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Article ; Online: Methotrexate and its mechanisms of action in inflammatory arthritis.

Cronstein, Bruce N / Aune, Thomas M

2020 Volume 16, Issue 3, Page(s) 145–154

Abstract: Despite the introduction of numerous biologic agents for the treatment of rheumatoid arthritis (RA) and other forms of inflammatory arthritis, low-dose methotrexate therapy remains the gold standard in RA therapy. Methotrexate is generally the first-line ...

Abstract	Despite the introduction of numerous biologic agents for the treatment of rheumatoid arthritis (RA) and other forms of inflammatory arthritis, low-dose methotrexate therapy remains the gold standard in RA therapy. Methotrexate is generally the first-line drug for the treatment of RA, psoriatic arthritis and other forms of inflammatory arthritis, and it enhances the effect of most biologic agents in RA. Understanding the mechanism of action of methotrexate could be instructive in the appropriate use of the drug and in the design of new regimens for the treatment of RA. Although methotrexate is one of the first examples of intelligent drug design, multiple mechanisms potentially contribute to the anti-inflammatory actions of methotrexate, including the inhibition of purine and pyrimidine synthesis, transmethylation reactions, translocation of nuclear factor-κB (NF-κB) to the nucleus, signalling via the Janus kinase (JAK)-signal transducer and activator of transcription (STAT) pathway and nitric oxide production, as well as the promotion of adenosine release and expression of certain long non-coding RNAs.
MeSH term(s)	Aminoimidazole Carboxamide/analogs & derivatives ; Aminoimidazole Carboxamide/antagonists & inhibitors ; Antirheumatic Agents/therapeutic use ; Arthritis/drug therapy ; Arthritis/immunology ; Arthritis/metabolism ; Humans ; Immunity, Cellular/drug effects ; Methotrexate/therapeutic use ; Ribonucleotides/antagonists & inhibitors ; T-Lymphocytes/drug effects ; T-Lymphocytes/immunology ; Tetrahydrofolate Dehydrogenase/drug effects ; Tetrahydrofolate Dehydrogenase/metabolism
Chemical Substances	Antirheumatic Agents ; Ribonucleotides ; Aminoimidazole Carboxamide (360-97-4) ; Tetrahydrofolate Dehydrogenase (EC 1.5.1.3) ; AICA ribonucleotide (F0X88YW0YK) ; Methotrexate (YL5FZ2Y5U1)
Language	English
Publishing date	2020-02-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2491532-4
ISSN	1759-4804 ; 1759-4790
ISSN (online)	1759-4804
ISSN	1759-4790
DOI	10.1038/s41584-020-0373-9
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Article ; Online: Immunoprecipitation of DNA:RNA Hybrids Using the S9.6 Antibody.

Gibbons, Hunter R / Aune, Thomas M

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

2020 Volume 2161, Page(s) 195–207

Abstract: Formation of DNA:RNA hybrids or R-loops contributes to numerous biologic processes. The development of the S9.6 antibody makes the analysis of R-Loops (DNA:RNA hybrids) possible through immunoprecipitation. Here, we describe the isolation of DNA:RNA ... ...

Abstract	Formation of DNA:RNA hybrids or R-loops contributes to numerous biologic processes. The development of the S9.6 antibody makes the analysis of R-Loops (DNA:RNA hybrids) possible through immunoprecipitation. Here, we describe the isolation of DNA:RNA hybrid structures using the S9.6 antibody. Using this protocol, both the DNA and RNA binding partners of the R-loop can be analyzed via qPCR, whole genome sequencing, or other methods.
MeSH term(s)	Antibodies/immunology ; DNA/chemistry ; HEK293 Cells ; Humans ; Immunoprecipitation/methods ; R-Loop Structures/immunology ; RNA/chemistry ; Sequence Analysis, RNA/methods
Chemical Substances	Antibodies ; RNA (63231-63-0) ; DNA (9007-49-2)
Language	English
Publishing date	2020-07-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-0680-3_14
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Article ; Online: A simplified method to produce mRNAs and functional proteins from synthetic double-stranded DNA templates.

