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Article ; Online: Suppression of PI3K signaling is linked to autophagy activation and the spatiotemporal induction of the lens organelle free zone.

Gheyas, Rifah / Ortega-Alvarez, Ramon / Chauss, Daniel / Kantorow, Marc / Menko, A Sue

2022 Volume 412, Issue 2, Page(s) 113043

Abstract: The terminal steps of lens cell differentiation require elimination of all organelles to create a central Organelle Free Zone (OFZ) that is required for lens function of focusing images on the retina. Previous studies show that the spatiotemporal ... ...

Abstract	The terminal steps of lens cell differentiation require elimination of all organelles to create a central Organelle Free Zone (OFZ) that is required for lens function of focusing images on the retina. Previous studies show that the spatiotemporal elimination of these organelles during development is autophagy-dependent. We now show that the inhibition of PI3K signaling in lens organ culture results in the premature induction of autophagy within 24 h, including a significant increase in LAMP1+ lysosomes, and the removal of lens organelles from the center of the lens. Specific inhibition of just the PI3K/Akt signaling axis was directly linked to the elimination of mitochondria and ER, while pan-PI3K inhibitors that block all PI3K downstream signaling removed all organelles, including nuclei. Therefore, blocking the PI3K/Akt pathway was alone insufficient to remove nuclei. RNAseq analysis revealed increased mRNA levels of the endogenous inhibitor of PI3K activation, PIK3IP1, in differentiating lens fiber cells preceding the induction of OFZ formation. Co-immunoprecipitation confirmed that PIK3IP1 associates with multiple PI3K p110 isoforms just prior to formation of the OFZ, providing a likely endogenous mechanism for blocking all PI3K signaling and activating the autophagy pathway required to form the OFZ during lens development.
MeSH term(s)	Animals ; Autophagy/physiology ; Cell Differentiation/physiology ; Cell Nucleus/metabolism ; Cell Nucleus/physiology ; Chick Embryo ; Epithelial Cells/metabolism ; Epithelial Cells/physiology ; Eye/metabolism ; Eye/physiopathology ; Lens, Crystalline/metabolism ; Lens, Crystalline/physiology ; Mitochondria/metabolism ; Mitochondria/physiology ; Phosphatidylinositol 3-Kinases/metabolism ; Proto-Oncogene Proteins c-akt/metabolism ; Signal Transduction/physiology
Chemical Substances	Proto-Oncogene Proteins c-akt (EC 2.7.11.1)
Language	English
Publishing date	2022-01-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1493-x
ISSN	1090-2422 ; 0014-4827
ISSN (online)	1090-2422
ISSN	0014-4827
DOI	10.1016/j.yexcr.2022.113043
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Article ; Online: Non-coding RNAs in immunoregulation and autoimmunity: Technological advances and critical limitations.

Kumar, Dhaneshwar / Sahoo, Subhransu Sekhar / Chauss, Daniel / Kazemian, Majid / Afzali, Behdad

Journal of autoimmunity

2022 Volume 134, Page(s) 102982

Abstract: Immune cell function is critically dependent on precise control over transcriptional output from the genome. In this respect, integration of environmental signals that regulate gene expression, specifically by transcription factors, enhancer DNA elements, ...

