Structures of Pathogenic Fungal FKBP12s Reveal Possible Self-Catalysis Function
Abstract
Invasive fungal infections remain difficult to treat and require novel targeting strategies. The 12-kDa FK506-binding protein (FKBP12) is a ubiquitously expressed peptidyl-prolyl isomerase with considerable homology between fungal pathogens and is thus a prime candidate for future targeting efforts to generate a panfungal strategy. Despite decades of research on FKBPs, their substrates and mechanisms of action remain unclear. Here we describe structural, biochemical, and in vivo analyses of FKBP12s from the pathogenic fungi Candida albicans, Candida glabrata, and Aspergillus fumigatus. Strikingly, multiple apo A. fumigatus and C. albicans FKBP12 crystal structures revealed a symmetric, intermolecular interaction involving the deep insertion of an active-site loop proline into the active-site pocket of an adjacent subunit. Such interactions have not been observed in previous FKBP structures. This finding indicates the possibility that this is a self-substrate interaction unique to the A. fumigatus and C. albicans fungal proteins that contain this central proline. Structures obtained with the proline in the cis and trans states provide more data in support of self-catalysis. Moreover, cysteine cross-linking experiments captured the interacting dimer, supporting the idea that it forms in solution. Finally, genetic studies exploring the impact of mutations altering the central proline and an adjacent residue providemore »
- Authors:
-
- Duke Univ. School of Medicine, Durham, NC (United States). Dept. of Biochemistry
- Duke Univ. School of Medicine, Durham, NC (United States). Division of Pediatric Infectious Diseases. Dept. of Pediatrics
- Duke Univ. School of Medicine, Durham, NC (United States). Dept. of Molecular Genetics and Microbiology
- Duke Univ. School of Medicine, Durham, NC (United States). Dept. of Biochemistry; Duke Univ. School of Medicine, Durham, NC (United States). Dept. of Radiology
- Duke Univ. School of Medicine, Durham, NC (United States). Division of Pediatric Infectious Diseases. Dept. of Pediatrics; Duke Univ. School of Medicine, Durham, NC (United States). Dept. of Molecular Genetics and Microbiology
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1626109
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 7; Journal Issue: 2; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Tonthat, Nam K., Juvvadi, Praveen Rao, Zhang, Hengshan, Lee, Soo Chan, Venters, Ron, Spicer, Leonard, Steinbach, William J., Heitman, Joseph, and Schumacher, Maria A. Structures of Pathogenic Fungal FKBP12s Reveal Possible Self-Catalysis Function. United States: N. p., 2016.
Web. doi:10.1128/mbio.00492-16.
Tonthat, Nam K., Juvvadi, Praveen Rao, Zhang, Hengshan, Lee, Soo Chan, Venters, Ron, Spicer, Leonard, Steinbach, William J., Heitman, Joseph, & Schumacher, Maria A. Structures of Pathogenic Fungal FKBP12s Reveal Possible Self-Catalysis Function. United States. https://doi.org/10.1128/mbio.00492-16
Tonthat, Nam K., Juvvadi, Praveen Rao, Zhang, Hengshan, Lee, Soo Chan, Venters, Ron, Spicer, Leonard, Steinbach, William J., Heitman, Joseph, and Schumacher, Maria A. Tue .
"Structures of Pathogenic Fungal FKBP12s Reveal Possible Self-Catalysis Function". United States. https://doi.org/10.1128/mbio.00492-16. https://www.osti.gov/servlets/purl/1626109.
