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Article: The Gut-Eye Axis: Lessons Learned from Murine Models.

Floyd, Jason L / Grant, Maria B

Ophthalmology and therapy

2020 Volume 9, Issue 3, Page(s) 499–513

Abstract: A healthy gut microbiota is essential in maintaining the human body in a homeostatic state by its functions in digestion and immune tolerance. Under states of aberrant microbial composition or function (dysbiosis), the gut microbiota induces systemic ... ...

Abstract	A healthy gut microbiota is essential in maintaining the human body in a homeostatic state by its functions in digestion and immune tolerance. Under states of aberrant microbial composition or function (dysbiosis), the gut microbiota induces systemic inflammation that can lead to the onset of many diseases. In this review, we describe some evidence, largely from rodent studies, that supports the possible role of a dysbiotic gut microbiota in the onset and exacerbation of ocular diseases, primarily diabetic retinopathy, age-related macular degeneration, choroidal neovascularization, and uveitis. Furthermore, we examine several potential therapeutic measures that show promise in restoring the gut microbiota to a eubiotic state, preventing the aforementioned disease pathologies.
Language	English
Publishing date	2020-07-02
Publishing country	England
Document type	Journal Article ; Review
ISSN	2193-8245
ISSN	2193-8245
DOI	10.1007/s40123-020-00278-2
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Article ; Online: Microbial Signatures in The Rodent Eyes With Retinal Dysfunction and Diabetic Retinopathy.

Prasad, Ram / Asare-Bediko, Bright / Harbour, Angela / Floyd, Jason L / Chakraborty, Dibyendu / Duan, Yaqian / Lamendella, Regina / Wright, Justin / Grant, Maria B

Investigative ophthalmology & visual science

2022 Volume 63, Issue 1, Page(s) 5

Abstract: Purpose: The gut microbiome has been linked to disease pathogenesis through their interaction in metabolic, endocrine, and immune functions. The goal of this study was to determine whether the gut and plasma microbiota could transfer microbes to the ... ...

Abstract	Purpose: The gut microbiome has been linked to disease pathogenesis through their interaction in metabolic, endocrine, and immune functions. The goal of this study was to determine whether the gut and plasma microbiota could transfer microbes to the retina in type 1 diabetic mice with retinopathy. Methods: We analyzed the fecal, plasma, whole globe, and retina microbiome in Akita mice and compared with age-matched wild-type (WT) mice using 16S rRNA sequencing and metatranscriptomic analysis. To eliminate the contribution of the ocular surface and plasma microbiome, mice were perfused with sterile saline solution, the whole globes were extracted, and the neural retina was removed under sterile conditions for retinal microbiome. Results: Our microbiome analysis revealed that Akita mice demonstrated a distinct pattern of microbes within each source: feces, plasma, whole globes, and retina. WT mice and Akita mice experienced transient bacteremia in the plasma and retina. Bacteria were identified in the retina of the Akita mice, specifically Corynebacterium, Pseudomonas, Lactobacillus, Staphylococcus, Enterococcus, and Bacillus. Significantly increased levels of peptidoglycan (0.036 ± 0.001 vs. 0.023 ± 0.002; P < 0.002) and TLR2 (3.47 ± 0.15 vs. 1.99 ± 0.07; P < 0.0001) were observed in the retina of Akita mice compared to WT. Increased IBA+ cells in the retina, reduced a- and b-waves on electroretinography, and increased acellular capillary formation demonstrated the presence of retinopathy in the Akita cohort compared to WT mice. Conclusions: Together, our findings suggest that transient bacteremia exists in the plasma and retina of both cohorts. The bacteria found in Akita mice are distinct from WT mice and may contribute to development of retinal inflammation and barrier dysfunction in retinopathy.
MeSH term(s)	Animals ; Bacteremia/microbiology ; Bacteria/genetics ; Bacteria/isolation & purification ; Diabetes Mellitus, Type 1/microbiology ; Diabetic Retinopathy/microbiology ; Disease Models, Animal ; Electroretinography ; Enzyme-Linked Immunosorbent Assay ; Eye/microbiology ; Feces/microbiology ; Gastrointestinal Microbiome/physiology ; Male ; Mice ; Mice, Inbred C57BL ; Microbiota/physiology ; RNA, Ribosomal, 16S/genetics ; Retina/microbiology
Chemical Substances	RNA, Ribosomal, 16S
Language	English
Publishing date	2022-01-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.63.1.5
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Article: Sustained ACE2 Expression by Probiotic Improves Integrity of Intestinal Lymphatics and Retinopathy in Type 1 Diabetic Model.

