Benazir, B., Patra, S., Vaishnavi, M. K., Gurusaran, M., Kanagarajan, S., Jeyakanthan, J., & Sekar, K. (2012) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2012.04.001 · Cited by 13 · see citing works
“It was hypothesized that repeat expansion and contraction may provide a mechanism for rapid morphological evolutionary changes [37] and that this expansion and contraction may be facilitated by replicative slippage [38,12].”
BackgroundAnalysis of flocculins in Ashbya gossypii reveals FIG2 regulation by TEC1
Grünler, A., Walther, A., Lämmel, J., & Wendland, J. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2010.04.001 · Cited by 13 · see citing works
Does Candida albicans Als5p Amyloid Play a Role in Commensalism in Caenorhabditis elegans?
Bois, M., Singh, S., Samlalsingh, A., Lipke, P., & Garcia, M. C. (2013) · Eukaryotic Cell · doi:10.1128/ec.00020-13 · Cited by 14 · see citing works
Self-citationThe Cell Wall: Glycoproteins, Remodeling, and Regulation
Munro, C. A., & Richard, M. L. (2014) · ASM Press eBooks · doi:10.1128/9781555817176.ch14 · Cited by 13 · see citing works
Ikeda, K., Inoue, K., Kitagawa, H., Meguro, H., Shimoi, S., & Park, P. (2012) · InTech eBooks · doi:10.5772/30801 · Cited by 12 · see citing works
“In addition to INT1, agglutinin family proteins, ALA1 and ALS1, and the fibronectin binding protein, FLS5, were also involved in blastospore adhesion (Fu et al., 1998; Rauceo et al., 2006).”
BackgroundImpact of Genetic Background on Allele Selection in a Highly Mutable Candida albicans Gene, PNG2
Zhang, N., Cannon, R. D., Holland, B. R., Patchett, M. L., & Schmid, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009614 · Cited by 11 · see citing works
“An effect of changes in repeat numbers on the adhesive function of the protein has been demonstrated experimentally for Als5p [17].”
BackgroundLi, J., Liu, Y., Zhu, H., & Zhang, K. (2016) · Scientific Reports · doi:10.1038/srep22609 · Cited by 11 · see citing works
Tekaia, F., Dujon, B., & Richard, G. (2013) · Eukaryotic Cell · doi:10.1128/ec.00001-13 · Cited by 11 · see citing works
“were shown to be important for yeast cellular adhesion to epithelial cells or to fibronectin (12, 13).”
BackgroundIbe, C., Walker, L. A., Gow, N. A. R., & Munro, C. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-50409-4_16 · Cited by 10 · see citing works
Lagree, K., & Mitchell, A. P. (2017) · ASM Press eBooks · doi:10.1128/9781555819583.ch42 · Cited by 9 · see citing works
The Long and the Short of Bacterial Adhesion Regulation
Thanassi, D. (2010) · Journal of Bacteriology · doi:10.1128/jb.01345-10 · Cited by 10 · see citing works
“Repetitive sequence elements have been shown to provide a source of expression and antigenic variation in surface-exposed adhesins in both bacterial and eukaryotic cells (2, 4, 7, 11).”
BackgroundRima, M., Villeneuve-Faure, C., Soumbo, M., Garah, F. E., Pilloux, L., Roques, C. G., & Makasheva, K. (2024) · Biomaterials Science · doi:10.1039/d4bm00099d · Cited by 9 · see citing works
Recent Advances in Vaginal Delivery for the Treatment of Vulvovaginal Candidiasis
Kaur, S., & Kaur, S. (2020) · Current Molecular Pharmacology · doi:10.2174/1573405616666200621200047 · Cited by 9 · see citing works
Candida albicans Cell Wall Mediated Virulence
Munro, C. (2010) · Springer eBooks · doi:10.1007/978-3-642-03150-2_4 · Cited by 12 · see citing works
Lim, S. J., Noor, N. D. M., Sabri, S., Ali, M. S. M., Salleh, A. B., & Oslan, S. N. (2024) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2023.2300757 · Cited by 8 · see citing works
“The external ligand-binding of NT-Ca Als3 was shown to facilitate the fungal adherence to one of the ECM proteins-fibronectin (Rauceo et al., 2006); its mutation in PBC evidently exhibited CaALS3 D − / − -like adhesion (J. Lin et al., 2014).”
Biological Roles of Protein-Coding Tandem Repeats in the Yeast Candida Albicans
Wilkins, M., Zhang, N., & Schmid, J. (2018) · Journal of Fungi · doi:10.3390/jof4030078 · Cited by 8 · see citing works
“These could for instance generate, through TR mutations, habitat-specific adhesins [39,43,44,69] or alterations of the wall [16,46,47,50,70,71].”