@article{osti_1626109,
title = {Structures of Pathogenic Fungal FKBP12s Reveal Possible Self-Catalysis Function},
author = {Tonthat, Nam K. and Juvvadi, Praveen Rao and Zhang, Hengshan and Lee, Soo Chan and Venters, Ron and Spicer, Leonard and Steinbach, William J. and Heitman, Joseph and Schumacher, Maria A.},
abstractNote = {Invasive fungal infections remain difficult to treat and require novel targeting strategies. The 12-kDa FK506-binding protein (FKBP12) is a ubiquitously expressed peptidyl-prolyl isomerase with considerable homology between fungal pathogens and is thus a prime candidate for future targeting efforts to generate a panfungal strategy. Despite decades of research on FKBPs, their substrates and mechanisms of action remain unclear. Here we describe structural, biochemical, and in vivo analyses of FKBP12s from the pathogenic fungi Candida albicans, Candida glabrata, and Aspergillus fumigatus. Strikingly, multiple apo A. fumigatus and C. albicans FKBP12 crystal structures revealed a symmetric, intermolecular interaction involving the deep insertion of an active-site loop proline into the active-site pocket of an adjacent subunit. Such interactions have not been observed in previous FKBP structures. This finding indicates the possibility that this is a self-substrate interaction unique to the A. fumigatus and C. albicans fungal proteins that contain this central proline. Structures obtained with the proline in the cis and trans states provide more data in support of self-catalysis. Moreover, cysteine cross-linking experiments captured the interacting dimer, supporting the idea that it forms in solution. Finally, genetic studies exploring the impact of mutations altering the central proline and an adjacent residue provide evidence that any dimeric state formed in vivo, where FKBP12 concentrations are low, is transient. Taken together, these findings suggest a unique mechanism of self-substrate regulation by fungal FKBP12s, lending further novel understanding of this protein for future drug-targeting efforts.},
doi = {10.1128/mbio.00492-16},
journal = {mBio (Online)},
number = 2,
volume = 7,
place = {United States},
year = {Tue Apr 26 00:00:00 EDT 2016},
month = {Tue Apr 26 00:00:00 EDT 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journalFigures / Tables:
TABLE 1: Data collection and refinement statistics for C. albicans FKBP12 structures
All figures and tables
(10 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases
journal, January 2004
- Fanghänel, Jörg
- Frontiers in Bioscience, Vol. 9, Issue 1-3
PPIase catalysis by human FK506-binding protein proceeds through a conformational twist mechanism.
journal, February 1992
- Park, S. T.; Aldape, R. A.; Futer, O.
- Journal of Biological Chemistry, Vol. 267, Issue 5
Structural Insights into Substrate Binding by Pv FKBP35, a Peptidylprolyl cis-trans Isomerase from the Human Malarial Parasite Plasmodium vivax
journal, February 2013
- Alag, Reema; Balakrishna, Asha Manikkoth; Rajan, Sreekanth
- Eukaryotic Cell, Vol. 12, Issue 4
Rapamycin Exerts Antifungal Activity In Vitro and In Vivo against Mucor circinelloides via FKBP12-Dependent Inhibition of Tor
journal, December 2011
- Bastidas, Robert J.; Shertz, Cecelia A.; Lee, Soo Chan
- Eukaryotic Cell, Vol. 11, Issue 3
A Conformational Unfolding Reaction Activates Phage fd for the Infection of Escherichia coli
journal, October 2007
- Eckert, Barbara; Schmid, Franz X.
- Journal of Molecular Biology, Vol. 373, Issue 2
Characterization of the FKBP12-Encoding Genes in Aspergillus fumigatus
journal, September 2015
- Falloon, Katie; Juvvadi, Praveen R.; Richards, Amber D.
- PLOS ONE, Vol. 10, Issue 9
Prolyl isomerization as a molecular timer in phage infection
journal, June 2005
- Eckert, Barbara; Martin, Andreas; Balbach, Jochen
- Nature Structural & Molecular Biology, Vol. 12, Issue 7
Rapamycin and Less Immunosuppressive Analogs Are Toxic to Candida albicans and Cryptococcus neoformans via FKBP12-Dependent Inhibition of TOR
journal, November 2001
- Cruz, M. Cristina; Goldstein, Alan L.; Blankenship, Jill
- Antimicrobial Agents and Chemotherapy, Vol. 45, Issue 11
FKBP12, the 12-kDa FK506-binding protein, is a physiologic regulator of the cell cycle
journal, February 2001
- Aghdasi, B.; Ye, K.; Resnick, A.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 5
Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation
journal, June 1992
- Clipstone, Neil A.; Crabtree, Gerald R.
- Nature, Vol. 357, Issue 6380
Proline cis-trans Isomerization Controls Autoinhibition of a Signaling Protein
journal, February 2007
- Sarkar, Paramita; Reichman, Charles; Saleh, Tamjeed
- Molecular Cell, Vol. 25, Issue 3
Cyclosporin A, FK-506, and Rapamycin: Pharmacologic Probes of Lymphocyte Signal Transduction
journal, April 1992
- Sigal, N. H.; Dumont, F. J.
- Annual Review of Immunology, Vol. 10, Issue 1
Native State Proline Isomerization: An Intrinsic Molecular Switch †
journal, August 2003
- Andreotti, Amy H.
- Biochemistry, Vol. 42, Issue 32
Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes
journal, April 1990
- Harrison, Richard K.; Stein, Ross L.
- Biochemistry, Vol. 29, Issue 16
Mechanism of Enzymatic and Nonenzymatic Prolyl Cis-Trans Isomerization
book, January 1993
- Stein, Ross L.