Tossberg, John T / Esmond, Tashawna M / Aune, Thomas M

BioTechniques

2020 Volume 69, Issue 4, Page(s) 281–288

Abstract: We present a method to synthesize mRNAs from synthetic DNA templates that produce biologically active proteins. To illustrate utility, we constructed five unique synthetic DNA templates, produced mRNAs and demonstrated biologic activity of their ... ...

Abstract	We present a method to synthesize mRNAs from synthetic DNA templates that produce biologically active proteins. To illustrate utility, we constructed five unique synthetic DNA templates, produced mRNAs and demonstrated biologic activity of their translated proteins. Examples include secreted luciferase, enhanced green fluorescence protein, IL-4, and IL-12A and IL-12B to form active IL-12. We propose that this method offers a cost- and time-saving alternative to plasmid-based cloning.
MeSH term(s)	Cloning, Molecular ; DNA/biosynthesis ; DNA/genetics ; Green Fluorescent Proteins/chemistry ; Interleukin-12/biosynthesis ; Interleukin-12/genetics ; Interleukin-4/biosynthesis ; Interleukin-4/genetics ; Luciferases/genetics ; Plasmids/genetics ; Protein Biosynthesis/genetics ; Proteins/genetics ; RNA, Messenger/biosynthesis ; RNA, Messenger/chemistry ; RNA, Messenger/genetics ; Templates, Genetic
Chemical Substances	Proteins ; RNA, Messenger ; enhanced green fluorescent protein ; Green Fluorescent Proteins (147336-22-9) ; Interleukin-12 (187348-17-0) ; Interleukin-4 (207137-56-2) ; DNA (9007-49-2) ; Luciferases (EC 1.13.12.-)
Keywords	covid19
Language	English
Publishing date	2020-08-20
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	48453-2
ISSN	1940-9818 ; 0736-6205
ISSN (online)	1940-9818
ISSN	0736-6205
DOI	10.2144/btn-2020-0037
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Article ; Online: Reduced A-to-I editing of endogenous Alu RNAs in lung after SARS-CoV-2 infection.

Crooke, Philip S / Tossberg, John T / Porter, Krislyn P / Aune, Thomas M

Current research in immunology

2021 Volume 2, Page(s) 52–59

Abstract: Due to potential severity of disease caused by SARS-CoV-2 infection, it is critical to understand both mechanisms of viral pathogenesis as well as diversity of host responses to infection. Reduced A-to-I editing of endogenous double-stranded RNAs (dsRNAs) ...

Abstract	Due to potential severity of disease caused by SARS-CoV-2 infection, it is critical to understand both mechanisms of viral pathogenesis as well as diversity of host responses to infection. Reduced A-to-I editing of endogenous double-stranded RNAs (dsRNAs), as a result of inactivating mutations in
Language	English
Publishing date	2021-04-30
Publishing country	Netherlands
Document type	Journal Article
ISSN	2590-2555
ISSN (online)	2590-2555
DOI	10.1016/j.crimmu.2021.04.001
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Article ; Online: Cutting Edge: Reduced Adenosine-to-Inosine Editing of Endogenous Alu RNAs in Severe COVID-19 Disease.

Crooke, Philip S / Tossberg, John T / Porter, Krislyn P / Aune, Thomas M

Journal of immunology (Baltimore, Md. : 1950)

2021 Volume 206, Issue 8, Page(s) 1691–1696

Abstract: Severe COVID-19 disease is associated with elevated inflammatory responses. One form of Aicardi-Goutières syndrome caused by inactivating mutations ... ...

