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Article ; Online: JC Polyomavirus Modifies the Expression of Human microRNAs in Progressive Multifocal Leukoencephalopathy Brain.

Honkimaa, Anni / Suppula, Joni / Tynninen, Olli / Saarela, Mika / Liimatainen, Hanna / Laine, Pia / Auvinen, Petri / Auvinen, Eeva

The Journal of infectious diseases

2023 Volume 228, Issue 7, Page(s) 829–833

Abstract: Progressive multifocal leukoencephalopathy (PML) is a severe neurological condition caused by reactivation of JC polyomavirus (JCPyV) in immunosuppression. Asymptomatic JCPyV persists in peripheral tissues. Upon reactivation, neurotropic rearrangements ... ...

Abstract	Progressive multifocal leukoencephalopathy (PML) is a severe neurological condition caused by reactivation of JC polyomavirus (JCPyV) in immunosuppression. Asymptomatic JCPyV persists in peripheral tissues. Upon reactivation, neurotropic rearrangements may emerge, and the virus gains access to the brain. To assess the mechanisms of PML pathogenesis, brain tissue material from PML patients was collected for small RNA sequencing. Upregulation of 8 microRNAs (miRNAs) in PML brain was validated using quantitative microRNA polymerase chain reaction (PCR). Bioinformatics tools were utilized to identify major associations of the upregulated miRNAs: neuroinflammation and blood-brain barrier disruption. The results indicate involvement of human miRNA regulation in PML pathogenesis.
MeSH term(s)	Humans ; Leukoencephalopathy, Progressive Multifocal/genetics ; Leukoencephalopathy, Progressive Multifocal/pathology ; JC Virus/genetics ; MicroRNAs/genetics ; Brain/pathology ; Base Sequence
Chemical Substances	MicroRNAs
Language	English
Publishing date	2023-03-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3019-3
ISSN	1537-6613 ; 0022-1899
ISSN (online)	1537-6613
ISSN	0022-1899
DOI	10.1093/infdis/jiad083
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Article ; Online: Differentiation of highly pathogenic strains of human JC polyomavirus in neurological patients by next generation sequencing.

Auvinen, Eeva / Honkimaa, Anni / Laine, Pia / Passerini, Sara / Moens, Ugo / Pietropaolo, Valeria / Saarela, Mika / Maunula, Leena / Mannonen, Laura / Tynninen, Olli / Haapasalo, Hannu / Rauramaa, Tuomas / Auvinen, Petri / Liimatainen, Hanna

Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology

2024 Volume 171, Page(s) 105652

Abstract: Background: JC polyomavirus (JCPyV) persists asymptomatic in more than half of the human population. Immunocompromising conditions may cause reactivation and acquisition of neurotropic rearrangements in the viral genome, especially in the non-coding ... ...

Abstract	Background: JC polyomavirus (JCPyV) persists asymptomatic in more than half of the human population. Immunocompromising conditions may cause reactivation and acquisition of neurotropic rearrangements in the viral genome, especially in the non-coding control region (NCCR). Such rearranged JCPyV strains are strongly associated with the development of progressive multifocal leukoencephalopathy (PML). Methods: Using next-generation sequencing (NGS) and bioinformatics tools, the NCCR was characterized in cerebrospinal fluid (CSF; N = 21) and brain tissue (N = 16) samples from PML patients (N = 25), urine specimens from systemic lupus erythematosus patients (N = 2), brain tissue samples from control individuals (N = 2) and waste-water samples (N = 5). Quantitative PCR was run in parallel for diagnostic PML samples. Results: Archetype NCCR (i.e. ABCDEF block structure) and archetype-like NCCR harboring minor mutations were detected in two CSF samples and in one CSF sample and in one tissue sample, respectively. Among samples from PML patients, rearranged NCCRs were found in 8 out of 21 CSF samples and in 14 out of 16 brain tissue samples. Complete or partial deletion of the C and D blocks was characteristic of most rearranged JCPyV strains. From ten CSF samples and one tissue sample NCCR could not be amplified. Conclusions: Rearranged NCCRs are predominant in brain tissue and common in CSF from PML patients. Extremely sensitive detection and identification of neurotropic viral populations in CSF or brain tissue by NGS may contribute to early and accurate diagnosis, timely intervention and improved patient care.
MeSH term(s)	Humans ; JC Virus/genetics ; High-Throughput Nucleotide Sequencing ; DNA, Viral/genetics ; DNA, Viral/cerebrospinal fluid ; Leukoencephalopathy, Progressive Multifocal/diagnosis ; Mutation
Chemical Substances	DNA, Viral
Language	English
Publishing date	2024-02-12
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1446080-4
ISSN	1873-5967 ; 1386-6532
ISSN (online)	1873-5967
ISSN	1386-6532
DOI	10.1016/j.jcv.2024.105652
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Article ; Online: Exploring JC polyomavirus sequences and human gene expression in brain tissue of patients with progressive multifocal leukoencephalopathy.