- Accessory Folding Proteins
X-ray Structure of a Monomeric Cyclophilin A-Cyclosporin A Crystal Complex at 2·1 Å Resolution
journal, December 1993
- Mikol, Vincent; Kallen, Jörg; Pflügl, Gaston
- Journal of Molecular Biology, Vol. 234, Issue 4
Requirements for peptidyl-prolyl isomerization activity: A comprehensive mutational analysis of the substrate-binding cavity of FK506-binding protein 12
journal, December 2007
- Ikura, Teikichi; Ito, Nobutoshi
- Protein Science, Vol. 16, Issue 12
Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections
journal, June 2007
- Steinbach, William J.; Reedy, Jennifer L.; Cramer, Robert A.
- Nature Reviews Microbiology, Vol. 5, Issue 6
Functional diversity and pharmacological profiles of the FKBPs and their complexes with small natural ligands
journal, December 2012
- Galat, Andrzej
- Cellular and Molecular Life Sciences, Vol. 70, Issue 18
Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus: Analysis of the calcineurin complex in Aspergillus fumigatus
journal, November 2011
- Juvvadi, Praveen Rao; Fortwendel, Jarrod R.; Rogg, Luise E.
- Molecular Microbiology, Vol. 82, Issue 5
Sequence-Specific and Phosphorylation-Dependent Proline Isomerization: A Potential Mitotic Regulatory Mechanism
journal, December 1997
- Yaffe, M. B.
- Science, Vol. 278, Issue 5345
Prolyl cis-trans isomerization as a molecular timer
journal, September 2007
- Lu, Kun Ping; Finn, Greg; Lee, Tae Ho
- Nature Chemical Biology, Vol. 3, Issue 10
Crystal Structure of the PP2A Phosphatase Activator: Implications for Its PP2A-Specific PPIase Activity
journal, August 2006
- Leulliot, Nicolas; Vicentini, Giorgia; Jordens, Jan
- Molecular Cell, Vol. 23, Issue 3
Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12
journal, January 1998
- Shou, Weinian; Aghdasi, Bahman; Armstrong, Dawna L.
- Nature, Vol. 391, Issue 6666
Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues
journal, November 1975
- Brandts, John F.; Halvorson, Herbert R.; Brennan, Maureen
- Biochemistry, Vol. 14, Issue 22
A cavity with an appropriate size is the basis of the PPIase activity
journal, January 2008
- Ikura, T.; Kinoshita, K.; Ito, N.
- Protein Engineering Design and Selection, Vol. 21, Issue 2
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands.
journal, December 1994
- Cardenas, M. E.; Hemenway, C.; Muir, R. S.
- The EMBO Journal, Vol. 13, Issue 24
Solution structure of FKBP, a rotamase enzyme and receptor for FK506 and rapamycin
journal, May 1991
- Michnick, S.; Rosen, M.; Wandless, T.
- Science, Vol. 252, Issue 5007
Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex
journal, May 1991
- Van Duyne, G.; Standaert, R.; Karplus, P.
- Science, Vol. 252, Issue 5007
FK506 Binding Protein Mutational Analysis: DEFINING THE SURFACE RESIDUE CONTRIBUTIONS TO STABILITY OF THE CALCINEURIN CO-COMPLEX
journal, August 1995
- Futer, Olga; DeCenzo, Maureen T.; Aldape, Robert A.
- Journal of Biological Chemistry, Vol. 270, Issue 32
Genetic Involvement of a cAMP-Dependent Protein Kinase in a G Protein Signaling Pathway Regulating Morphological and Chemical Transitions in Aspergillus nidulans
journal, February 2001
- Shimizu, Kiminori; Keller, Nancy P.
- Genetics, Vol. 157, Issue 2
Acid catalysis of the formation of the slow-folding species of RNase A: Evidence that the reaction is proline isomerization
journal, October 1978
- Schmid, F. X.; Baldwin, R. L.
- Proceedings of the National Academy of Sciences, Vol. 75, Issue 10
Chemistry and biology of the immunophilins and their immunosuppressive ligands
journal, January 1991
- Schreiber, S.
- Science, Vol. 251, Issue 4991
FKBP Family Proteins: Immunophilins with Versatile Biological Functions
journal, January 2008
- Kang, Cong Bao; Hong, Ye; Dhe-Paganon, Sirano
- Neurosignals, Vol. 16, Issue 4
Structural characterization of a proline-driven conformational switch within the Itk SH2 domain
journal, October 2002
- Mallis, Robert J.; Brazin, Kristine N.; Fulton, D. Bruce
- Nature Structural Biology, Vol. 9, Issue 12
Structures of Immunophilins and their Ligand Complexes
journal, August 2003
- Dornan, Jacqueline; Taylor, Paul; Walkinshaw, Malcolm
- Current Topics in Medicinal Chemistry, Vol. 3, Issue 12
FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin
journal, June 1992
- O'Keefe, Stephen J.; Tamura, Jun'ichi; Kincaid, Randall L.
