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Article: Innate lymphoid cells in neuroinflammation.

Kveštak, Daria / Mihalić, Andrea / Jonjić, Stipan / Brizić, Ilija

2024 Volume 18, Page(s) 1364485

Abstract: Innate lymphoid cells (ILCs) are largely tissue-resident cells that participate in the maintenance of tissue homeostasis and react early to inflammatory events. Mature ILCs are divided into three major groups based on the transcription factors required ... ...

Abstract	Innate lymphoid cells (ILCs) are largely tissue-resident cells that participate in the maintenance of tissue homeostasis and react early to inflammatory events. Mature ILCs are divided into three major groups based on the transcription factors required for their development and function. Under physiological conditions, ILCs are present within the choroid plexus and meninges while the CNS parenchyma is almost devoid of these cells. However, pathological conditions such as autoimmune neuroinflammation and viral infections of the CNS result in the infiltration of ILCs into parenchyma. In this article, we provide an overview of the involvement and function of the ILCs within the CNS during physiological conditions and in infections, autoimmune diseases, neurodegeneration, and injury.
Language	English
Publishing date	2024-02-21
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2452963-1
ISSN	1662-5102
ISSN	1662-5102
DOI	10.3389/fncel.2024.1364485
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Article ; Online: Comprehensive Analysis of Soluble Mediator Profiles in Congenital CMV Infection Using an MCMV Model.

Karner, Dubravka / Kvestak, Daria / Lisnic, Berislav / Cokaric Brdovcak, Maja / Juranic Lisnic, Vanda / Kucan Brlic, Paola / Hasan, Milena / Lenac Rovis, Tihana

Viruses

2024 Volume 16, Issue 2

Abstract: Congenital human cytomegalovirus (HCMV) infection may cause life-threatening disease and permanent damage to the central nervous system. The mouse model of CMV infection is most commonly used to study mechanisms of infection and pathogenesis. While ... ...

Abstract	Congenital human cytomegalovirus (HCMV) infection may cause life-threatening disease and permanent damage to the central nervous system. The mouse model of CMV infection is most commonly used to study mechanisms of infection and pathogenesis. While essential to limit mouse CMV (MCMV) replication, the inflammatory responses, particularly IFNγ and TNFα, cause neurodevelopmental abnormalities. Other soluble mediators of the immune response in most tissues remain largely unexplored. To address this gap, we quantified 48 soluble mediators of the immune response, including 32 cytokines, 10 chemokines, 3 growth factors/regulators, and 3 soluble receptors in the spleen, liver, lungs, and brain at 9 and 14 days postinfection (dpi). Our analysis found 25 induced molecules in the brain at 9 dpi, with an additional 8 showing statistically elevated responses at 14 dpi. Specifically, all analyzed CCL group cytokines (CCL2, CCL3, CCL4, CCL5, CCL7, and CCL11) were upregulated at 14 dpi in the brain. Furthermore, data revealed differentially regulated analytes across tissues, such as CCL11, CXCL5, and IL-10 in the brain, IL-33/IL-33R in the liver, and VEGF-a and IL-5 in the lungs. Overall, this study provides an overview of the immune dynamics of soluble mediators in congenital CMV.
MeSH term(s)	Animals ; Humans ; Mice ; Cytomegalovirus Infections ; Cytokines ; Brain ; Tumor Necrosis Factor-alpha ; Muromegalovirus
Chemical Substances	Cytokines ; Tumor Necrosis Factor-alpha
Language	English
Publishing date	2024-01-30
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/v16020208
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Article ; Online: Viral infection of the ovaries compromises pregnancy and reveals innate immune mechanisms protecting fertility.