Honkimaa, Anni / Laine, Pia / Suppula, Joni / Tynninen, Olli / Saarela, Mika / Laakso, Sini M / Hetemäki, Iivo / Liimatainen, Hanna / Auvinen, Petri / Auvinen, Eeva

The Journal of infectious diseases

2024

Abstract: Progressive multifocal leukoencephalopathy (PML) is a rare neurological condition associated with reactivation of dormant JC polyomavirus (JCPyV). In this study, we characterized gene expression and JCPyV rearrangements in PML brain tissue. Infection of ... ...

Abstract	Progressive multifocal leukoencephalopathy (PML) is a rare neurological condition associated with reactivation of dormant JC polyomavirus (JCPyV). In this study, we characterized gene expression and JCPyV rearrangements in PML brain tissue. Infection of white matter astrocytes and oligodendrocytes as well as occasional brain cortex neurons was shown. PML brain harbored exclusively rearranged JCPyV variants. Viral transcripts covered the whole genome on both strands. Strong differential expression of human genes associated with neuroinflammation, blood-brain-barrier permeability and neurodegenerative diseases was shown. Pathway analysis revealed wide immune activation in PML brain. The study provides novel insights into the pathogenesis of PML.
Language	English
Publishing date	2024-02-14
Publishing country	United States
Document type	Journal Article
ZDB-ID	3019-3
ISSN	1537-6613 ; 0022-1899
ISSN (online)	1537-6613
ISSN	0022-1899
DOI	10.1093/infdis/jiae066
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Article ; Online: Eradication of persistent coxsackievirus B infection from a pancreatic cell line with clinically used antiviral drugs.

Honkimaa, Anni / Sioofy-Khojine, Amir-Babak / Oikarinen, Sami / Bertin, Antoine / Hober, Didier / Hyöty, Heikki

Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology

2020 Volume 128, Page(s) 104334

Abstract: Background: Persistent enterovirus infections create a difficult therapeutic challenge in immunocompromised patients and may also contribute to the development of chronic diseases including type 1 diabetes, cardiomyopathies, post-polio syndrome and ... ...