Abstract	Severe COVID-19 disease is associated with elevated inflammatory responses. One form of Aicardi-Goutières syndrome caused by inactivating mutations in
MeSH term(s)	Adenosine/genetics ; Adenosine/metabolism ; Alu Elements/genetics ; COVID-19/genetics ; COVID-19/pathology ; Dendritic Cells/metabolism ; Dendritic Cells/virology ; Genome, Human ; Humans ; Inosine/genetics ; Inosine/metabolism ; Interferon Regulatory Factors/metabolism ; NF-kappa B/metabolism ; RNA Editing/genetics ; RNA, Double-Stranded/genetics ; RNA-Seq ; SARS-CoV-2 ; Severity of Illness Index ; Signal Transduction/genetics
Chemical Substances	Interferon Regulatory Factors ; NF-kappa B ; RNA, Double-Stranded ; Inosine (5A614L51CT) ; Adenosine (K72T3FS567)
Language	English
Publishing date	2021-03-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2001428
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Article ; Online: Alu RNA Structural Features Modulate Immune Cell Activation and A-to-I Editing of Alu RNAs Is Diminished in Human Inflammatory Bowel Disease.

Aune, Thomas M / Tossberg, John T / Heinrich, Rachel M / Porter, Krislyn P / Crooke, Philip S

Frontiers in immunology

2022 Volume 13, Page(s) 818023

Abstract: Alu retrotransposons belong to the class of short interspersed nuclear elements (SINEs). Alu RNA is abundant in cells and its repetitive structure forms double-stranded RNAs (dsRNA) that activate dsRNA sensors and trigger innate immune responses with ... ...

Abstract	Alu retrotransposons belong to the class of short interspersed nuclear elements (SINEs). Alu RNA is abundant in cells and its repetitive structure forms double-stranded RNAs (dsRNA) that activate dsRNA sensors and trigger innate immune responses with significant pathological consequences. Mechanisms to prevent innate immune activation include deamination of adenosines to inosines in dsRNAs, referred to as A-to-I editing, degradation of Alu RNAs by endoribonucleases, and sequestration of Alu RNAs by RNA binding proteins. We have previously demonstrated that widespread loss of Alu RNA A-to-I editing is associated with diverse human diseases including viral (COVID-19, influenza) and autoimmune diseases (multiple sclerosis). Here we demonstrate loss of A-to-I editing in leukocytes is also associated with inflammatory bowel diseases. Our structure-function analysis demonstrates that ability to activate innate immune responses resides in the left arm of Alu RNA, requires a 5'-PPP, RIG-I is the major Alu dsRNA sensor, and A-to-I editing disrupts both structure and function. Further, edited Alu RNAs inhibit activity of unedited Alu RNAs. Altering Alu RNA nucleotide sequence increases biological activity. Two classes of Alu RNAs exist, one class stimulates both IRF and NF-kB transcriptional activity and a second class only stimulates IRF transcriptional activity. Thus, Alu RNAs play important roles in human disease but may also have therapeutic potential.
MeSH term(s)	Adenosine ; Alu Elements/genetics ; Alu Elements/immunology ; COVID-19 ; Humans ; Inflammatory Bowel Diseases/genetics ; Inflammatory Bowel Diseases/immunology ; Inosine ; RNA, Double-Stranded/genetics ; RNA, Double-Stranded/immunology ; SARS-CoV-2
Chemical Substances	RNA, Double-Stranded ; Inosine (5A614L51CT) ; Adenosine (K72T3FS567)
Language	English
Publishing date	2022-01-20
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.818023
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Article ; Online: Reduced RNA adenosine-to-inosine editing in hippocampus vasculature associated with Alzheimer's disease.

Crooke, Philip S / Tossberg, John T / Heinrich, Rachel M / Porter, Krislyn P / Aune, Thomas M

Brain communications

2022 Volume 4, Issue 5, Page(s) fcac238

Abstract: Alzheimer's disease is the most common form of dementia and recent studies identify a type 1 interferon response in Alzheimer's disease possibly driving neuro-inflammation and other Alzheimer's disease pathologies. Loss of adenosine-to-inosine editing of ...