BackgroundAspergillus nidulans Pmts form heterodimers in all pairwise combinations
Kriangkripipat, T., & Momany, M. (2014) · FEBS Open Bio · doi:10.1016/j.fob.2014.03.006 · Cited by 8 · see citing works
von Ranke, N. V., Bello, M. L., Cabral, L., Castro, H., & Rodrigues, C. (2018) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2017.1417159 · Cited by 7 · see citing works
“albicans (Bamford et al., 2015; Chan & Lipke, 2014; Garcia-Sherman et al., 2014; Otoo et al., 2008; Rauceo et al., 2006) although other studies suggest that the AFR has little contribution to the C.”
ResultCandida albicans Biofilm Development and Its Genetic Control
Desai, J. V., & Mitchell, A. P. (2015) · ASM Press eBooks · doi:10.1128/9781555817466.ch5 · Cited by 7 · see citing works
19F-Labeled amino acids for NMR structure analysis of membrane-bound peptides
Komarov, I. V., Afonin, S., & Ulrich, A. S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812733-9.00010-6 · Cited by 7 · see citing works
Saravanan, K. M., & Ponnuraj, K. (2018) · Journal of Molecular Recognition · doi:10.1002/jmr.2768 · Cited by 7 · see citing works
“It was shown that the sequence repeats in a protein enriched with amino acid Thr could increase fibronectin binding.(47) From our compositional analysis of tandem repeats, it is found that FnBPs contain Glu/Thr rich tandem repeats.”
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Inhibition of enteroaggregative Escherichia coli cell adhesion in-vitro by designed peptides
Gupta, D., Sarkar, S., Sharma, M., Thapa, B. R., & Chakraborti, A. (2016) · Microbial Pathogenesis · doi:10.1016/j.micpath.2016.06.014 · Cited by 5 · see citing works
Defining Key Residues of the Swi1 Prion Domain in Prion Formation and Maintenance
Goncharoff, D. K., Cabral, R., Applebey, S. V., Pagadala, M. S., Du, Z., & Li, L. (2021) · Molecular and Cellular Biology · doi:10.1128/mcb.00044-21 · Cited by 5 · see citing works
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Encounters with Mammalian Cells: Survival Strategies of Candida Species
Vylkova, S., & Lorenz, M. (2012) · ASM Press eBooks · doi:10.1128/9781555817176.ch17 · Cited by 8 · see citing works
Atomic Force Microscopy of Living Cells
Alsteens, D., & Dufrêne, Y. F. (2014) · Neuromethods · doi:10.1007/978-1-62703-983-3_10 · Cited by 3 · see citing works
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Pärnänen, P. (2010) · Työväentutkimus Vuosikirja · Cited by 2 · see citing works
Genome Plasticity inCandida albicans
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- Authors
- Rauceo, J. M., De Armond, R., Otoo, H., Kahn, P. C., Klotz, S. A., Gaur, N. K., & Lipke, P. N.
- Affiliations
- City University of New York (US)
- Southern Arizona VA Health Care System, Tucson, Arizona
- Rutgers, The State University of New Jersey (US)
- University of Arizona (US)
- Southern Arizona VA Health Care System (US)
- Venue
- Eukaryotic Cell
- Publisher
- American Society for Microbiology
- Published
- 2006-10
- Volume
- 5
- Issue
- 10
- Pages
- 1664-1673
- ISSN
- 1535-9778 (ISSN-L)
- 1535-9786
- PMC
- PMC1595330
- OpenAlex
- W2146537281
- Cited by
- 115
- References
- 38
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 5 · 2017: 5 · 2016: 4 · 2015: 3 · 2014: 14 · 2013: 9 · 2012: 11
- FWCI
- 4.08
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Locations
- Eukaryotic Cell (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- U.S. Public Health Service (S06 60654)
- National Institute of General Medical Sciences (F31GM070122)
- National Center for Research Resources (RR 030307)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Keywords
- Candida albicans, fibronectin binding, immunoglobulin-like domains, protein secondary structure, β-sheet content, cell adhesion, cell-cell aggregation, fungal virulence
- MeSH terms
- Animals, Candida albicans, Cell Adhesion, Circular Dichroism, Concanavalin A, Fibronectins, Fungal Proteins, Horseradish Peroxidase, Immunoglobulins, Peptide Fragments, Protein Binding, Substrate Specificity, Threonine, Yeasts, Cell Adhesion Molecules, Protein Structure, Secondary, Protein Structure, Tertiary, Repetitive Sequences, Amino Acid
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