Prasad, Ram / Adu-Agyeiwaah, Yvonne / Floyd, Jason L / Asare-Bediako, Bright / Li Calzi, Sergio / Chakraborty, Dibyendu / Harbour, Angela / Rohella, Aayush / Busik, Julia V / Li, Qiuhong / Grant, Maria B

Journal of clinical medicine

2023 Volume 12, Issue 5

Abstract: Intestinal lymphatic, known as lacteal, plays a critical role in maintaining intestinal homeostasis by regulating several key functions, including the absorption of dietary lipids, immune cell trafficking, and interstitial fluid balance in the gut. The ... ...

Abstract	Intestinal lymphatic, known as lacteal, plays a critical role in maintaining intestinal homeostasis by regulating several key functions, including the absorption of dietary lipids, immune cell trafficking, and interstitial fluid balance in the gut. The absorption of dietary lipids relies on lacteal integrity, mediated by button-like and zipper-like junctions. Although the intestinal lymphatic system is well studied in many diseases, including obesity, the contribution of lacteals to the gut-retinal axis in type 1 diabetes (T1D) has not been examined. Previously, we showed that diabetes induces a reduction in intestinal angiotensin-converting enzyme 2 (ACE2), leading to gut barrier disruption. However, when ACE2 levels are maintained, a preservation of gut barrier integrity occurs, resulting in less systemic inflammation and a reduction in endothelial cell permeability, ultimately retarding the development of diabetic complications, such as diabetic retinopathy. Here, we examined the impact of T1D on intestinal lymphatics and circulating lipids and tested the impact of intervention with ACE-2-expressing probiotics on key aspects of gut and retinal function.
Language	English
Publishing date	2023-02-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2662592-1
ISSN	2077-0383
ISSN	2077-0383
DOI	10.3390/jcm12051771
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Article ; Online: Hematopoietic Cells Influence Vascular Development in the Retina.

Asare-Bediako, Bright / Adu-Agyeiwaah, Yvonne / Abad, Antonio / Li Calzi, Sergio / Floyd, Jason L / Prasad, Ram / DuPont, Mariana / Asare-Bediako, Richmond / Bustelo, Xose R / Grant, Maria B

Cells

2022 Volume 11, Issue 20

Abstract: Hematopoietic cells play a crucial role in the adult retina in health and disease. Monocytes, macrophages, microglia and myeloid angiogenic cells (MACs) have all been implicated in retinal pathology. However, the role that hematopoietic cells play in ... ...

Abstract	Hematopoietic cells play a crucial role in the adult retina in health and disease. Monocytes, macrophages, microglia and myeloid angiogenic cells (MACs) have all been implicated in retinal pathology. However, the role that hematopoietic cells play in retinal development is understudied. The temporal changes in recruitment of hematopoietic cells into the developing retina and the phenotype of the recruited cells are not well understood. In this study, we used the hematopoietic cell-specific protein Vav1 to track and investigate hematopoietic cells in the developing retina. By flow cytometry and immunohistochemistry, we show that hematopoietic cells are present in the retina as early as P0, and include microglia, monocytes and MACs. Even before the formation of retinal blood vessels, hematopoietic cells localize to the inner retina where they eventually form networks that intimately associate with the developing vasculature. Loss of Vav1 lead to a reduction in the density of medium-sized vessels and an increased inflammatory response in retinal astrocytes. When pups were subjected to oxygen-induced retinopathy, hematopoietic cells maintained a close association with the vasculature and occasionally formed 'frameworks' for the generation of new vessels. Our study provides further evidence for the underappreciated role of hematopoietic cells in retinal vasculogenesis and the formation of a healthy retina.
MeSH term(s)	Animals ; Animals, Newborn ; Retina/metabolism ; Retinal Vessels/metabolism ; Oxygen/metabolism ; Microglia
Chemical Substances	Oxygen (S88TT14065)
Language	English
Publishing date	2022-10-13
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells11203207
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Article: Plasma microbiome in COVID-19 subjects: an indicator of gut barrier defects and dysbiosis.

Prasad, Ram / Patton, Michael John / Floyd, Jason L / Vieira, Cristiano Pedrozo / Fortmann, Seth / DuPont, Mariana / Harbour, Angie / Jeremy, Chen See / Wright, Justin / Lamendella, Regina / Stevens, Bruce R / Grant, Maria B

bioRxiv : the preprint server for biology

2021

Abstract: The gut is a well-established route of infection and target for viral damage by SARS-CoV-2. This is supported by the clinical observation that about half of COVID-19 patients exhibit gastrointestinal ( ...