Abstract	Immune cell function is critically dependent on precise control over transcriptional output from the genome. In this respect, integration of environmental signals that regulate gene expression, specifically by transcription factors, enhancer DNA elements, genome topography and non-coding RNAs (ncRNAs), are key components. The first three have been extensively investigated. Even though non-coding RNAs represent the vast majority of cellular RNA species, this class of RNA remains historically understudied. This is partly because of a lag in technological and bioinformatic innovations specifically capable of identifying and accurately measuring their expression. Nevertheless, recent progress in this domain has enabled a profusion of publications identifying novel sub-types of ncRNAs and studies directly addressing the function of ncRNAs in human health and disease. Many ncRNAs, including circular and enhancer RNAs, have now been demonstrated to play key functions in the regulation of immune cells and to show associations with immune-mediated diseases. Some ncRNAs may function as biomarkers of disease, aiding in diagnostics and in estimating response to treatment, while others may play a direct role in the pathogenesis of disease. Importantly, some are relatively stable and are amenable to therapeutic targeting, for example through gene therapy. Here, we provide an overview of ncRNAs and review technological advances that enable their study and hold substantial promise for the future. We provide context-specific examples by examining the associations of ncRNAs with four prototypical human autoimmune diseases, specifically rheumatoid arthritis, psoriasis, inflammatory bowel disease and multiple sclerosis. We anticipate that the utility and mechanistic roles of these ncRNAs in autoimmunity will be further elucidated in the near future.
MeSH term(s)	Humans ; Autoimmunity/genetics ; RNA, Untranslated/genetics ; RNA, Untranslated/metabolism ; Autoimmune Diseases/diagnosis ; Autoimmune Diseases/genetics ; Arthritis, Rheumatoid ; Multiple Sclerosis
Chemical Substances	RNA, Untranslated
Language	English
Publishing date	2022-12-31
Publishing country	England
Document type	Journal Article ; Review ; Research Support, N.I.H., Intramural ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	639452-8
ISSN	1095-9157 ; 0896-8411
ISSN (online)	1095-9157
ISSN	0896-8411
DOI	10.1016/j.jaut.2022.102982
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Zs.A 2368: Show issues

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Article ; Online: A functional map of genomic HIF1α-DNA complexes in the eye lens revealed through multiomics analysis.

Disatham, Joshua / Brennan, Lisa / Chauss, Daniel / Kantorow, Jason / Afzali, Behdad / Kantorow, Marc

BMC genomics

2021 Volume 22, Issue 1, Page(s) 497

Abstract: Background: During eye lens development the embryonic vasculature regresses leaving the lens without a direct oxygen source. Both embryonically and throughout adult life, the lens contains a decreasing oxygen gradient from the surface to the core that ... ...

Abstract	Background: During eye lens development the embryonic vasculature regresses leaving the lens without a direct oxygen source. Both embryonically and throughout adult life, the lens contains a decreasing oxygen gradient from the surface to the core that parallels the natural differentiation of immature surface epithelial cells into mature core transparent fiber cells. These properties of the lens suggest a potential role for hypoxia and the master regulator of the hypoxic response, hypoxia-inducible transcription factor 1 (HIF1), in the regulation of genes required for lens fiber cell differentiation, structure and transparency. Here, we employed a multiomics approach combining CUT&RUN, RNA-seq and ATACseq analysis to establish the genomic complement of lens HIF1α binding sites, genes activated or repressed by HIF1α and the chromatin states of HIF1α-regulated genes. Results: CUT&RUN analysis revealed 8375 HIF1α-DNA binding complexes in the chick lens genome. One thousand one hundred ninety HIF1α-DNA binding complexes were significantly clustered within chromatin accessible regions (χ Conclusions: These data establish the first functional map of genomic HIF1α-DNA complexes in the eye lens. They identify HIF1α as an important regulator of a wide-variety of genes previously shown to be critical for lens formation and function and they reveal a requirement for HIF1α in the regulation of a wide-variety of genes not yet examined for lens function. They support a requirement for HIF1α in lens fiber cell formation, structure and function and they provide a basis for understanding the potential roles and requirements for HIF1α in the development, structure and function of more complex tissues.
MeSH term(s)	Cell Differentiation ; Chromatin ; DNA ; Genomics ; Hypoxia-Inducible Factor 1, alpha Subunit ; Lens, Crystalline
Chemical Substances	Chromatin ; Hypoxia-Inducible Factor 1, alpha Subunit ; DNA (9007-49-2)
Language	English
Publishing date	2021-07-03
Publishing country	England
Document type	Journal Article
ZDB-ID	2041499-7
ISSN	1471-2164 ; 1471-2164
ISSN (online)	1471-2164
ISSN	1471-2164
DOI	10.1186/s12864-021-07795-9
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Article ; Online: Patterns of Crystallin Gene Expression in Differentiation State Specific Regions of the Embryonic Chicken Lens.

Ma, Zhiwei / Chauss, Daniel / Disatham, Joshua / Jiao, Xiaodong / Brennan, Lisa Ann / Menko, A Sue / Kantorow, Marc / Hejtmancik, J Fielding

Investigative ophthalmology & visual science

2022 Volume 63, Issue 4, Page(s) 8

Abstract: Purpose: Transition from lens epithelial cells to lens fiber cell is accompanied by numerous changes in gene expression critical for lens transparency. We identify expression patterns of highly prevalent genes including ubiquitous and enzyme crystallins ...

