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Article ; Online: Globoside and the mucosal pH mediate parvovirus B19 entry through the epithelial barrier.

Suter, Corinne / Colakovic, Minela / Bieri, Jan / Gultom, Mitra / Dijkman, Ronald / Ros, Carlos

2023 Volume 19, Issue 5, Page(s) e1011402

Abstract: Parvovirus B19 (B19V) is transmitted primarily via the respiratory route, however, the mechanism involved remains unknown. B19V targets a restricted receptor expressed in erythroid progenitor cells in the bone marrow. However, B19V shifts the receptor ... ...

Abstract	Parvovirus B19 (B19V) is transmitted primarily via the respiratory route, however, the mechanism involved remains unknown. B19V targets a restricted receptor expressed in erythroid progenitor cells in the bone marrow. However, B19V shifts the receptor under acidic conditions and targets the widely expressed globoside. The pH-dependent interaction with globoside may allow virus entry through the naturally acidic nasal mucosa. To test this hypothesis, MDCK II cells and well-differentiated human airway epithelial cell (hAEC) cultures were grown on porous membranes and used as models to study the interaction of B19V with the epithelial barrier. Globoside expression was detected in polarized MDCK II cells and the ciliated cell population of well-differentiated hAEC cultures. Under the acidic conditions of the nasal mucosa, virus attachment and transcytosis occurred without productive infection. Neither virus attachment nor transcytosis was observed under neutral pH conditions or in globoside knockout cells, demonstrating the concerted role of globoside and acidic pH in the transcellular transport of B19V. Globoside-dependent virus uptake involved VP2 and occurred by a clathrin-independent pathway that is cholesterol and dynamin-dependent. This study provides mechanistic insight into the transmission of B19V through the respiratory route and reveals novel vulnerability factors of the epithelial barrier to viruses.
MeSH term(s)	Animals ; Dogs ; Humans ; Parvovirus B19, Human ; Globosides/metabolism ; Cell Line ; Mucous Membrane/metabolism ; Madin Darby Canine Kidney Cells
Chemical Substances	Globosides
Language	English
Publishing date	2023-05-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1011402
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Globoside and the mucosal pH mediate parvovirus B19 entry through the epithelial barrier.

Corinne Suter / Minela Colakovic / Jan Bieri / Mitra Gultom / Ronald Dijkman / Carlos Ros

PLoS Pathogens, Vol 19, Iss 5, p e

2023 Volume 1011402

Abstract	Parvovirus B19 (B19V) is transmitted primarily via the respiratory route, however, the mechanism involved remains unknown. B19V targets a restricted receptor expressed in erythroid progenitor cells in the bone marrow. However, B19V shifts the receptor under acidic conditions and targets the widely expressed globoside. The pH-dependent interaction with globoside may allow virus entry through the naturally acidic nasal mucosa. To test this hypothesis, MDCK II cells and well-differentiated human airway epithelial cell (hAEC) cultures were grown on porous membranes and used as models to study the interaction of B19V with the epithelial barrier. Globoside expression was detected in polarized MDCK II cells and the ciliated cell population of well-differentiated hAEC cultures. Under the acidic conditions of the nasal mucosa, virus attachment and transcytosis occurred without productive infection. Neither virus attachment nor transcytosis was observed under neutral pH conditions or in globoside knockout cells, demonstrating the concerted role of globoside and acidic pH in the transcellular transport of B19V. Globoside-dependent virus uptake involved VP2 and occurred by a clathrin-independent pathway that is cholesterol and dynamin-dependent. This study provides mechanistic insight into the transmission of B19V through the respiratory route and reveals novel vulnerability factors of the epithelial barrier to viruses.
Keywords	Immunologic diseases. Allergy ; RC581-607 ; Biology (General) ; QH301-705.5
Subject code	616
Language	English
Publishing date	2023-05-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Well-Differentiated Primary Mammalian Airway Epithelial Cell Cultures.

Gultom, Mitra / Laloli, Laura / Dijkman, Ronald

Methods in molecular biology (Clifton, N.J.)

2020 Volume 2203, Page(s) 119–134

Abstract: Well-differentiated primary airway epithelial cell (AEC) cultures have been widely used for the characterization of several human respiratory viruses including coronaviruses. In recent years, there has been an increase in interest toward animal AEC ... ...