Abstract	Alzheimer's disease is the most common form of dementia and recent studies identify a type 1 interferon response in Alzheimer's disease possibly driving neuro-inflammation and other Alzheimer's disease pathologies. Loss of adenosine-to-inosine editing of endogenous Alu RNAs results in accumulation of Alu double-stranded RNAs, activation of double-stranded RNA sensors, and induction of interferon and nuclear factor kappa B regulated genes. Here, we investigated if changes in adenosine-to-inosine editing were associated with presence of Alzheimer's disease in total prefrontal cortex, total hippocampus, cortex vasculature and hippocampus vasculature using available RNA sequencing files. We found similar levels of Alu RNA adenosine-to-inosine editing in cortex and cortex vasculature from individuals with Alzheimer's disease or normal cognition at the time of death and brain donation. We found modest and substantial loss of adenosine-to-inosine editing in hippocampus and hippocampus vasculature, respectively, in Alzheimer's disease relative to normal cognition and increased expression of interferon and nuclear factor kappa B regulated genes in hippocampus. Unedited Alu RNAs as found in Alzheimer's disease hippocampus vasculature were potent innate immune activators while edited Alu RNAs as found in normal cognition hippocampus vasculature were weak innate immune activators. Taken together, our results support a model whereby loss of Alu RNA adenosine-to-inosine editing in hippocampus results in innate immune activation that may contribute to Alzheimer's disease pathogenesis.
Language	English
Publishing date	2022-09-22
Publishing country	England
Document type	Journal Article
ISSN	2632-1297
ISSN (online)	2632-1297
DOI	10.1093/braincomms/fcac238
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Article ; Online: Nanoparticle Delivery of Immunostimulatory Alu RNA for Cancer Immunotherapy.

Garland, Kyle M / Kwiatkowski, Alexander J / Tossberg, John T / Crooke, Philip S / Aune, Thomas M / Wilson, John T

Cancer research communications

2023 Volume 3, Issue 9, Page(s) 1800–1809

Abstract: It was recently found that patients with relapsing remitting multiple sclerosis exhibit widespread loss of adenosine-to-inosine (A-to-I) RNA editing, which contributes to the accumulation of immunostimulatory double-stranded Alu RNA in circulating ... ...

Abstract	It was recently found that patients with relapsing remitting multiple sclerosis exhibit widespread loss of adenosine-to-inosine (A-to-I) RNA editing, which contributes to the accumulation of immunostimulatory double-stranded Alu RNA in circulating leukocytes and an attendant increase in levels of proinflammatory cytokines (e.g., type I IFNs). A specific Alu RNA (i.e., AluJb RNA) was implicated in activating multiple RNA-sensing pathways and found to be a potent innate immune agonist. Here, we have performed a bioinformatic analysis of A-to-I RNA editing in human melanoma samples and determined that pre-therapy levels of A-to-I RNA editing negatively correlate with survival times, suggesting that an accumulation of endogenous double-stranded Alu RNA might contribute to cancer patient survival. Furthermore, we demonstrated that immunostimulatory Alu RNA can be leveraged pharmacologically for cancer immunotherapy. AluJb RNA was Significance: Loss of A-to-I editing leads to accumulation of unedited Alu RNAs that activate innate immunity via RNA-sensing pattern recognition receptors. When packaged into endosome-releasing polymer nanoparticles, AluJB RNA becomes highly immunostimulatory and can be used pharmacologically to inhibit tumor growth in mouse melanoma models. These findings identify Alu RNAs as a new class of nucleic acid innate immune agonists for cancer immunotherapy.
MeSH term(s)	Humans ; Animals ; Mice ; Immunotherapy ; Immunization ; Nucleic Acids ; RNA, Double-Stranded ; Melanoma/genetics
Chemical Substances	Nucleic Acids ; RNA, Double-Stranded
Language	English
Publishing date	2023-09-08
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	2767-9764
ISSN (online)	2767-9764
DOI	10.1158/2767-9764.CRC-22-0354
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Article ; Online: Long non-coding RNAs in innate and adaptive immunity.

Aune, Thomas M / Spurlock, Charles F

Virus research

2015 Volume 212, Page(s) 146–160

Abstract: Long noncoding RNAs (lncRNAs) represent a newly discovered class of regulatory molecules that impact a variety of biological processes in cells and organ systems. In humans, it is estimated that there may be more than twice as many lncRNA genes than ... ...