Abstract	Background: Persistent enterovirus infections create a difficult therapeutic challenge in immunocompromised patients and may also contribute to the development of chronic diseases including type 1 diabetes, cardiomyopathies, post-polio syndrome and chronic fatigue syndrome. Objectives: To study the ability of antiviral drugs to eradicate such infection in vitro to evalaute their potential in the treatments of these patients. Study design: We set out to evaluate several licensed or clinically tested drugs which have shown some anti-enterovirus activity in previous studies for their ability to cure persistent infection established by two different coxsackievirus B1 strains in a pancreatic cell line (PANC-1 cells). Results: Among all tested drugs Enviroxime, Fluoxetine, concentrated human IgG product (Hizentra) and Pleconaril were able to eradicate persistent Coxsackievirus B1 infection. The effect Enviroxime, Hizentra and Pleconaril varied between the two virus strains. Conclusions: The identified drugs are feasible candidates for clinical trials among patients with persistent coxsackievirus B infections or chronic enterovirus-associated diseases.
MeSH term(s)	A549 Cells ; Antiviral Agents/pharmacology ; Cell Line, Tumor ; Cytopathogenic Effect, Viral/drug effects ; Drug Discovery ; Enterovirus B, Human/drug effects ; Enterovirus B, Human/physiology ; Humans ; Microbial Viability/drug effects ; Models, Biological ; Pancreatic Neoplasms ; Phenotype ; Virus Replication/drug effects
Chemical Substances	Antiviral Agents
Language	English
Publishing date	2020-04-26
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1446080-4
ISSN	1873-5967 ; 1386-6532
ISSN (online)	1873-5967
ISSN	1386-6532
DOI	10.1016/j.jcv.2020.104334
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Genetic Adaptation of Coxsackievirus B1 during Persistent Infection in Pancreatic Cells

Honkimaa, Anni / Kimura, Bryn / Sioofy-Khojine, Amir-Babak / Lin, Jake / Laiho, Jutta / Oikarinen, Sami / Hyöty, Heikki

Microorganisms. 2020 Nov. 15, v. 8, no. 11

2020

Abstract: Coxsackie B (CVB) viruses have been associated with type 1 diabetes. We have recently observed that CVB1 was linked to the initiation of the autoimmune process leading to type 1 diabetes in Finnish children. Viral persistency in the pancreas is currently ...

Abstract	Coxsackie B (CVB) viruses have been associated with type 1 diabetes. We have recently observed that CVB1 was linked to the initiation of the autoimmune process leading to type 1 diabetes in Finnish children. Viral persistency in the pancreas is currently considered as one possible mechanism. In the current study persistent infection was established in pancreatic ductal and beta cell lines (PANC-1 and 1.1B4) using four different CVB1 strains, including the prototype strain and three clinical isolates. We sequenced 5′ untranslated region (UTR) and regions coding for structural and non-structural proteins and the second single open reading frame (ORF) protein of all persisting CVB1 strains using next generation sequencing to identify mutations that are common for all of these strains. One mutation, K257R in VP1, was found from all persisting CVB1 strains. The mutations were mainly accumulated in viral structural proteins, especially at BC, DE, EF loops and C-terminus of viral capsid protein 1 (VP1), the puff region of VP2, the knob region of VP3 and infection-enhancing epitope of VP4. This showed that the capsid region of the viruses sustains various changes during persistency some of which could be hallmark(s) of persistency.
Keywords	capsid ; cell lines ; children ; chronic diseases ; coat proteins ; epitopes ; high-throughput nucleotide sequencing ; insulin-dependent diabetes mellitus ; mutation ; open reading frames ; pancreas ; prototypes ; strains ; structural proteins ; viral nonstructural proteins ; viruses
Language	English
Dates of publication	2020-1115
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
Note	NAL-light
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms8111790
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Vemurafenib Inhibits Acute and Chronic Enterovirus Infection by Affecting Cellular Kinase Phosphatidylinositol 4-Kinase Type IIIβ.

Laajala, Mira / Zwaagstra, Marleen / Martikainen, Mari / Nekoua, Magloire Pandoua / Benkahla, Mehdi / Sane, Famara / Gervais, Emily / Campagnola, Grace / Honkimaa, Anni / Sioofy-Khojine, Amir-Babak / Hyöty, Heikki / Ojha, Ravi / Bailliot, Marie / Balistreri, Giuseppe / Peersen, Olve / Hober, Didier / Van Kuppeveld, Frank / Marjomäki, Varpu

Microbiology spectrum

2023 Volume 11, Issue 4, Page(s) e0055223

Abstract: Enteroviruses are one of the most abundant viruses causing mild to serious acute infections in humans and also contributing to chronic diseases like type 1 diabetes. Presently, there are no approved antiviral drugs against enteroviruses. Here, we studied ...