Tomac, Jelena / Mazor, Marija / Lisnić, Berislav / Golemac, Mijo / Kveštak, Daria / Bralić, Marina / Bilić Zulle, Lidija / Brinkmann, Melanie M / Dölken, Lars / Reinert, Line S / Paludan, Soren R / Krmpotić, Astrid / Jonjić, Stipan / Juranić Lisnić, Vanda

Immunity

2021 Volume 54, Issue 7, Page(s) 1478–1493.e6

Abstract: Viral infections during pregnancy are a considerable cause of adverse outcomes and birth defects, and the underlying mechanisms are poorly understood. Among those, cytomegalovirus (CMV) infection stands out as the most common intrauterine infection in ... ...

Abstract	Viral infections during pregnancy are a considerable cause of adverse outcomes and birth defects, and the underlying mechanisms are poorly understood. Among those, cytomegalovirus (CMV) infection stands out as the most common intrauterine infection in humans, putatively causing early pregnancy loss. We employed murine CMV as a model to study the consequences of viral infection on pregnancy outcome and fertility maintenance. Even though pregnant mice successfully controlled CMV infection, we observed highly selective, strong infection of corpus luteum (CL) cells in their ovaries. High infection densities indicated complete failure of immune control in CL cells, resulting in progesterone insufficiency and pregnancy loss. An abundance of gap junctions, absence of vasculature, strong type I interferon (IFN) responses, and interaction of innate immune cells fully protected the ovarian follicles from viral infection. Our work provides fundamental insights into the effect of CMV infection on pregnancy loss and mechanisms protecting fertility.
MeSH term(s)	Animals ; Corpus Luteum/immunology ; Corpus Luteum/virology ; Cytomegalovirus/immunology ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/virology ; Female ; Fertility/immunology ; Gap Junctions/immunology ; Immunity, Innate/immunology ; Interferon Type I/immunology ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Inbred NOD ; Pregnancy ; Progesterone/immunology
Chemical Substances	Interferon Type I ; Progesterone (4G7DS2Q64Y)
Language	English
Publishing date	2021-05-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1217235-2
ISSN	1097-4180 ; 1074-7613
ISSN (online)	1097-4180
ISSN	1074-7613
DOI	10.1016/j.immuni.2021.04.020
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Zs.A 4227: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Characterization of M116.1p, a Murine Cytomegalovirus Protein Required for Efficient Infection of Mononuclear Phagocytes.

Ružić, Tina / Juranić Lisnić, Vanda / Mahmutefendić Lučin, Hana / Lenac Roviš, Tihana / Železnjak, Jelena / Cokarić Brdovčak, Maja / Vrbanović, Ana / Oreb, Deni / Kveštak, Daria / Gotovac Jerčić, Kristina / Borovečki, Fran / Lučin, Pero / Adler, Barbara / Jonjić, Stipan / Lisnić, Berislav

Journal of virology

2021 Volume 96, Issue 2, Page(s) e0087621

Abstract: Broad tissue tropism of cytomegaloviruses (CMVs) is facilitated by different glycoprotein entry complexes, which are conserved between human CMV (HCMV) and murine CMV (MCMV). Among the wide array of cell types susceptible to the infection, mononuclear ... ...

Abstract	Broad tissue tropism of cytomegaloviruses (CMVs) is facilitated by different glycoprotein entry complexes, which are conserved between human CMV (HCMV) and murine CMV (MCMV). Among the wide array of cell types susceptible to the infection, mononuclear phagocytes (MNPs) play a unique role in the pathogenesis of the infection as they contribute both to the virus spread and immune control. CMVs have dedicated numerous genes for the efficient infection and evasion of macrophages and dendritic cells. In this study, we have characterized the properties and function of
MeSH term(s)	Animals ; Fibroblasts/metabolism ; Fibroblasts/virology ; Glycosylation ; Herpesviridae Infections/virology ; Membrane Glycoproteins/metabolism ; Mice ; Mononuclear Phagocyte System/metabolism ; Mononuclear Phagocyte System/virology ; Muromegalovirus/physiology ; Transcription, Genetic ; Viral Envelope Proteins/genetics ; Viral Envelope Proteins/metabolism ; Virion/metabolism ; Virus Assembly ; Virus Internalization ; Virus Replication
Chemical Substances	Membrane Glycoproteins ; Viral Envelope Proteins
Language	English
Publishing date	2021-10-27
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.00876-21
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Article ; Online: NK/ILC1 cells mediate neuroinflammation and brain pathology following congenital CMV infection.