Abstract	Long noncoding RNAs (lncRNAs) represent a newly discovered class of regulatory molecules that impact a variety of biological processes in cells and organ systems. In humans, it is estimated that there may be more than twice as many lncRNA genes than protein-coding genes. However, only a handful of lncRNAs have been analyzed in detail. In this review, we describe expression and functions of lncRNAs that have been demonstrated to impact innate and adaptive immunity. These emerging paradigms illustrate remarkably diverse mechanisms that lncRNAs utilize to impact the transcriptional programs of immune cells required to fight against pathogens and maintain normal health and homeostasis.
MeSH term(s)	Adaptive Immunity ; Animals ; Humans ; Immunity, Innate ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/immunology ; Virus Diseases/genetics ; Virus Diseases/immunology ; Virus Diseases/virology ; Viruses/genetics ; Viruses/immunology
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2015-07-09
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2015.07.003
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Article ; Online: Adenosine-to-Inosine RNA Editing of Alu Double-Stranded (ds)RNAs Is Markedly Decreased in Multiple Sclerosis and Unedited Alu dsRNAs Are Potent Activators of Proinflammatory Transcriptional Responses.

Tossberg, John T / Heinrich, Rachel M / Farley, Virginia M / Crooke, Philip S / Aune, Thomas M

Journal of immunology (Baltimore, Md. : 1950)

2020 Volume 205, Issue 10, Page(s) 2606–2617

Abstract: Sensors that detect dsRNA stimulate IFN responses as a defense against viral infection. IFN responses are also well documented in a variety of human autoimmune diseases, including relapsing-remitting multiple sclerosis (MS), in which increased IFN ... ...

Abstract	Sensors that detect dsRNA stimulate IFN responses as a defense against viral infection. IFN responses are also well documented in a variety of human autoimmune diseases, including relapsing-remitting multiple sclerosis (MS), in which increased IFN responses result from increased levels of double-stranded endogenous Alu RNAs. Mechanisms underlying increases in double-stranded Alu RNAs in MS are obscure. We find widespread loss of adenosine-to-inosine editing of Alu RNAs in MS. Unedited Alu RNAs are potent activators of both IFN and NF-κB responses via the dsRNA sensors, RIG-I, and TLR3. Minor editing of highly active Alu elements abrogates the ability to activate both transcriptional responses. Thus, adenosine-to-inosine editing may also represent an important defense against autoimmune diseases such as MS.
MeSH term(s)	Adenosine/genetics ; Alu Elements/genetics ; Alu Elements/immunology ; DEAD Box Protein 58/metabolism ; Datasets as Topic ; HEK293 Cells ; Humans ; Inflammation/genetics ; Inflammation/immunology ; Inosine/genetics ; Interferons/metabolism ; Multiple Sclerosis, Relapsing-Remitting/blood ; Multiple Sclerosis, Relapsing-Remitting/genetics ; Multiple Sclerosis, Relapsing-Remitting/immunology ; NF-kappa B/metabolism ; RNA Editing/immunology ; RNA, Double-Stranded/genetics ; RNA, Double-Stranded/immunology ; RNA, Double-Stranded/metabolism ; RNA-Seq ; Receptors, Immunologic/metabolism ; Signal Transduction/genetics ; Signal Transduction/immunology ; THP-1 Cells ; Toll-Like Receptor 3/metabolism ; Transcriptional Activation/immunology ; Whole Genome Sequencing
Chemical Substances	NF-kappa B ; RNA, Double-Stranded ; Receptors, Immunologic ; TLR3 protein, human ; Toll-Like Receptor 3 ; Inosine (5A614L51CT) ; Interferons (9008-11-1) ; RIGI protein, human (EC 3.6.1.-) ; DEAD Box Protein 58 (EC 3.6.4.13) ; Adenosine (K72T3FS567)
Language	English
Publishing date	2020-10-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2000384
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