Mucoricin is a ricin-like toxin that is critical for the pathogenesis of mucormycosis

Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We demonstrate that Mucorales fungi produce a toxin, which plays a central role in virulence. Polyclonal antibodies against this toxin inhibit its ability to damage human cells in vitro...

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Published inNature microbiology Vol. 6; no. 3; pp. 313 - 326
Main Authors Soliman, Sameh S. M., Baldin, Clara, Gu, Yiyou, Singh, Shakti, Gebremariam, Teclegiorgis, Swidergall, Marc, Alqarihi, Abdullah, Youssef, Eman G., Alkhazraji, Sondus, Pikoulas, Antonis, Perske, Christina, Venkataramani, Vivek, Rich, Abigail, Bruno, Vincent M., Hotopp, Julie Dunning, Mantis, Nicolas J., Edwards, John E., Filler, Scott G., Chamilos, Georgios, Vitetta, Ellen S., Ibrahim, Ashraf S.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.03.2021
Nature Publishing Group
Subjects
631/326/193/2542
692/420/254
Animals
Antitoxins - immunology
Antitoxins - pharmacology
Antitoxins - therapeutic use
Apoptosis
Biomedical and Life Sciences
Capillary Permeability
Cells, Cultured
Cross Reactions
Fungi
Humans
Hyphae - chemistry
Hyphae - pathogenicity
Infectious Diseases
Lectins - metabolism
Life Sciences
Medical Microbiology
Mice
Microbiology
Mucorales
Mucorales - chemistry
Mucorales - classification
Mucorales - genetics
Mucorales - pathogenicity
Mucormycosis
Mucormycosis - microbiology
Mucormycosis - pathology
Mucormycosis - prevention & control
Mycotoxins - chemistry
Mycotoxins - genetics
Mycotoxins - immunology
Mycotoxins - metabolism
N-Glycosylase
Necrosis
Parasitology
Pathogenesis
Permeability
Polyclonal antibodies
Protein biosynthesis
Rhizopus - chemistry
Rhizopus - genetics
Rhizopus - pathogenicity
Ribosome Inactivating Proteins - metabolism
Ricin
Ricin - chemistry
Ricin - immunology
Ricin - metabolism
RNA Interference
RNA-mediated interference
Structure-function relationships
Therapeutic applications
Therapeutic targets
Virology
Virulence
Virulence - drug effects
Virulence - genetics
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Abstract Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We demonstrate that Mucorales fungi produce a toxin, which plays a central role in virulence. Polyclonal antibodies against this toxin inhibit its ability to damage human cells in vitro and prevent hypovolemic shock, organ necrosis and death in mice with mucormycosis. Inhibition of the toxin in Rhizopus delemar through RNA interference compromises the ability of the fungus to damage host cells and attenuates virulence in mice. This 17 kDa toxin has structural and functional features of the plant toxin ricin, including the ability to inhibit protein synthesis through its N -glycosylase activity, the existence of a motif that mediates vascular leak and a lectin sequence. Antibodies against the toxin inhibit R. delemar- or toxin-mediated vascular permeability in vitro and cross react with ricin. A monoclonal anti-ricin B chain antibody binds to the toxin and also inhibits its ability to cause vascular permeability. Therefore, we propose the name ‘mucoricin’ for this toxin. Not only is mucoricin important in the pathogenesis of mucormycosis but our data suggest that a ricin-like toxin is produced by organisms beyond the plant and bacterial kingdoms. Importantly, mucoricin should be a promising therapeutic target. Mucorales fungi produce a ricin-like toxin, mucoricin, which is required for fungal pathogenesis and represents a potential therapeutic target.
AbstractList Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We demonstrate that Mucorales fungi produce a toxin, which plays a central role in virulence. Polyclonal antibodies against this toxin inhibit its ability to damage human cells in vitro and prevent hypovolemic shock, organ necrosis and death in mice with mucormycosis. Inhibition of the toxin in Rhizopus delemar through RNA interference compromises the ability of the fungus to damage host cells and attenuates virulence in mice. This 17 kDa toxin has structural and functional features of the plant toxin ricin, including the ability to inhibit protein synthesis through its N-glycosylase activity, the existence of a motif that mediates vascular leak and a lectin sequence. Antibodies against the toxin inhibit R. delemar- or toxin-mediated vascular permeability in vitro and cross react with ricin. A monoclonal anti-ricin B chain antibody binds to the toxin and also inhibits its ability to cause vascular permeability. Therefore, we propose the name 'mucoricin' for this toxin. Not only is mucoricin important in the pathogenesis of mucormycosis but our data suggest that a ricin-like toxin is produced by organisms beyond the plant and bacterial kingdoms. Importantly, mucoricin should be a promising therapeutic target.
Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We demonstrate that Mucorales fungi produce a toxin, which plays a central role in virulence. Polyclonal antibodies against this toxin inhibit its ability to damage human cells in vitro and prevent hypovolemic shock, organ necrosis and death in mice with mucormycosis. Inhibition of the toxin in Rhizopus delemar through RNA interference compromises the ability of the fungus to damage host cells and attenuates virulence in mice. This 17 kDa toxin has structural and functional features of the plant toxin ricin, including the ability to inhibit protein synthesis through its N -glycosylase activity, the existence of a motif that mediates vascular leak and a lectin sequence. Antibodies against the toxin inhibit R. delemar- or toxin-mediated vascular permeability in vitro and cross react with ricin. A monoclonal anti-ricin B chain antibody binds to the toxin and also inhibits its ability to cause vascular permeability. Therefore, we propose the name ‘mucoricin’ for this toxin. Not only is mucoricin important in the pathogenesis of mucormycosis but our data suggest that a ricin-like toxin is produced by organisms beyond the plant and bacterial kingdoms. Importantly, mucoricin should be a promising therapeutic target. Mucorales fungi produce a ricin-like toxin, mucoricin, which is required for fungal pathogenesis and represents a potential therapeutic target.
Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We now demonstrate that Mucorales fungi produce a toxin that plays a central role in virulence. Polyclonal antibodies against this toxin inhibit its ability to damage human cells in vitro, and prevent hypovolemic shock, organ necrosis, and death in mice with mucormycosis. RNAi inhibition of the toxin in Rhizopus delemar, compromises the ability of the fungus to damage host cells and attenuates virulence in mice. This 17 kDa toxin has structural and functional features of the plant toxin, ricin, including the ability to inhibit protein synthesis by its N-glycosylase activity, the existence of a motif that mediates vascular leak, and a lectin sequence. Antibodies against the toxin inhibit R. delemar- or toxin-mediated vascular permeability in vitro and cross-react with ricin. A monoclonal anti-ricin B chain antibody binds to the toxin and also inhibits its ability to cause vascular permeability. Therefore, we propose the name “mucoricin” for this toxin. Not only is mucoricin important in the pathogenesis of mucormycosis but our data suggest that a ricin-like toxin is produced by organisms beyond the plant and bacterial kingdoms. Importantly, mucoricin should be a promising therapeutic target.
Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We demonstrate that Mucorales fungi produce a toxin, which plays a central role in virulence. Polyclonal antibodies against this toxin inhibit its ability to damage human cells in vitro and prevent hypovolemic shock, organ necrosis and death in mice with mucormycosis. Inhibition of the toxin in Rhizopus delemar through RNA interference compromises the ability of the fungus to damage host cells and attenuates virulence in mice. This 17 kDa toxin has structural and functional features of the plant toxin ricin, including the ability to inhibit protein synthesis through its N-glycosylase activity, the existence of a motif that mediates vascular leak and a lectin sequence. Antibodies against the toxin inhibit R. delemar- or toxin-mediated vascular permeability in vitro and cross react with ricin. A monoclonal anti-ricin B chain antibody binds to the toxin and also inhibits its ability to cause vascular permeability. Therefore, we propose the name ‘mucoricin’ for this toxin. Not only is mucoricin important in the pathogenesis of mucormycosis but our data suggest that a ricin-like toxin is produced by organisms beyond the plant and bacterial kingdoms. Importantly, mucoricin should be a promising therapeutic target.Mucorales fungi produce a ricin-like toxin, mucoricin, which is required for fungal pathogenesis and represents a potential therapeutic target.
Author Soliman, Sameh S. M.
Hotopp, Julie Dunning
Youssef, Eman G.
Gu, Yiyou
Alkhazraji, Sondus
Chamilos, Georgios
Perske, Christina
Swidergall, Marc
Filler, Scott G.
Ibrahim, Ashraf S.
Edwards, John E.
Venkataramani, Vivek
Baldin, Clara
Gebremariam, Teclegiorgis
Alqarihi, Abdullah
Rich, Abigail
Pikoulas, Antonis
Singh, Shakti
Vitetta, Ellen S.
Mantis, Nicolas J.
Bruno, Vincent M.