Abstract	Purpose: Transition from lens epithelial cells to lens fiber cell is accompanied by numerous changes in gene expression critical for lens transparency. We identify expression patterns of highly prevalent genes including ubiquitous and enzyme crystallins in the embryonic day 13 chicken lens. Methods: Embryonic day 13 chicken lenses were dissected into central epithelial cell (EC), equatorial epithelial cell (EQ), cortical fiber cell (FP), and nuclear fiber cell (FC) compartments. Total RNA was prepared, subjected to high-throughput unidirectional mRNA sequencing, analyzed, mapped to the chicken genome, and functionally grouped. Results: A total of 77,097 gene-specific transcripts covering 17,450 genes were expressed, of which 10,345 differed between two or more lens subregions. Ubiquitous crystallin gene expression increased from EC to EQ and was similar in FP and FC. Highly expressed crystallin genes fell into three coordinately expressed groups with R2 ≥ 0.93: CRYAA, CRYBB2, CRYAB, and CRYBA2; CRYBB1, CRYBA4, CRYGN, ASL1, and ASL; and CRYBB3 and CRYBA1. The highly expressed transcription factors YBX1, YBX3, PNRC1, and BASP1 were coordinately expressed with the second group of crystallins (r2 > 0.88). Conclusions: Although it is well known that lens crystallin gene expression changes during the epithelial to fiber cell transition, these data identify for the first time three distinct patterns of expression for specific subsets of crystallin genes, each highly correlated with expression of specific transcription factors. The results provide a quantitative basis for designing functional experiments pinpointing the mechanisms governing the landscape of crystallin expression during fiber cell differentiation to attain lens transparency.
MeSH term(s)	Animals ; Cell Differentiation ; Chick Embryo ; Chickens ; Crystallins/genetics ; Crystallins/metabolism ; Gene Expression ; Lens, Crystalline/metabolism ; Transcription Factors/metabolism
Chemical Substances	Crystallins ; Transcription Factors
Language	English
Publishing date	2022-04-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.63.4.8
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Zs.A 45: Show issues

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Article ; Online: 1,25-Dihydroxyvitamin D3 suppresses CD4

Bishop, Emma L / Gudgeon, Nancy H / Mackie, Gillian M / Chauss, Daniel / Roberts, Jennie / Tennant, Daniel A / Maslowski, Kendle M / Afzali, Behdad / Hewison, Martin / Dimeloe, Sarah

Immunology

2022 Volume 166, Issue 3, Page(s) 299–309

Abstract: ... In ... ...

Abstract	In CD4
MeSH term(s)	Calcitriol/metabolism ; Calcitriol/pharmacology ; Glycolysis ; Interferon-gamma/metabolism ; T-Lymphocytes, Helper-Inducer/metabolism ; Vitamin D
Chemical Substances	Vitamin D (1406-16-2) ; Interferon-gamma (82115-62-6) ; Calcitriol (FXC9231JVH)
Language	English
Publishing date	2022-03-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Intramural
ZDB-ID	80124-0
ISSN	1365-2567 ; 0019-2805 ; 0953-4954
ISSN (online)	1365-2567
ISSN	0019-2805 ; 0953-4954
DOI	10.1111/imm.13472
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Article ; Online: Folic acid-mediated fibrosis is driven by C5a receptor 1-mediated activation of kidney myeloid cells.

Sahu, Ranjit K / Xavier, Sandhya / Chauss, Daniel / Wang, Luopin / Chew, Claude / Taylor, Ronald / Stallcup, William B / Ma, Jennie Z / Kazemian, Majid / Afzali, Behdad / Köhl, Jörg / Portilla, Didier

American journal of physiology. Renal physiology

2022 Volume 322, Issue 6, Page(s) F597–F610

Abstract: We have previously reported that increased expression and activation of kidney cell complement components play an important role in the pathogenesis of renal scarring. Here, we used floxed green fluorescent protein (GFP)-C5a receptor 1 (C5aR1) knockin ... ...

