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Article ; Online: Isolation and Characterization of Extracellular Vesicles Through Orthogonal Approaches for the Development of Intraocular EV Therapy.

Leung, Justin / Pollalis, Dimitrios / Nair, Gopa K G / Bailey, Jeffrey K / Pennington, Britney O / Khan, Amir I / Kelly, Kaitlin R / Yeh, Ashley K / Sundaram, Kartik S / Clegg, Dennis O / Peng, Chen-Ching / Xu, Liya / Lee, Sun Young

Investigative ophthalmology & visual science

2024 Volume 65, Issue 3, Page(s) 6

Abstract: Purpose: Isolating extracellular vesicles (EVs) with high yield, replicable purity, and characterization remains a bottleneck in the development of EV therapeutics. To address these challenges, the current study aims to establish the necessary framework ...

Abstract	Purpose: Isolating extracellular vesicles (EVs) with high yield, replicable purity, and characterization remains a bottleneck in the development of EV therapeutics. To address these challenges, the current study aims to establish the necessary framework for preclinical and clinical studies in the development of stem cell-derived intraocular EV therapeutics. Methods: Small EVs (sEVs) were separated from the conditioned cell culture medium (CCM) of the human embryogenic stem cell-derived fully polarized retinal pigment epithelium (hESC-RPE-sEV) by a commercially available microfluidic tangential flow filtration (TFF) device ExoDisc (ED) or differential ultracentrifugation (dUC). The scaling and concentration capabilities and purity of recovered sEVs were assessed. Size, number, and surface markers of sEVs were determined by orthogonal approaches using multiple devices. Results: ED yielded higher numbers of sEVs, ranging from three to eight times higher depending on the measurement device, compared to dUC using the same 5 mL of CCM input. Within the same setting, the purity of ED-recovered hESC-RPE-sEVs was higher than that for dUC-recovered sEVs. ED yielded a higher concentration of particles, which is strongly correlated with the input volume, up to 10 mL (r = 0.98, P = 0.016). Meanwhile, comprehensive characterization profiles of EV surface markers between ED- and dUC-recovered hESC-RPE-sEVs were compatible. Conclusions: Our study supports TFF as a valuable strategy for separating sEVs for the development of intraocular EV therapeutics. However, there is a growing need for diverse devices to optimize TFF for use in EV preparation. Using orthogonal approaches in EV characterization remains ideal for reliably characterizing heterogeneous EV.
MeSH term(s)	Humans ; Culture Media, Conditioned ; Extracellular Vesicles ; Filtration ; Human Embryonic Stem Cells ; Retinal Pigment Epithelium
Chemical Substances	Culture Media, Conditioned
Language	English
Publishing date	2024-03-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.65.3.6
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Article ; Online: Pluripotent Stem Cell-Based Therapies in Combination with Substrate for the Treatment of Age-Related Macular Degeneration.

Pennington, Britney O / Clegg, Dennis O

Journal of ocular pharmacology and therapeutics : the official journal of the Association for Ocular Pharmacology and Therapeutics

2016 Volume 32, Issue 5, Page(s) 261–271

Abstract: Age-related macular degeneration (AMD) is the leading cause of blindness in the western world, which severely decreases the quality of life in the patients and places an economic burden on their families and society. The disease is caused by the ... ...

Abstract	Age-related macular degeneration (AMD) is the leading cause of blindness in the western world, which severely decreases the quality of life in the patients and places an economic burden on their families and society. The disease is caused by the dysfunction of a specialized cell layer in the back of the eye called the retinal pigmented epithelium (RPE). Pluripotent stem cells can provide an unlimited source of RPE, and laboratories around the world are investigating their potential as therapies for AMD. To ensure the precise delivery of functional RPE to the diseased site, some groups are developing a therapy composed of mature RPE monolayers on a supportive scaffold for transplantation as an alternative to injecting a single-cell suspension. This review summarizes methods of generating RPE from pluripotent stem cells, compares biodegradable and biostable materials as scaffolds, and describes the specific combination of human embryonic stem cell-derived RPE on Parylene-C membranes, which is scheduled to begin clinical trials in the United Sates in 2016. Stem cell-derived RPE monolayers on scaffolds hold great promise for the treatment of AMD and other retinal diseases.
MeSH term(s)	Age Factors ; Animals ; Humans ; Macular Degeneration/pathology ; Macular Degeneration/therapy ; Pluripotent Stem Cells/cytology ; Pluripotent Stem Cells/transplantation ; Retinal Pigment Epithelium/cytology ; Retinal Pigment Epithelium/metabolism ; Stem Cell Transplantation ; Tissue Scaffolds
Language	English
Publishing date	2016-06
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	1237021-6
ISSN	1557-7732 ; 1080-7683
ISSN (online)	1557-7732
ISSN	1080-7683
DOI	10.1089/jop.2015.0153
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Article: Rescuing Photoreceptors in RPE Dysfunction-Driven Retinal Degeneration: The Role of Small Extracellular Vesicles Secreted from Retinal Pigment Epithelium.