Kveštak, Daria / Juranić Lisnić, Vanda / Lisnić, Berislav / Tomac, Jelena / Golemac, Mijo / Brizić, Ilija / Indenbirken, Daniela / Cokarić Brdovčak, Maja / Bernardini, Giovanni / Krstanović, Fran / Rožmanić, Carmen / Grundhoff, Adam / Krmpotić, Astrid / Britt, William J / Jonjić, Stipan

The Journal of experimental medicine

2021 Volume 218, Issue 5

Abstract: Congenital human cytomegalovirus (cHCMV) infection of the brain is associated with a wide range of neurocognitive sequelae. Using infection of newborn mice with mouse cytomegalovirus (MCMV) as a reliable model that recapitulates many aspects of cHCMV ... ...

Abstract	Congenital human cytomegalovirus (cHCMV) infection of the brain is associated with a wide range of neurocognitive sequelae. Using infection of newborn mice with mouse cytomegalovirus (MCMV) as a reliable model that recapitulates many aspects of cHCMV infection, including disseminated infection, CNS infection, altered neurodevelopment, and sensorineural hearing loss, we have previously shown that mitigation of inflammation prevented alterations in cerebellar development, suggesting that host inflammatory factors are key drivers of neurodevelopmental defects. Here, we show that MCMV infection causes a dramatic increase in the expression of the microglia-derived chemokines CXCL9/CXCL10, which recruit NK and ILC1 cells into the brain in a CXCR3-dependent manner. Surprisingly, brain-infiltrating innate immune cells not only were unable to control virus infection in the brain but also orchestrated pathological inflammatory responses, which lead to delays in cerebellar morphogenesis. Our results identify NK and ILC1 cells as the major mediators of immunopathology in response to virus infection in the developing CNS, which can be prevented by anti-IFN-γ antibodies.
MeSH term(s)	Animals ; Animals, Newborn ; Brain/immunology ; Brain/pathology ; Brain/virology ; Chemokine CXCL10/genetics ; Chemokine CXCL10/immunology ; Chemokine CXCL10/metabolism ; Chemokine CXCL9/genetics ; Chemokine CXCL9/immunology ; Chemokine CXCL9/metabolism ; Cytomegalovirus/immunology ; Cytomegalovirus/physiology ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/virology ; Gene Expression Regulation/immunology ; Humans ; Immunity, Innate/immunology ; Inflammation/genetics ; Inflammation/immunology ; Inflammation/virology ; Killer Cells, Natural/immunology ; Killer Cells, Natural/metabolism ; Lymphocytes/immunology ; Lymphocytes/metabolism ; Mice, 129 Strain ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Microglia/immunology ; Microglia/metabolism ; Microglia/virology ; Receptors, CXCR3/genetics ; Receptors, CXCR3/immunology ; Receptors, CXCR3/metabolism ; Mice
Chemical Substances	Chemokine CXCL10 ; Chemokine CXCL9 ; Cxcr3 protein, mouse ; Receptors, CXCR3
Language	English
Publishing date	2021-02-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20201503
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Article ; Online: Immunobiology of congenital cytomegalovirus infection of the central nervous system—the murine cytomegalovirus model.

Slavuljica, Irena / Kveštak, Daria / Huszthy, Peter Csaba / Kosmac, Kate / Britt, William J / Jonjić, Stipan

Cellular & molecular immunology

2014 Volume 12, Issue 2, Page(s) 180–191

Abstract: Congenital human cytomegalovirus infection is a leading infectious cause of long-term neurodevelopmental sequelae, including mental retardation and hearing defects. Strict species specificity of cytomegaloviruses has restricted the scope of studies of ... ...