Abstract	Enteroviruses are one of the most abundant viruses causing mild to serious acute infections in humans and also contributing to chronic diseases like type 1 diabetes. Presently, there are no approved antiviral drugs against enteroviruses. Here, we studied the potency of vemurafenib, an FDA-approved RAF kinase inhibitor for treating BRAF
MeSH term(s)	Animals ; Mice ; Humans ; Vemurafenib/pharmacology ; Vemurafenib/therapeutic use ; Enterovirus ; 1-Phosphatidylinositol 4-Kinase ; Proto-Oncogene Proteins B-raf/genetics ; Proto-Oncogene Proteins B-raf/metabolism ; Melanoma/drug therapy ; Protein Kinase Inhibitors/pharmacology ; Enterovirus Infections/drug therapy ; Mitogen-Activated Protein Kinase Kinases ; Mutation
Chemical Substances	Vemurafenib (207SMY3FQT) ; 1-Phosphatidylinositol 4-Kinase (EC 2.7.1.67) ; Proto-Oncogene Proteins B-raf (EC 2.7.11.1) ; Protein Kinase Inhibitors ; Mitogen-Activated Protein Kinase Kinases (EC 2.7.12.2)
Language	English
Publishing date	2023-07-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2807133-5
ISSN	2165-0497 ; 2165-0497
ISSN (online)	2165-0497
ISSN	2165-0497
DOI	10.1128/spectrum.00552-23
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Article: Genetic Adaptation of Coxsackievirus B1 during Persistent Infection in Pancreatic Cells.

Honkimaa, Anni / Kimura, Bryn / Sioofy-Khojine, Amir-Babak / Lin, Jake / Laiho, Jutta / Oikarinen, Sami / Hyöty, Heikki

Microorganisms

2020 Volume 8, Issue 11

Abstract	Coxsackie B (CVB) viruses have been associated with type 1 diabetes. We have recently observed that CVB1 was linked to the initiation of the autoimmune process leading to type 1 diabetes in Finnish children. Viral persistency in the pancreas is currently considered as one possible mechanism. In the current study persistent infection was established in pancreatic ductal and beta cell lines (PANC-1 and 1.1B4) using four different CVB1 strains, including the prototype strain and three clinical isolates. We sequenced 5' untranslated region (UTR) and regions coding for structural and non-structural proteins and the second single open reading frame (ORF) protein of all persisting CVB1 strains using next generation sequencing to identify mutations that are common for all of these strains. One mutation, K257R in VP1, was found from all persisting CVB1 strains. The mutations were mainly accumulated in viral structural proteins, especially at BC, DE, EF loops and C-terminus of viral capsid protein 1 (VP1), the puff region of VP2, the knob region of VP3 and infection-enhancing epitope of VP4. This showed that the capsid region of the viruses sustains various changes during persistency some of which could be hallmark(s) of persistency.
Language	English
Publishing date	2020-11-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms8111790
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Article: Detection of Viral −RNA and +RNA Strands in Enterovirus-Infected Cells and Tissues

Salmikangas, Sami / Laiho, Jutta E / Kalander, Kerttu / Laajala, Mira / Honkimaa, Anni / Shanina, Iryna / Oikarinen, Sami / Horwitz, Marc S / Hyöty, Heikki / Marjomäki, Varpu

Microorganisms. 2020 Dec. 04, v. 8, no. 12

2020

Abstract: The current methods to study the distribution and dynamics of viral RNA molecules inside infected cells are not ideal, as electron microscopy and immunohistochemistry can only detect mature virions, and quantitative real-time PCR does not reveal ... ...