Abstract	The gut is a well-established route of infection and target for viral damage by SARS-CoV-2. This is supported by the clinical observation that about half of COVID-19 patients exhibit gastrointestinal (
Language	English
Publishing date	2021-04-06
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.04.06.438634
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Article ; Online: Circulating SARS-CoV-2+ megakaryocytes are associated with severe viral infection in COVID-19.

Blood advances

2023 Volume 7, Issue 15, Page(s) 4200–4214

Abstract: Several independent lines of evidence suggest that megakaryocytes are dysfunctional in severe COVID-19. Herein, we characterized peripheral circulating megakaryocytes in a large cohort of inpatients with COVID-19 and correlated the subpopulation ... ...

Abstract	Several independent lines of evidence suggest that megakaryocytes are dysfunctional in severe COVID-19. Herein, we characterized peripheral circulating megakaryocytes in a large cohort of inpatients with COVID-19 and correlated the subpopulation frequencies with clinical outcomes. Using peripheral blood, we show that megakaryocytes are increased in the systemic circulation in COVID-19, and we identify and validate S100A8/A9 as a defining marker of megakaryocyte dysfunction. We further reveal a subpopulation of S100A8/A9+ megakaryocytes that contain severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) protein and RNA. Using flow cytometry of peripheral blood and in vitro studies on SARS-CoV-2-infected primary human megakaryocytes, we demonstrate that megakaryocytes can transfer viral antigens to emerging platelets. Mechanistically, we show that SARS-CoV-2-containing megakaryocytes are nuclear factor κB (NF-κB)-activated, via p65 and p52; express the NF-κB-mediated cytokines interleukin-6 (IL-6) and IL-1β; and display high surface expression of Toll-like receptor 2 (TLR2) and TLR4, canonical drivers of NF-κB. In a cohort of 218 inpatients with COVID-19, we correlate frequencies of megakaryocyte subpopulations with clinical outcomes and show that SARS-CoV-2-containing megakaryocytes are a strong risk factor for mortality and multiorgan injury, including respiratory failure, mechanical ventilation, acute kidney injury, thrombotic events, and intensive care unit admission. Furthermore, we show that SARS-CoV-2+ megakaryocytes are present in lung and brain autopsy tissues from deceased donors who had COVID-19. To our knowledge, this study offers the first evidence implicating SARS-CoV-2+ peripheral megakaryocytes in severe disease and suggests that circulating megakaryocytes warrant investigation in inflammatory disorders beyond COVID-19.
MeSH term(s)	Humans ; COVID-19 ; SARS-CoV-2 ; Megakaryocytes/metabolism ; NF-kappa B/metabolism ; Lung/metabolism
Chemical Substances	NF-kappa B
Language	English
Publishing date	2023-03-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2915908-8
ISSN	2473-9537 ; 2473-9529
ISSN (online)	2473-9537
ISSN	2473-9529
DOI	10.1182/bloodadvances.2022009022
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Article ; Online: Maintenance of Enteral ACE2 Prevents Diabetic Retinopathy in Type 1 Diabetes.

Prasad, Ram / Floyd, Jason L / Dupont, Mariana / Harbour, Angela / Adu-Agyeiwaah, Yvonne / Asare-Bediako, Bright / Chakraborty, Dibyendu / Kichler, Kara / Rohella, Aayush / Li Calzi, Sergio / Lammendella, Regina / Wright, Justin / Boulton, Michael E / Oudit, Gavin Y / Raizada, Mohan K / Stevens, Bruce R / Li, Qiuhong / Grant, Maria B

Circulation research

2022 Volume 132, Issue 1, Page(s) e1–e21

Abstract: Background: We examined components of systemic and intestinal renin-angiotensin system on gut barrier permeability, glucose homeostasis, systemic inflammation, and progression of diabetic retinopathy (DR) in human subjects and mice with type 1 diabetes ( ...