Abstract	Congenital human cytomegalovirus infection is a leading infectious cause of long-term neurodevelopmental sequelae, including mental retardation and hearing defects. Strict species specificity of cytomegaloviruses has restricted the scope of studies of cytomegalovirus infection in animal models. To investigate the pathogenesis of congenital human cytomegalovirus infection, we developed a mouse cytomegalovirus model that recapitulates the major characteristics of central nervous system infection in human infants, including the route of neuroinvasion and neuropathological findings. Following intraperitoneal inoculation of newborn animals with mouse cytomegalovirus, the virus disseminates to the central nervous system during high-level viremia and replicates in the brain parenchyma, resulting in a focal but widespread, non-necrotizing encephalitis. Central nervous system infection is coupled with the recruitment of resident and peripheral immune cells as well as the expression of a large number of pro-inflammatory cytokines. Although infiltration of cellular constituents of the innate immune response characterizes the early immune response in the central nervous system, resolution of productive infection requires virus-specific CD8(+) T cells. Perinatal mouse cytomegalovirus infection results in profoundly altered postnatal development of the mouse central nervous system and long-term motor and sensory disabilities. Based on an enhanced understanding of the pathogenesis of this infection, prospects for novel intervention strategies aimed to improve the outcome of congenital human cytomegalovirus infection are proposed.
MeSH term(s)	Animals ; Animals, Newborn/virology ; Central Nervous System Diseases/congenital ; Central Nervous System Diseases/immunology ; Central Nervous System Diseases/virology ; Cytomegalovirus/immunology ; Cytomegalovirus Infections/congenital ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/virology ; Disease Models, Animal ; Humans ; Mice
Language	English
Publishing date	2014-07-21
Publishing country	China
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2435097-7
ISSN	2042-0226 ; 1672-7681
ISSN (online)	2042-0226
ISSN	1672-7681
DOI	10.1038/cmi.2014.51
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Article: Murine Cytomegalovirus Infection Induces Susceptibility to EAE in Resistant BALB/c Mice.

Milovanovic, Jelena / Popovic, Branka / Milovanovic, Marija / Kvestak, Daria / Arsenijevic, Aleksandar / Stojanovic, Bojana / Tanaskovic, Irena / Krmpotic, Astrid / Arsenijevic, Nebojsa / Jonjic, Stipan / Lukic, Miodrag L

Frontiers in immunology

2017 Volume 8, Page(s) 192

Abstract: In contrast to C57BL/6 mice, BALB/c mice are relatively resistant to the induction of experimental autoimmune encephalomyelitis (EAE) after challenge with ... ...

Abstract	In contrast to C57BL/6 mice, BALB/c mice are relatively resistant to the induction of experimental autoimmune encephalomyelitis (EAE) after challenge with MOG
Language	English
Publishing date	2017
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606827-8
ISSN	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2017.00192
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Article ; Online: Brain-resident memory CD8

Brizić, Ilija / Šušak, Božo / Arapović, Maja / Huszthy, Peter C / Hiršl, Lea / Kveštak, Daria / Juranić Lisnić, Vanda / Golemac, Mijo / Pernjak Pugel, Ester / Tomac, Jelena / Oxenius, Annette / Britt, William J / Arapović, Jurica / Krmpotić, Astrid / Jonjić, Stipan

European journal of immunology

2018 Volume 48, Issue 6, Page(s) 950–964

Abstract: Congenital HCMV infection is a leading infectious cause of long-term neurodevelopmental sequelae. Infection of newborn mice with mouse cytomegalovirus (MCMV) intraperitoneally is a well-established model of congenital human cytomegalovirus infection, ... ...