AuthorAffiliation 7 Department of Pathology, University Medicine Göttingen, Göttingen, Germany
3 Department of Biological Chemistry, Medical University of Innsbruck, Innsbruck, Austria
4 David Geffen School of Medicine at UCLA, Los Angeles, Ca, U.S.A
2 College of Pharmacy and Research Institute for Medical and Health Sciences, University of Sharjah, P.O. Box 27272, Sharjah, United Arab Emirates
6 Department of Medicine, University of Crete, Foundation for Research and Technology, 71300 Heraklion, Crete, Greece
11 New York State Department of Health, Wadsworth Center, Albany, NY, U.S.A
1 Division of Infectious Diseases, The Lundquist Institute for Biomedical Innovation at Harbor-University of California at Los Angeles (UCLA) Medical Center, Torrance, CA, U.S.A
10 Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, U.S.A
5 Department of Biotechnology and Life Sciences, Faculty of Postgraduate Studies for Advanced Sciences, Beni-Suef University, Beni-Suef, Egypt
9 De
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  email: ibrahim@lundquist.org
  organization: Division of Infectious Diseases, The Lundquist Institute for Biomedical Innovation, Harbor-University of California at Los Angeles (UCLA) Medical Center, David Geffen School of Medicine at UCLA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33462434$$D View this record in MEDLINE/PubMed
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Notes Equal contribution
Author contributions
S.S.M.S. conceived, designed and performed studies to purify and identify the toxin, and screen its activity in vitro and in vivo and wrote the manuscript. C.B. generated mucoricin mutants and characterized their virulence in vitro and in vivo and conducted the antibody efficacy studies. Y.G. helped in animal studies, conducted confocal microscopy, cross reactivity studies, and RIP activity studies. S.S. designed and performed homology modeling, cross reactivity studies, and toxin secretion studies. T.G. helped in the animal studies. M.S. performed the necrosis/apoptosis assay and the mouse immunohistochemistry studies. A.A. performed permeability studies, E.G.Y. performed sequence alignment and gene ontology studies. S.A. purified recombinant toxin and polyclonal antibodies. A.P. and G.C. provided and performed the human immunohistochemistry studies. C.P. and V.V. performed and interpreted the mouse histology studies. AR carried out studies on cross-reactivity of mucoricin and ricin. V.M.B. and J.D.H. performed phylogenetic studies and blast search of mucoricin in Mucorales. N.J.M. generated and characterized the 8A1 monoclonal antibody. J.E.E. and S.G.F. provided intellectual advice, designed studies, and edited the manuscript. E.S.V. conceived, designed and carried out studies of cross reactivity, provided reagents and expertise on ricin and helped write the manuscript. A.S.I. conceived, designed, coordinated and supervised the studies, performed experiments, analyzed data, and wrote the manuscript along with comments from co-authors.
ORCID 0000-0001-6521-0998
0000-0002-5083-8640
0000-0003-3787-8530
0000-0002-2295-058X
0000-0002-5261-6267
0000-0002-7301-1945
0000-0003-3862-986X
0000-0001-7278-3700
0000-0002-7691-615X
0000-0002-3167-1347
0000-0003-4408-6398
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC7914224
PMID 33462434
PQID 2493255135
PQPubID 2069616
PageCount 14
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_7914224
proquest_journals_2493255135
crossref_primary_10_1038_s41564_020_00837_0
pubmed_primary_33462434
springer_journals_10_1038_s41564_020_00837_0
PublicationCentury 2000
PublicationDate 2021-03-01
PublicationDateYYYYMMDD 2021-03-01
PublicationDate_xml – month: 03
  year: 2021
  text: 2021-03-01
  day: 01
PublicationDecade 2020
PublicationPlace London
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PublicationTitle Nature microbiology
PublicationTitleAbbrev Nat Microbiol
PublicationTitleAlternate Nat Microbiol
PublicationYear 2021
Publisher Nature Publishing Group UK
Nature Publishing Group
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
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Snippet Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We demonstrate that Mucorales fungi produce a...
Fungi of the order Mucorales cause mucormycosis, a lethal infection with an incompletely understood pathogenesis. We now demonstrate that Mucorales fungi...
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proquest
crossref
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springer
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Publisher
StartPage 313
SubjectTerms 631/326/193/2542
692/420/254
Animals
Antitoxins - immunology
Antitoxins - pharmacology
Antitoxins - therapeutic use
Apoptosis
Biomedical and Life Sciences
Capillary Permeability
Cells, Cultured
Cross Reactions
Fungi
Humans
Hyphae - chemistry
Hyphae - pathogenicity
Infectious Diseases
Lectins - metabolism
Life Sciences
Medical Microbiology
Mice
Microbiology
Mucorales
Mucorales - chemistry
Mucorales - classification
Mucorales - genetics
Mucorales - pathogenicity
Mucormycosis
Mucormycosis - microbiology
Mucormycosis - pathology
Mucormycosis - prevention & control
Mycotoxins - chemistry
Mycotoxins - genetics
Mycotoxins - immunology
Mycotoxins - metabolism
N-Glycosylase
Necrosis
Parasitology
Pathogenesis
Permeability
Polyclonal antibodies
Protein biosynthesis
Rhizopus - chemistry
Rhizopus - genetics
Rhizopus - pathogenicity
Ribosome Inactivating Proteins - metabolism
Ricin
Ricin - chemistry
Ricin - immunology
Ricin - metabolism
RNA Interference
RNA-mediated interference
Structure-function relationships
Therapeutic applications
Therapeutic targets
Virology
Virulence
Virulence - drug effects
Virulence - genetics
Title Mucoricin is a ricin-like toxin that is critical for the pathogenesis of mucormycosis
URI https://link.springer.com/article/10.1038/s41564-020-00837-0
https://www.ncbi.nlm.nih.gov/pubmed/33462434
https://www.proquest.com/docview/2493255135
https://pubmed.ncbi.nlm.nih.gov/PMC7914224
Volume 6
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