Abstract	Background: We examined components of systemic and intestinal renin-angiotensin system on gut barrier permeability, glucose homeostasis, systemic inflammation, and progression of diabetic retinopathy (DR) in human subjects and mice with type 1 diabetes (T1D). Methods: T1D individual with (n=18) and without (n=20) DR and controls (n=34) were examined for changes in gut-regulated components of the immune system, gut leakage markers (FABP2 [fatty acid binding protein 2] and peptidoglycan), and Ang II (angiotensin II); Results: T1D subjects exhibit elevations in gut-derived circulating immune cells (ILC1 cells) and higher gut leakage markers, which were positively correlated with plasma Ang II and DR severity. The LP-ACE2 prevention cohort and genetic overexpression of intestinal ACE2 preserved barrier integrity, reduced inflammatory response, improved hyperglycemia, and delayed development of DR. Improvements in glucose homeostasis were due to intestinal MasR activation, resulting in a GSK-3β (glycogen synthase kinase-3 beta)/c-Myc (cellular myelocytomatosis oncogene)-mediated decrease in intestinal glucose transporter expression. In the LP-ACE2 intervention cohort, gut barrier integrity was improved and DR reversed, but no improvement in hyperglycemia was observed. These data support that the beneficial effects of LP-ACE2 on DR are due to the action of ACE2, not improved glucose homeostasis. Conclusions: Dysregulated systemic and intestinal renin-angiotensin system was associated with worsening gut barrier permeability, gut-derived immune cell activation, systemic inflammation, and progression of DR in human subjects. In
MeSH term(s)	Animals ; Humans ; Mice ; Angiotensin-Converting Enzyme 2/metabolism ; Diabetes Mellitus, Type 1/complications ; Diabetes Mellitus, Type 1/metabolism ; Diabetic Retinopathy/prevention & control ; Glucose/metabolism ; Glycogen Synthase Kinase 3 beta/metabolism ; Hyperglycemia/complications ; Inflammation/metabolism ; Intestine, Small ; Peptide Fragments/metabolism ; Peptidyl-Dipeptidase A/genetics ; Renin-Angiotensin System/physiology
Chemical Substances	Angiotensin-Converting Enzyme 2 (EC 3.4.17.23) ; Glucose (IY9XDZ35W2) ; Glycogen Synthase Kinase 3 beta (EC 2.7.11.1) ; Peptide Fragments ; Peptidyl-Dipeptidase A (EC 3.4.15.1) ; ACE2 protein, human (EC 3.4.17.23) ; Ace2 protein, mouse (EC 3.4.17.23)
Language	English
Publishing date	2022-11-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80100-8
ISSN	1524-4571 ; 0009-7330 ; 0931-6876
ISSN (online)	1524-4571
ISSN	0009-7330 ; 0931-6876
DOI	10.1161/CIRCRESAHA.122.322003
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Article ; Online: Plasma microbiome in COVID-19 subjects: an indicator of gut barrier defects and dysbiosis

Prasad, Ram / Patton, Michael John / Floyd, Jason L / Vieira, Cristiano P / Fortmann, Seth D. / DuPont, Mariana / Harbour, Angie / Chen See, Jeremy R / Wright, Justin / Lamendella, Regina / Stevens, Bruce R. / Grant, Maria B.

bioRxiv

Abstract	The gut is a well-established route of infection and target for viral damage by SARS-CoV-2. This is supported by the clinical observation that about half of COVID-19 patients exhibit gastrointestinal (GI) symptoms. We asked whether the analysis of plasma could provide insight into gut barrier dysfunction in patients with COVID-19 infection. Plasma samples of COVID-19 patients (n=30) and healthy control (n=16) were collected during hospitalization. Plasma microbiome was analyzed using 16S rRNA sequencing, metatranscriptomic analysis, and gut permeability markers including FABP-2, PGN and LPS in both patient cohorts. Almost 65% (9 out 14) COVID-19 patients showed abnormal presence of gut microbes in their bloodstream. Plasma samples contained predominately Proteobacteria, Firmicutes, and Actinobacteria. The abundance of gram-negative bacteria (Acinetobacter, Nitrospirillum, Cupriavidus, Pseudomonas, Aquabacterium, Burkholderia, Caballeronia, Parabhurkholderia, Bravibacterium, and Sphingomonas) was higher than the gram-positive bacteria (Staphylococcus and Lactobacillus) in COVID-19 subjects. The levels of plasma gut permeability markers FABP2 (1282 [plusmn]199.6 vs 838.1[plusmn]91.33; p=0.0757), PGN (34.64[plusmn]3.178 vs 17.53[plusmn]2.12; p<0.0001), and LPS (405.5[plusmn]48.37 vs 249.6[plusmn]17.06; p=0.0049) were higher in COVID-19 patients compared to healthy subjects. These findings support that the intestine may represent a source for bacteremia and may contribute to worsening COVID-19 outcomes. Therapies targeting the gut and prevention of gut barrier defects may represent a strategy to improve outcomes in COVID-19 patients.
Keywords	covid19
Language	English
Publishing date	2021-04-06
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2021.04.06.438634
Database	COVID19

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Article ; Online: Specific mesoderm subset derived from human pluripotent stem cells ameliorates microvascular pathology in type 2 diabetic mice.