Abstract	The current methods to study the distribution and dynamics of viral RNA molecules inside infected cells are not ideal, as electron microscopy and immunohistochemistry can only detect mature virions, and quantitative real-time PCR does not reveal localized distribution of RNAs. We demonstrated here the branched DNA in situ hybridization (bDNA ISH) technology to study both the amount and location of the emerging -RNA and +RNA during acute and persistent enterovirus infections. According to our results, the replication of the viral RNA started 2–3 h after infection and the translation shortly after at 3–4 h post-infection. The replication hotspots with newly emerging -RNA were located quite centrally in the cell, while the +RNA production and most likely virion assembly took place in the periphery of the cell. We also discovered that the pace of replication of -RNA and +RNA strands was almost identical, and -RNA was absent during antiviral treatments. ViewRNA ISH with our custom probes also showed a good signal during acute and persistent enterovirus infections in cell and mouse models. Considering these results, along with the established bDNA FISH protocol modified by us, the effects of antiviral drugs and the emergence of enterovirus RNAs in general can be studied more effectively.
Keywords	DNA ; Enterovirus ; RNA ; antiviral agents ; cells ; detection ; dynamics ; electron microscopy ; enterovirus Infections ; fish ; immunohistochemistry ; in situ hybridization ; infection ; microorganisms ; protocols ; quantitative polymerase chain reaction ; technology ; tissues ; virion
Language	English
Dates of publication	2020-1204
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
Note	NAL-light
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms8121928
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Persistent coxsackievirus B1 infection triggers extensive changes in the transcriptome of human pancreatic ductal cells.

Buchacher, Tanja / Honkimaa, Anni / Välikangas, Tommi / Lietzén, Niina / Hirvonen, M Karoliina / Laiho, Jutta E / Sioofy-Khojine, Amir-Babak / Eskelinen, Eeva-Liisa / Hyöty, Heikki / Elo, Laura L / Lahesmaa, Riitta

iScience

2021 Volume 25, Issue 1, Page(s) 103653

Abstract: Enteroviruses, particularly the group B coxsackieviruses (CVBs), have been associated with the development of type 1 diabetes. Several CVB serotypes establish chronic infections in human ... ...

Abstract	Enteroviruses, particularly the group B coxsackieviruses (CVBs), have been associated with the development of type 1 diabetes. Several CVB serotypes establish chronic infections in human cells
Language	English
Publishing date	2021-12-18
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2021.103653
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Article: Detection of Viral -RNA and +RNA Strands in Enterovirus-Infected Cells and Tissues.

Salmikangas, Sami / Laiho, Jutta E / Kalander, Kerttu / Laajala, Mira / Honkimaa, Anni / Shanina, Iryna / Oikarinen, Sami / Horwitz, Marc S / Hyöty, Heikki / Marjomäki, Varpu

Microorganisms

2020 Volume 8, Issue 12

Abstract	The current methods to study the distribution and dynamics of viral RNA molecules inside infected cells are not ideal, as electron microscopy and immunohistochemistry can only detect mature virions, and quantitative real-time PCR does not reveal localized distribution of RNAs. We demonstrated here the branched DNA in situ hybridization (bDNA ISH) technology to study both the amount and location of the emerging -RNA and +RNA during acute and persistent enterovirus infections. According to our results, the replication of the viral RNA started 2-3 h after infection and the translation shortly after at 3-4 h post-infection. The replication hotspots with newly emerging -RNA were located quite centrally in the cell, while the +RNA production and most likely virion assembly took place in the periphery of the cell. We also discovered that the pace of replication of -RNA and +RNA strands was almost identical, and -RNA was absent during antiviral treatments. ViewRNA ISH with our custom probes also showed a good signal during acute and persistent enterovirus infections in cell and mouse models. Considering these results, along with the established bDNA FISH protocol modified by us, the effects of antiviral drugs and the emergence of enterovirus RNAs in general can be studied more effectively.
Language	English
Publishing date	2020-12-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms8121928
Database	MEDical Literature Analysis and Retrieval System OnLINE

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