Abstract	Well-differentiated primary airway epithelial cell (AEC) cultures have been widely used for the characterization of several human respiratory viruses including coronaviruses. In recent years, there has been an increase in interest toward animal AEC cultures and their application to characterize veterinary viruses with zoonotic potential, as well as studying host-pathogen interactions in animal reservoir host species. In this chapter, we provide a revised and improved protocol for the isolation and establishment of well-differentiated AEC cultures from diverse mammalian species and the use of the cultures for the characterization of veterinary coronavirus. We also describe immunohistochemistry protocols with validated antibodies for the visualization and identification of viral cell tropism in well-differentiated AEC cultures from human, swine, bovine, and feline origin.
MeSH term(s)	Animals ; Bronchi/cytology ; Cats ; Cattle ; Cell Differentiation ; Coronavirus/physiology ; Epithelial Cells/cytology ; Epithelial Cells/virology ; Fluorescent Antibody Technique ; Humans ; Immunohistochemistry/methods ; Primary Cell Culture/instrumentation ; Primary Cell Culture/methods ; Swine ; Trachea/cytology ; Viral Tropism
Keywords	covid19
Language	English
Publishing date	2020-07-29
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-0900-2_10
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Generation and Characterization of an Influenza D Reporter Virus.

Probst, Lukas / Laloli, Laura / Licheri, Manon Flore / Licheri, Matthias / Gultom, Mitra / Holwerda, Melle / V'kovski, Philip / Dijkman, Ronald

Viruses

2023 Volume 15, Issue 12

Abstract: Influenza D virus (IDV) can infect various livestock animals, such as cattle, swine, and small ruminants, and was shown to have zoonotic potential. Therefore, it is important to identify viral factors involved in the broad host tropism and identify ... ...

Abstract	Influenza D virus (IDV) can infect various livestock animals, such as cattle, swine, and small ruminants, and was shown to have zoonotic potential. Therefore, it is important to identify viral factors involved in the broad host tropism and identify potential antiviral compounds that can inhibit IDV infection. Recombinant reporter viruses provide powerful tools for studying viral infections and antiviral drug discovery. Here we present the generation of a fluorescent reporter IDV using our previously established reverse genetic system for IDV. The mNeonGreen (mNG) fluorescent reporter gene was incorporated into the IDV non-structural gene segment as a fusion protein with the viral NS1 or NS2 proteins, or as a separate protein flanked by two autoproteolytic cleavage sites. We demonstrate that only recombinant reporter viruses expressing mNG as an additional separate protein or as an N-terminal fusion protein with NS1 could be rescued, albeit attenuated, compared to the parental reverse genetic clone. Serial passaging experiments demonstrated that the mNG gene is stably integrated for up to three passages, after which internal deletions accumulate. We conducted a proof-of-principle antiviral screening with the established fluorescent reporter viruses and identified two compounds influencing IDV infection. These results demonstrate that the newly established recombinant IDV reporter virus can be applied for antiviral drug discovery and monitoring viral replication, adding a new molecular tool for investigating IDV.
MeSH term(s)	Cattle ; Animals ; Swine ; Humans ; Influenza, Human/genetics ; Deltainfluenzavirus ; Thogotovirus/genetics ; Orthomyxoviridae Infections ; Orthomyxoviridae/genetics ; Viral Proteins/genetics ; Genes, Reporter ; Antiviral Agents/pharmacology
Chemical Substances	Viral Proteins ; Antiviral Agents
Language	English
Publishing date	2023-12-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v15122444
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Article ; Online: Time-resolved characterization of the innate immune response in the respiratory epithelium of human, porcine, and bovine during influenza virus infection.

Laloli, Laura / Licheri, Manon Flore / Probst, Lukas / Licheri, Matthias / Gultom, Mitra / Holwerda, Melle / V'kovski, Philip / Dijkman, Ronald

Frontiers in immunology

2022 Volume 13, Page(s) 970325

Abstract: Viral cross-species transmission is recognized to be a major threat to both human and animal health, however detailed information on determinants underlying virus host tropism and susceptibility is missing. Influenza C and D viruses (ICV, IDV) are two ... ...

Abstract	Viral cross-species transmission is recognized to be a major threat to both human and animal health, however detailed information on determinants underlying virus host tropism and susceptibility is missing. Influenza C and D viruses (ICV, IDV) are two respiratory viruses that share up to 50% genetic similarity, and both employ 9-O-acetylated sialic acids to enter a host cell. While ICV infections are mainly restricted to humans, IDV possesses a much broader host tropism and has shown to have a zoonotic potential. This suggests that additional virus-host interactions play an important role in the distinct host spectrum of ICV and IDV. In this study, we aimed to characterize the innate immune response of the respiratory epithelium of biologically relevant host species during influenza virus infection to identify possible determinants involved in viral cross-species transmission. To this end, we performed a detailed characterization of ICV and IDV infection in primary airway epithelial cell (AEC) cultures from human, porcine, and bovine origin. We monitored virus replication kinetics, cellular and host tropism, as well as the host transcriptional response over time at distinct ambient temperatures. We observed that both ICV and IDV predominantly infect ciliated cells, independently from host and temperature. Interestingly, temperature had a profound influence on ICV replication in both porcine and bovine AEC cultures, while IDV replicated efficiently irrespective of temperature and host. Detailed time-resolved transcriptome analysis revealed both species-specific and species uniform host responses and highlighted 34 innate immune-related genes with clear virus-specific and temperature-dependent profiles. These data provide the first comprehensive insights into important common and species-specific virus-host dynamics underlying the distinct host tropism of ICV and IDV, as well as possible determinants involved in viral cross-species transmission.
MeSH term(s)	Animals ; Cattle ; Communicable Diseases ; Humans ; Immunity, Innate ; Influenza, Human ; Orthomyxoviridae ; Orthomyxoviridae Infections ; Respiratory Mucosa ; Swine ; Thogotovirus/genetics
Language	English
Publishing date	2022-08-19
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.970325
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Article: Well-Differentiated Primary Mammalian Airway Epithelial Cell Cultures