Abstract	We have previously reported that increased expression and activation of kidney cell complement components play an important role in the pathogenesis of renal scarring. Here, we used floxed green fluorescent protein (GFP)-C5a receptor 1 (C5aR1) knockin mice (GFP-
MeSH term(s)	Animals ; Cicatrix ; Fibrosis ; Folic Acid/pharmacology ; Green Fluorescent Proteins ; Kidney/pathology ; Mice ; Mice, Knockout ; Myeloid Cells/pathology ; Receptor, Anaphylatoxin C5a/genetics ; Receptors, Platelet-Derived Growth Factor
Chemical Substances	Receptor, Anaphylatoxin C5a ; Green Fluorescent Proteins (147336-22-9) ; Folic Acid (935E97BOY8) ; Receptors, Platelet-Derived Growth Factor (EC 2.7.10.1)
Language	English
Publishing date	2022-04-04
Publishing country	United States
Document type	Journal Article
ZDB-ID	603837-2
ISSN	1522-1466 ; 0363-6127
ISSN (online)	1522-1466
ISSN	0363-6127
DOI	10.1152/ajprenal.00404.2021
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Article ; Online: Transcription factor EGR2 controls homing and pathogenicity of T

Nature immunology

2023 Volume 24, Issue 8, Page(s) 1331–1344

Abstract: ... ...

Abstract	CD4
MeSH term(s)	Animals ; Mice ; Cell Differentiation ; Central Nervous System ; Encephalomyelitis, Autoimmune, Experimental ; Mice, Inbred C57BL ; Multiple Sclerosis ; Neuroinflammatory Diseases ; Th1 Cells ; Th17 Cells ; Transcription Factors ; Virulence ; Humans
Chemical Substances	Egr2 protein, mouse ; Transcription Factors
Language	English
Publishing date	2023-07-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/s41590-023-01553-7
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Article ; Online: Reply to Grigoriev et al., "Sequences of SARS-CoV-2 'Hybrids' with the Human Genome: Signs of Non-coding RNA?"

Yan, Bingyu / Chakravorty, Srishti / Mirabelli, Carmen / Wang, Luopin / Trujillo-Ochoa, Jorge L / Chauss, Daniel / Kumar, Dhaneshwar / Lionakis, Michail S / Olson, Matthew R / Wobus, Christiane E / Afzali, Behdad / Kazemian, Majid

Journal of virology

2021 Volume 96, Issue 2, Page(s) e0169021

MeSH term(s)	COVID-19 ; Genome, Human ; Genome, Viral/genetics ; Humans ; RNA, Untranslated ; RNA, Viral/genetics ; SARS-CoV-2
Chemical Substances	RNA, Untranslated ; RNA, Viral
Language	English
Publishing date	2021-10-27
Publishing country	United States
Document type	Letter ; Research Support, N.I.H., Extramural ; Research Support, N.I.H., Intramural ; Comment
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.01690-21
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Article: Host-virus chimeric events in SARS-CoV2 infected cells are infrequent and artifactual.

bioRxiv : the preprint server for biology

2021

Abstract: Pathogenic mechanisms underlying severe SARS-CoV2 infection remain largely unelucidated. High throughput sequencing technologies that capture genome and transcriptome information are key approaches to gain detailed mechanistic insights from infected ... ...