Pollalis, Dimitrios / Georgescu, Constantin / Wren, Jonathan D / Tombulyan, Grigor / Leung, Justin M / Lo, Pein-An / Bloemhof, Clarisa Marie / Lee, Ryang Hwa / Bae, EunHye / Bailey, Jeffrey K / Pennington, Britney O / Khan, Amir I / Kelly, Kaitlin R / Yeh, Ashley K / Sundaram, Kartik S / Humayun, Mark / Louie, Stain / Clegg, Dennis O / Lee, Sun Young

bioRxiv : the preprint server for biology

2024

Abstract: Dysfunction of the retinal pigment epithelium (RPE) is a common shared pathology in major degenerative retinal diseases despite variations in the primary etiologies of each disease. Due to their demanding and indispensable functional roles throughout the ...

Abstract	Dysfunction of the retinal pigment epithelium (RPE) is a common shared pathology in major degenerative retinal diseases despite variations in the primary etiologies of each disease. Due to their demanding and indispensable functional roles throughout the lifetime, RPE cells are vulnerable to genetic predisposition, external stress, and aging processes. Building upon recent advancements in stem cell technology for differentiating healthy RPE cells and recognizing the significant roles of small extracellular vesicles (sEV) in cellular paracrine and autocrine actions, we investigated the hypothesis that the RPE-secreted sEV alone can restore essential RPE functions and rescue photoreceptors in RPE dysfunction-driven retinal degeneration. Our findings support the rationale for developing intravitreal treatment of sEV. We demonstrate that intravitreally delivered sEV effectively penetrate the full thickness of the retina. Xenogenic intraocular administration of human-derived EVs did not induce acute immune reactions in rodents. sEV derived from human embryonic stem cell (hESC)-derived fully differentiated RPE cells, but not sEV-depleted conditioned cell culture media (CCM minus sEV), rescued photoreceptors and their function in a Royal College of Surgeons (RCS) rat model. This model is characterized by photoreceptor death and retinal degeneration resulting from a mutation in the
Language	English
Publishing date	2024-04-13
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.04.09.588773
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Article: Microcarrier-Based Culture of Human Pluripotent Stem-Cell-Derived Retinal Pigmented Epithelium.

Faynus, Mohamed A / Bailey, Jeffrey K / Pennington, Britney O / Katsura, Mika / Proctor, Duncan A / Yeh, Ashley K / Menon, Sneha / Choi, Dylan G / Lebkowski, Jane S / Johnson, Lincoln V / Clegg, Dennis O

Bioengineering (Basel, Switzerland)

2022 Volume 9, Issue 7

Abstract: Dry age-related macular degeneration (AMD) is estimated to impact nearly 300 million individuals globally by 2040. While no treatment options are currently available, multiple clinical trials investigating retinal pigmented epithelial cells derived from ... ...

Abstract	Dry age-related macular degeneration (AMD) is estimated to impact nearly 300 million individuals globally by 2040. While no treatment options are currently available, multiple clinical trials investigating retinal pigmented epithelial cells derived from human pluripotent stem cells (hPSC-RPE) as a cellular replacement therapeutic are currently underway. It has been estimated that a production capacity of >109 RPE cells annually would be required to treat the afflicted population, but current manufacturing protocols are limited, being labor-intensive and time-consuming. Microcarrier technology has enabled high-density propagation of many adherent mammalian cell types via monolayer culture on surfaces of uM-diameter matrix spheres; however, few studies have explored microcarrier-based culture of RPE cells. Here, we provide an approach to the growth, maturation, and differentiation of hPSC-RPE cells on Cytodex 1 (C1) and Cytodex 3 (C3) microcarriers. We demonstrate that hPSC-RPE cells adhere to microcarriers coated with Matrigel, vitronectin or collagen, and mature in vitro to exhibit characteristic epithelial cell morphology and pigmentation. Microcarrier-grown hPSC-RPE cells (mcRPE) are viable; metabolically active; express RPE signature genes including BEST1, RPE65, TYRP1, and PMEL17; secrete the trophic factors PEDF and VEGF; and demonstrate phagocytosis of photoreceptor outer segments. Furthermore, we show that undifferentiated hESCs also adhere to Matrigel-coated microcarriers and are amenable to directed RPE differentiation. The capacity to support hPSC-RPE cell cultures using microcarriers enables efficient large-scale production of therapeutic RPE cells sufficient to meet the treatment demands of a large AMD patient population.
Language	English
Publishing date	2022-07-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2746191-9
ISSN	2306-5354
ISSN	2306-5354
DOI	10.3390/bioengineering9070297
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Article ; Online: Interactive Hangman teaches amino acid structures and abbreviations.