Gultom, Mitra / Laloli, Laura / Dijkman, Ronald

Methods Mol Biol

Abstract	Well-differentiated primary airway epithelial cell (AEC) cultures have been widely used for the characterization of several human respiratory viruses including coronaviruses. In recent years, there has been an increase in interest toward animal AEC cultures and their application to characterize veterinary viruses with zoonotic potential, as well as studying host-pathogen interactions in animal reservoir host species. In this chapter, we provide a revised and improved protocol for the isolation and establishment of well-differentiated AEC cultures from diverse mammalian species and the use of the cultures for the characterization of veterinary coronavirus. We also describe immunohistochemistry protocols with validated antibodies for the visualization and identification of viral cell tropism in well-differentiated AEC cultures from human, swine, bovine, and feline origin.
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #729903
Database	COVID19

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Article ; Online: Establishment of well-differentiated camelid airway cultures to study Middle East respiratory syndrome coronavirus.

Gultom, Mitra / Kratzel, Annika / Portmann, Jasmine / Stalder, Hanspeter / Chanfon Bätzner, Astrid / Gantenbein, Hans / Gurtner, Corinne / Ebert, Nadine / Gad, Hans Henrik / Hartmann, Rune / Posthaus, Horst / Zanolari, Patrik / Pfaender, Stephanie / Thiel, Volker / Dijkman, Ronald

Scientific reports

2022 Volume 12, Issue 1, Page(s) 10340

Abstract: In 2012, Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in Saudi Arabia and was mostly associated with severe respiratory illness in humans. Dromedary camels are the zoonotic reservoir for MERS-CoV. To investigate the biology of MERS-CoV ...

Abstract	In 2012, Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in Saudi Arabia and was mostly associated with severe respiratory illness in humans. Dromedary camels are the zoonotic reservoir for MERS-CoV. To investigate the biology of MERS-CoV in camelids, we developed a well-differentiated airway epithelial cell (AEC) culture model for Llama glama and Camelus bactrianus. Histological characterization revealed progressive epithelial cellular differentiation with well-resemblance to autologous ex vivo tissues. We demonstrate that MERS-CoV displays a divergent cell tropism and replication kinetics profile in both AEC models. Furthermore, we observed that in the camelid AEC models MERS-CoV replication can be inhibited by both type I and III interferons (IFNs). In conclusion, we successfully established camelid AEC cultures that recapitulate the in vivo airway epithelium and reflect MERS-CoV infection in vivo. In combination with human AEC cultures, this system allows detailed characterization of the molecular basis of MERS-CoV cross-species transmission in respiratory epithelium.
MeSH term(s)	Animals ; Camelids, New World ; Camelus ; Coronavirus Infections ; Middle East Respiratory Syndrome Coronavirus ; Respiratory System
Language	English
Publishing date	2022-06-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-022-13777-y
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Article ; Online: Punctuated Loci on Chromosome IV Determine Natural Variation in Orsay Virus Susceptibility of

Sterken, Mark G / van Sluijs, Lisa / Wang, Yiru A / Ritmahan, Wannisa / Gultom, Mitra L / Riksen, Joost A G / Volkers, Rita J M / Snoek, L Basten / Pijlman, Gorben P / Kammenga, Jan E

Journal of virology

2021 Volume 95, Issue 12

Abstract: Host-pathogen interactions play a major role in evolutionary selection and shape natural genetic variation. The genetically ... ...