- Nature, Vol. 357, Issue 6380
Crystal structure of recombinant human T-cell cyclophilin A at 2.5 A resolution.
journal, November 1991
- Ke, H. M.; Zydowsky, L. D.; Liu, J.
- Proceedings of the National Academy of Sciences, Vol. 88, Issue 21
Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands.
journal, December 1994
- Cardenas, M. E.; Hemenway, C.; Muir, R. S.
- The EMBO Journal, Vol. 13, Issue 24
Calcineurin: Structure, function, and inhibition
journal, February 1999
- Hemenway, Charles S.; Heitman, Joseph
- Cell Biochemistry and Biophysics, Vol. 30, Issue 1
Functional diversity and pharmacological profiles of the FKBPs and their complexes with small natural ligands
journal, December 2012
- Galat, Andrzej
- Cellular and Molecular Life Sciences, Vol. 70, Issue 18
Crystal Structure of the PP2A Phosphatase Activator: Implications for Its PP2A-Specific PPIase Activity
journal, August 2006
- Leulliot, Nicolas; Vicentini, Giorgia; Jordens, Jan
- Molecular Cell, Vol. 23, Issue 3
Proline cis-trans Isomerization Controls Autoinhibition of a Signaling Protein
journal, February 2007
- Sarkar, Paramita; Reichman, Charles; Saleh, Tamjeed
- Molecular Cell, Vol. 25, Issue 3
Structural and Functional Analysis of the Mitotic Rotamase Pin1 Suggests Substrate Recognition Is Phosphorylation Dependent
journal, June 1997
- Ranganathan, Rama; Lu, Kun Ping; Hunter, Tony
- Cell, Vol. 89, Issue 6
Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes
journal, April 1990
- Harrison, Richard K.; Stein, Ross L.
- Biochemistry, Vol. 29, Issue 16
Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12
journal, January 1998
- Shou, Weinian; Aghdasi, Bahman; Armstrong, Dawna L.
- Nature, Vol. 391, Issue 6666
Prolyl cis-trans isomerization as a molecular timer
journal, September 2007
- Lu, Kun Ping; Finn, Greg; Lee, Tae Ho
- Nature Chemical Biology, Vol. 3, Issue 10
Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections
journal, June 2007
- Steinbach, William J.; Reedy, Jennifer L.; Cramer, Robert A.
- Nature Reviews Microbiology, Vol. 5, Issue 6
Structural characterization of a proline-driven conformational switch within the Itk SH2 domain
journal, October 2002
- Mallis, Robert J.; Brazin, Kristine N.; Fulton, D. Bruce
- Nature Structural Biology, Vol. 9, Issue 12
FKBP12, the 12-kDa FK506-binding protein, is a physiologic regulator of the cell cycle
journal, February 2001
- Aghdasi, B.; Ye, K.; Resnick, A.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 5
Acid catalysis of the formation of the slow-folding species of RNase A: Evidence that the reaction is proline isomerization
journal, October 1978
- Schmid, F. X.; Baldwin, R. L.
- Proceedings of the National Academy of Sciences, Vol. 75, Issue 10
Crystal structure of recombinant human T-cell cyclophilin A at 2.5 A resolution.
journal, November 1991
- Ke, H. M.; Zydowsky, L. D.; Liu, J.
- Proceedings of the National Academy of Sciences, Vol. 88, Issue 21
FK506 Binding Protein Mutational Analysis: DEFINING THE SURFACE RESIDUE CONTRIBUTIONS TO STABILITY OF THE CALCINEURIN CO-COMPLEX
journal, August 1995
- Futer, Olga; DeCenzo, Maureen T.; Aldape, Robert A.
- Journal of Biological Chemistry, Vol. 270, Issue 32
Genetic Involvement of a cAMP-Dependent Protein Kinase in a G Protein Signaling Pathway Regulating Morphological and Chemical Transitions in Aspergillus nidulans
journal, February 2001
- Shimizu, Kiminori; Keller, Nancy P.
- Genetics, Vol. 157, Issue 2
A cavity with an appropriate size is the basis of the PPIase activity
journal, January 2008
- Ikura, T.; Kinoshita, K.; Ito, N.