Abstract	Congenital HCMV infection is a leading infectious cause of long-term neurodevelopmental sequelae. Infection of newborn mice with mouse cytomegalovirus (MCMV) intraperitoneally is a well-established model of congenital human cytomegalovirus infection, which best recapitulates the hematogenous route of virus spread to brain and subsequent pathology. Here, we used this model to investigate the role, dynamics, and phenotype of CD8
MeSH term(s)	Adoptive Transfer ; Animals ; Animals, Newborn ; Brain/immunology ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/transplantation ; Cells, Cultured ; Congenital Abnormalities ; Cytomegalovirus/physiology ; Cytomegalovirus Infections/immunology ; Disease Models, Animal ; Humans ; Immunologic Memory ; Mice ; Mice, Inbred C57BL ; Muromegalovirus/physiology ; T-Lymphocytes, Cytotoxic/immunology ; T-Lymphocytes, Cytotoxic/transplantation ; Virus Activation/immunology
Language	English
Publishing date	2018-03-23
Publishing country	Germany
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	120108-6
ISSN	1521-4141 ; 0014-2980
ISSN (online)	1521-4141
ISSN	0014-2980
DOI	10.1002/eji.201847526
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Zs.A 489: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Inflammatory monocytes and NK cells play a crucial role in DNAM-1-dependent control of cytomegalovirus infection.

Lenac Rovis, Tihana / Kucan Brlic, Paola / Kaynan, Noa / Juranic Lisnic, Vanda / Brizic, Ilija / Jordan, Stefan / Tomic, Adriana / Kvestak, Daria / Babic, Marina / Tsukerman, Pinchas / Colonna, Marco / Koszinowski, Ulrich / Messerle, Martin / Mandelboim, Ofer / Krmpotic, Astrid / Jonjic, Stipan

The Journal of experimental medicine

2016 Volume 213, Issue 9, Page(s) 1835–1850

Abstract: The poliovirus receptor (PVR) is a ubiquitously expressed glycoprotein involved in cellular adhesion and immune response. It engages the activating receptor DNAX accessory molecule (DNAM)-1, the inhibitory receptor TIGIT, and the CD96 receptor with both ... ...

Abstract	The poliovirus receptor (PVR) is a ubiquitously expressed glycoprotein involved in cellular adhesion and immune response. It engages the activating receptor DNAX accessory molecule (DNAM)-1, the inhibitory receptor TIGIT, and the CD96 receptor with both activating and inhibitory functions. Human cytomegalovirus (HCMV) down-regulates PVR expression, but the significance of this viral function in vivo remains unknown. Here, we demonstrate that mouse CMV (MCMV) also down-regulates the surface PVR. The m20.1 protein of MCMV retains PVR in the endoplasmic reticulum and promotes its degradation. A MCMV mutant lacking the PVR inhibitor was attenuated in normal mice but not in mice lacking DNAM-1. This attenuation was partially reversed by NK cell depletion, whereas the simultaneous depletion of mononuclear phagocytes abolished the virus control. This effect was associated with the increased expression of DNAM-1, whereas TIGIT and CD96 were absent on these cells. An increased level of proinflammatory cytokines in sera of mice infected with the virus lacking the m20.1 and an increased production of iNOS by inflammatory monocytes was observed. Blocking of CCL2 or the inhibition of iNOS significantly increased titer of the virus lacking m20.1. In this study, we have demonstrated that inflammatory monocytes, together with NK cells, are essential in the early control of CMV through the DNAM-1-PVR pathway.
MeSH term(s)	Animals ; Antigens, Differentiation, T-Lymphocyte/physiology ; Cytomegalovirus Infections/etiology ; Cytomegalovirus Infections/immunology ; Interleukin-12/biosynthesis ; Killer Cells, Natural/physiology ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Monocytes/physiology ; Nitric Oxide Synthase Type II/physiology ; Receptors, Virus/antagonists & inhibitors ; Receptors, Virus/physiology
Chemical Substances	Antigens, Differentiation, T-Lymphocyte ; CD226 antigen ; Receptors, Virus ; poliovirus receptor ; Interleukin-12 (187348-17-0) ; Nitric Oxide Synthase Type II (EC 1.14.13.39) ; Nos2 protein, mouse (EC 1.14.13.39)
Language	English
Publishing date	2016-08-08
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20151899
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