Abstract	Host-pathogen interactions play a major role in evolutionary selection and shape natural genetic variation. The genetically distinct
MeSH term(s)	Animals ; Caenorhabditis elegans/genetics ; Caenorhabditis elegans/virology ; Caenorhabditis elegans Proteins/genetics ; Chromosomes/genetics ; Cullin Proteins/genetics ; Genes, Helminth ; Genetic Predisposition to Disease ; Genetic Variation ; Host-Pathogen Interactions ; Multifactorial Inheritance ; Nodaviridae/pathogenicity ; Nodaviridae/physiology ; Polymorphism, Single Nucleotide ; Quantitative Trait Loci ; Viral Load
Chemical Substances	CUL-6 protein, C elegans ; Caenorhabditis elegans Proteins ; Cullin Proteins
Language	English
Publishing date	2021-05-24
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.02430-20
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Article ; Online: Establishment of well-differentiated camelid airway cultures to study Middle East respiratory syndrome coronavirus

Mitra Gultom / Annika Kratzel / Jasmine Portmann / Hanspeter Stalder / Astrid Chanfon Bätzner / Hans Gantenbein / Corinne Gurtner / Nadine Ebert / Hans Henrik Gad / Rune Hartmann / Horst Posthaus / Patrik Zanolari / Stephanie Pfaender / Volker Thiel / Ronald Dijkman

Scientific Reports, Vol 12, Iss 1, Pp 1-

2022 Volume 9

Abstract: Abstract In 2012, Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in Saudi Arabia and was mostly associated with severe respiratory illness in humans. Dromedary camels are the zoonotic reservoir for MERS-CoV. To investigate the biology of ...

Abstract	Abstract In 2012, Middle East respiratory syndrome coronavirus (MERS-CoV) emerged in Saudi Arabia and was mostly associated with severe respiratory illness in humans. Dromedary camels are the zoonotic reservoir for MERS-CoV. To investigate the biology of MERS-CoV in camelids, we developed a well-differentiated airway epithelial cell (AEC) culture model for Llama glama and Camelus bactrianus. Histological characterization revealed progressive epithelial cellular differentiation with well-resemblance to autologous ex vivo tissues. We demonstrate that MERS-CoV displays a divergent cell tropism and replication kinetics profile in both AEC models. Furthermore, we observed that in the camelid AEC models MERS-CoV replication can be inhibited by both type I and III interferons (IFNs). In conclusion, we successfully established camelid AEC cultures that recapitulate the in vivo airway epithelium and reflect MERS-CoV infection in vivo. In combination with human AEC cultures, this system allows detailed characterization of the molecular basis of MERS-CoV cross-species transmission in respiratory epithelium.
Keywords	Medicine ; R ; Science ; Q
Language	English
Publishing date	2022-06-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Establishment of caprine airway epithelial cells grown in an air-liquid interface system to study caprine respiratory viruses and bacteria.

Strässle, Marina / Laloli, Laura / Gultom, Mitra / V'kovski, Philip / Stoffel, Michael H / Crespo Pomar, Silvia / Chanfon Bätzner, Astrid / Ebert, Nadine / Labroussaa, Fabien / Dijkman, Ronald / Jores, Joerg / Thiel, Volker

Veterinary microbiology

2021 Volume 257, Page(s) 109067

Abstract: Respiratory diseases negatively impact the global goat industry, but are understudied. There is a shortage of established and biological relevant in vitro or ex vivo assays to study caprine respiratory infections. Here, we describe the establishment of ... ...

Abstract	Respiratory diseases negatively impact the global goat industry, but are understudied. There is a shortage of established and biological relevant in vitro or ex vivo assays to study caprine respiratory infections. Here, we describe the establishment of an in vitro system based on well-differentiated caprine airway epithelial cell (AEC) cultures grown under air liquid interface conditions as an experimental platform to study caprine respiratory pathogens. The functional differentiation of the AEC cultures was monitored and confirmed by light and immunofluorescence microscopy, scanning electron microscopy and examination of histological sections. We validated the functionality of the platform by studying Influenza D Virus (IDV) infection and Mycoplasma mycoides subsp. capri (Mmc) colonization over 5 days, including monitoring of infectious agents by titration and qPCR as well as colour changing units, respectively. The inoculation of caprine AEC cultures with IDV showed that efficient viral replication takes place, and revealed that IDV has a marked cell tropism for ciliated cells. Furthermore, AEC cultures were successfully infected with Mmc using a multiplicity of infection of 0.1 and colonization was monitored over several days. Altogether, these results demonstrate that our newly-established caprine AEC cultures can be used to investigate host-pathogen interactions of caprine respiratory pathogens.
MeSH term(s)	Animals ; Bronchi/cytology ; Cell Culture Techniques/methods ; Cell Culture Techniques/veterinary ; Cell Differentiation ; Cells, Cultured ; Epithelial Cells/microbiology ; Epithelial Cells/virology ; Goats ; Host-Pathogen Interactions ; Microscopy, Electron, Scanning ; Mycoplasma/physiology ; Respiratory Mucosa/microbiology ; Respiratory Mucosa/virology ; Respiratory System/cytology ; Thogotovirus/physiology ; Viral Tropism ; Virus Replication/physiology
Language	English
Publishing date	2021-04-10
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	753154-0
ISSN	1873-2542 ; 0378-1135
ISSN (online)	1873-2542
ISSN	0378-1135
DOI	10.1016/j.vetmic.2021.109067
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