- Protein Engineering Design and Selection, Vol. 21, Issue 2
Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus: Analysis of the calcineurin complex in Aspergillus fumigatus
journal, November 2011
- Juvvadi, Praveen Rao; Fortwendel, Jarrod R.; Rogg, Luise E.
- Molecular Microbiology, Vol. 82, Issue 5
Chemistry and biology of the immunophilins and their immunosuppressive ligands
journal, January 1991
- Schreiber, S.
- Science, Vol. 251, Issue 4991
Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex
journal, May 1991
- Van Duyne, G.; Standaert, R.; Karplus, P.
- Science, Vol. 252, Issue 5007
Sequence-Specific and Phosphorylation-Dependent Proline Isomerization: A Potential Mitotic Regulatory Mechanism
journal, December 1997
- Yaffe, M. B.
- Science, Vol. 278, Issue 5345
Calcineurin Controls Growth, Morphology, and Pathogenicity in Aspergillus fumigatus
journal, July 2006
- Steinbach, William J.; Cramer, Robert A.; Perfect, B. Zachary
- Eukaryotic Cell, Vol. 5, Issue 7
Cyclosporin A, FK-506, and Rapamycin: Pharmacologic Probes of Lymphocyte Signal Transduction
journal, April 1992
- Sigal, N. H.; Dumont, F. J.
- Annual Review of Immunology, Vol. 10, Issue 1
FKBP Family Proteins: Immunophilins with Versatile Biological Functions
journal, January 2008
- Kang, Cong Bao; Hong, Ye; Dhe-Paganon, Sirano
- Neurosignals, Vol. 16, Issue 4
Characterization of the FKBP12-Encoding Genes in Aspergillus fumigatus
journal, September 2015
- Falloon, Katie; Juvvadi, Praveen R.; Richards, Amber D.
- PLOS ONE, Vol. 10, Issue 9
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Structures of Immunophilins and their Ligand Complexes
journal, August 2003
- Dornan, Jacqueline; Taylor, Paul; Walkinshaw, Malcolm
- Current Topics in Medicinal Chemistry, Vol. 3, Issue 12
Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases
journal, January 2004
- Fanghänel, Jörg
- Frontiers in Bioscience, Vol. 9, Issue 1-3
Works referencing / citing this record:
Harnessing calcineurin-FK506-FKBP12 crystal structures from invasive fungal pathogens to develop antifungal agents
journal, September 2019
- Juvvadi, Praveen R.; Fox, David; Bobay, Benjamin G.
- Nature Communications, Vol. 10, Issue 1
1H, 13C, 15 N chemical shift assignments of the FKBP12 protein from the pathogenic fungi Candida auris and Candida glabrata
journal, January 2020
- Bashir, Qamar; LeMaster, David M.; Hernández, Griselda
- Biomolecular NMR Assignments, Vol. 14, Issue 1
FKBP12-Dependent Inhibition of Calcineurin Mediates Immunosuppressive Antifungal Drug Action in Malassezia
journal, October 2017
- Ianiri, Giuseppe; Applen Clancey, Shelly; Lee, Soo Chan
- mBio, Vol. 8, Issue 5
In Vitro and In Vivo Assessment of FK506 Analogs as Novel Antifungal Drug Candidates
journal, September 2018
- Lee, Yeonseon; Lee, Kyung-Tae; Lee, Soo Jung
- Antimicrobial Agents and Chemotherapy, Vol. 62, Issue 11
Genome-wide analyses of genes encoding FK506-binding proteins reveal their involvement in abiotic stress responses in apple
journal, September 2018
- Dong, Qinglong; Mao, Ke; Duan, Dingyue
- BMC Genomics, Vol. 19, Issue 1
Calcineurin in fungal virulence and drug resistance: Prospects for harnessing targeted inhibition of calcineurin for an antifungal therapeutic approach
journal, June 2016
- Juvvadi, Praveen R.; Lee, Soo Chan; Heitman, Joseph
- Virulence, Vol. 8, Issue 2
FKBP12-Dependent Inhibition of Calcineurin Mediates Immunosuppressive Antifungal Drug Action in Malassezia
journal, October 2017
- Ianiri, Giuseppe; Applen Clancey, Shelly; Lee, Soo Chan
- mBio, Vol. 8, Issue 5
Ser/Thr protein phosphatases in fungi: structure, regulation and function
journal, May 2019
- Ariño, Joaquín; Velázquez, Diego; Casamayor, Antonio
- Microbial Cell, Vol. 6, Issue 5
Protein-Protein Interactions in Candida albicans
journal, August 2019
- Schoeters, Floris; Van Dijck, Patrick
- Frontiers in Microbiology, Vol. 10
Figures / Tables found in this record:
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.