Abstract	Pathogenic mechanisms underlying severe SARS-CoV2 infection remain largely unelucidated. High throughput sequencing technologies that capture genome and transcriptome information are key approaches to gain detailed mechanistic insights from infected cells. These techniques readily detect both pathogen and host-derived sequences, providing a means of studying host-pathogen interactions. Recent studies have reported the presence of host-virus chimeric (HVC) RNA in RNA-seq data from SARS-CoV2 infected cells and interpreted these findings as evidence of viral integration in the human genome as a potential pathogenic mechanism. Since SARS-CoV2 is a positive sense RNA virus that replicates in the cytoplasm it does not have a nuclear phase in its life cycle, it is biologically unlikely to be in a location where splicing events could result in genome integration. Here, we investigated the biological authenticity of HVC events. In contrast to true biological events such as mRNA splicing and genome rearrangement events, which generate reproducible chimeric sequencing fragments across different biological isolates, we found that HVC events across >100 RNA-seq libraries from patients with COVID-19 and infected cell lines, were highly irreproducible. RNA-seq library preparation is inherently error-prone due to random template switching during reverse transcription of RNA to cDNA. By counting chimeric events observed when constructing an RNA-seq library from human RNA and spike-in RNA from an unrelated species, such as fruit-fly, we estimated that ~1% of RNA-seq reads are artifactually chimeric. In SARS-CoV2 RNA-seq we found that the frequency of HVC events was, in fact, not greater than this background "noise". Finally, we developed a novel experimental approach to enrich SARS-CoV2 sequences from bulk RNA of infected cells. This method enriched viral sequences but did not enrich for HVC events, suggesting that the majority of HVC events are, in all likelihood, artifacts of library construction. In conclusion, our findings indicate that HVC events observed in RNA-sequencing libraries from SARS-CoV2 infected cells are extremely rare and are likely artifacts arising from either random template switching of reverse-transcriptase and/or sequence alignment errors. Therefore, the observed HVC events do not support SARS-CoV2 fusion to cellular genes and/or integration into human genomes.
Language	English
Publishing date	2021-02-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.02.17.431704
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Article ; Online: Host-Virus Chimeric Events in SARS-CoV-2-Infected Cells Are Infrequent and Artifactual.

Journal of virology

2021 Volume 95, Issue 15, Page(s) e0029421

Abstract: The pathogenic mechanisms underlying severe SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) infection remain largely unelucidated. High-throughput sequencing technologies that capture genome and transcriptome information are key approaches ... ...

Abstract	The pathogenic mechanisms underlying severe SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) infection remain largely unelucidated. High-throughput sequencing technologies that capture genome and transcriptome information are key approaches to gain detailed mechanistic insights from infected cells. These techniques readily detect both pathogen- and host-derived sequences, providing a means of studying host-pathogen interactions. Recent studies have reported the presence of host-virus chimeric (HVC) RNA in transcriptome sequencing (RNA-seq) data from SARS-CoV-2-infected cells and interpreted these findings as evidence of viral integration in the human genome as a potential pathogenic mechanism. Since SARS-CoV-2 is a positive-sense RNA virus that replicates in the cytoplasm, it does not have a nuclear phase in its life cycle. Thus, it is biologically unlikely to be in a location where splicing events could result in genome integration. Therefore, we investigated the biological authenticity of HVC events. In contrast to true biological events like mRNA splicing and genome rearrangement events, which generate reproducible chimeric sequencing fragments across different biological isolates, we found that HVC events across >100 RNA-seq libraries from patients with coronavirus disease 2019 (COVID-19) and infected cell lines were highly irreproducible. RNA-seq library preparation is inherently error prone due to random template switching during reverse transcription of RNA to cDNA. By counting chimeric events observed when constructing an RNA-seq library from human RNA and spiked-in RNA from an unrelated species, such as the fruit fly, we estimated that ∼1% of RNA-seq reads are artifactually chimeric. In SARS-CoV-2 RNA-seq, we found that the frequency of HVC events was, in fact, not greater than this background "noise." Finally, we developed a novel experimental approach to enrich SARS-CoV-2 sequences from bulk RNA of infected cells. This method enriched viral sequences but did not enrich HVC events, suggesting that the majority of HVC events are, in all likelihood, artifacts of library construction. In conclusion, our findings indicate that HVC events observed in RNA-sequencing libraries from SARS-CoV-2-infected cells are extremely rare and are likely artifacts arising from random template switching of reverse transcriptase and/or sequence alignment errors. Therefore, the observed HVC events do not support SARS-CoV-2 fusion to cellular genes and/or integration into human genomes.
MeSH term(s)	COVID-19/genetics ; COVID-19/metabolism ; COVID-19/pathology ; Cell Line, Tumor ; Host-Pathogen Interactions ; Humans ; RNA, Viral/genetics ; RNA, Viral/metabolism ; RNA-Seq ; SARS-CoV-2/physiology ; Virus Replication
Chemical Substances	RNA, Viral
Language	English
Publishing date	2021-07-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, N.I.H., Intramural ; 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.00294-21
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