Gil, Chang-Hyun / Chakraborty, Dibyendu / Vieira, Cristiano P / Prasain, Nutan / Li Calzi, Sergio / Fortmann, Seth D / Hu, Ping / Banno, Kimihiko / Jamal, Mohamed / Huang, Chao / Sielski, Micheli S / Lin, Yang / Huang, Xinxin / Dupont, Mariana D / Floyd, Jason L / Prasad, Ram / Longhini, Ana Leda F / McGill, Trevor J / Chung, Hyung-Min /

Murphy, Michael P / Kotton, Darrell N / Boulton, Michael E / Yoder, Mervin C / Grant, Maria B

Science advances

2022 Volume 8, Issue 9, Page(s) eabm5559

Abstract: Human induced pluripotent stem cells (hiPSCs) were differentiated into a specific mesoderm subset characterized by ... ...

Abstract	Human induced pluripotent stem cells (hiPSCs) were differentiated into a specific mesoderm subset characterized by KDR
Language	English
Publishing date	2022-03-04
Publishing country	United States
Document type	Journal Article
ZDB-ID	2810933-8
ISSN	2375-2548 ; 2375-2548
ISSN (online)	2375-2548
ISSN	2375-2548
DOI	10.1126/sciadv.abm5559
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Article ; Online: Selective LXR agonist DMHCA corrects retinal and bone marrow dysfunction in type 2 diabetes.

Vieira, Cristiano P / Fortmann, Seth D / Hossain, Masroor / Longhini, Ana Leda / Hammer, Sandra S / Asare-Bediako, Bright / Crossman, David K / Sielski, Micheli S / Adu-Agyeiwaah, Yvonne / Dupont, Mariana / Floyd, Jason L / Li Calzi, Sergio / Lydic, Todd / Welner, Robert S / Blanchard, Gary J / Busik, Julia V / Grant, Maria B

JCI insight

2020 Volume 5, Issue 13

Abstract: In diabetic dyslipidemia, cholesterol accumulates in the plasma membrane, decreasing fluidity and thereby suppressing the ability of cells to transduce ligand-activated signaling pathways. Liver X receptors (LXRs) make up the main cellular mechanism by ... ...

Abstract	In diabetic dyslipidemia, cholesterol accumulates in the plasma membrane, decreasing fluidity and thereby suppressing the ability of cells to transduce ligand-activated signaling pathways. Liver X receptors (LXRs) make up the main cellular mechanism by which intracellular cholesterol is regulated and play important roles in inflammation and disease pathogenesis. N, N-dimethyl-3β-hydroxy-cholenamide (DMHCA), a selective LXR agonist, specifically activates the cholesterol efflux arm of the LXR pathway without stimulating triglyceride synthesis. In this study, we use a multisystem approach to understand the effects and molecular mechanisms of DMHCA treatment in type 2 diabetic (db/db) mice and human circulating angiogenic cells (CACs), which are hematopoietic progenitor cells with vascular reparative capacity. We found that DMHCA is sufficient to correct retinal and BM dysfunction in diabetes, thereby restoring retinal structure, function, and cholesterol homeostasis; rejuvenating membrane fluidity in CACs; hampering systemic inflammation; and correcting BM pathology. Using single-cell RNA sequencing on lineage-sca1+c-Kit+ (LSK) hematopoietic stem cells (HSCs) from untreated and DMHCA-treated diabetic mice, we provide potentially novel insights into hematopoiesis and reveal DMHCA's mechanism of action in correcting diabetic HSCs by reducing myeloidosis and increasing CACs and erythrocyte progenitors. Taken together, these findings demonstrate the beneficial effects of DMHCA treatment on diabetes-induced retinal and BM pathology.
MeSH term(s)	Animals ; Bone Marrow/drug effects ; Bone Marrow/pathology ; Bone Marrow Cells/cytology ; Bone Marrow Cells/drug effects ; Cholesterol/metabolism ; Cholic Acids/pharmacology ; Diabetes Mellitus, Experimental/drug therapy ; Diabetes Mellitus, Experimental/metabolism ; Diabetes Mellitus, Type 2/drug therapy ; Diabetes Mellitus, Type 2/metabolism ; Humans ; Inflammation/metabolism ; Lipid Metabolism/drug effects ; Lipogenesis/drug effects ; Lipogenesis/physiology ; Liver X Receptors/metabolism ; Mice ; Retina/drug effects ; Retina/pathology
Chemical Substances	Cholic Acids ; Liver X Receptors ; N,N-dimethyl-3-hydroxy-5-cholenamide ; Cholesterol (97C5T2UQ7J)
Language	English
Publishing date	2020-07-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.137230
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