Pennington, Britney O / Sears, Duane / Clegg, Dennis O

Biochemistry and molecular biology education : a bimonthly publication of the International Union of Biochemistry and Molecular Biology

2014 Volume 42, Issue 6, Page(s) 495–500

Abstract: We developed an interactive exercise to teach students how to draw the structures of the 20 standard amino acids and to identify the one-letter abbreviations by modifying the familiar game of "Hangman." Amino acid structures were used to represent single ...

Abstract	We developed an interactive exercise to teach students how to draw the structures of the 20 standard amino acids and to identify the one-letter abbreviations by modifying the familiar game of "Hangman." Amino acid structures were used to represent single letters throughout the game. To provide additional practice in identifying structures, hints to the answers were written in "amino acid sentences" for the students to translate. Students were required to draw the structure of the corresponding letter they wished to guess on a whiteboard. Each student received a reference sheet of the structures and abbreviations, but was required to draw from memory when guessing a letter. Preassessments and postassessments revealed a drastic improvement in the students' ability to recognize and draw structures from memory. This activity provides a fun, educational game to play in biochemistry discussion sections or during long incubations in biochemistry laboratories.
MeSH term(s)	Amino Acids/chemistry ; Biochemistry/education ; Educational Measurement/methods ; Humans ; Molecular Structure ; Students ; Teaching ; Terminology as Topic
Chemical Substances	Amino Acids
Language	English
Publishing date	2014-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1539-3429
ISSN (online)	1539-3429
DOI	10.1002/bmb.20826
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Article: Defined culture of human embryonic stem cells and xeno-free derivation of retinal pigmented epithelial cells on a novel, synthetic substrate.

Pennington, Britney O / Clegg, Dennis O / Melkoumian, Zara K / Hikita, Sherry T

Stem cells translational medicine

2015 Volume 4, Issue 2, Page(s) 165–177

Abstract: Age-related macular degeneration (AMD), a leading cause of blindness, is characterized by the death of the retinal pigmented epithelium (RPE), which is a monolayer posterior to the retina that supports the photoreceptors. Human embryonic stem cells ( ... ...

Abstract	Age-related macular degeneration (AMD), a leading cause of blindness, is characterized by the death of the retinal pigmented epithelium (RPE), which is a monolayer posterior to the retina that supports the photoreceptors. Human embryonic stem cells (hESCs) can generate an unlimited source of RPE for cellular therapies, and clinical trials have been initiated. However, protocols for RPE derivation using defined conditions free of nonhuman derivatives (xeno-free) are preferred for clinical translation. This avoids exposing AMD patients to animal-derived products, which could incite an immune response. In this study, we investigated the maintenance of hESCs and their differentiation into RPE using Synthemax II-SC, which is a novel, synthetic animal-derived component-free, RGD peptide-containing copolymer compliant with good manufacturing practices designed for xeno-free stem cell culture. Cells on Synthemax II-SC were compared with cultures grown with xenogeneic and xeno-free control substrates. This report demonstrates that Synthemax II-SC supports long-term culture of H9 and H14 hESC lines and permits efficient differentiation of hESCs into functional RPE. Expression of RPE-specific markers was assessed by flow cytometry, quantitative polymerase chain reaction, and immunocytochemistry, and RPE function was determined by phagocytosis of rod outer segments and secretion of pigment epithelium-derived factor. Both hESCs and hESC-RPE maintained normal karyotypes after long-term culture on Synthemax II-SC. Furthermore, RPE generated on Synthemax II-SC are functional when seeded onto parylene-C scaffolds designed for clinical use. These experiments suggest that Synthemax II-SC is a suitable, defined substrate for hESC culture and the xeno-free derivation of RPE for cellular therapies.
MeSH term(s)	Cell Culture Techniques/methods ; Cell Differentiation ; Cell Line ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/metabolism ; Epithelial Cells/cytology ; Epithelial Cells/metabolism ; Humans ; Macular Degeneration/metabolism ; Macular Degeneration/therapy ; Retinal Pigment Epithelium/cytology ; Retinal Pigment Epithelium/metabolism
Language	English
Publishing date	2015-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2642270-0
ISSN	2157-6580 ; 2157-6564
ISSN (online)	2157-6580
ISSN	2157-6564
DOI	10.5966/sctm.2014-0179
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Article ; Online: Long-term Follow-up of a Phase 1/2a Clinical Trial of a Stem Cell-Derived Bioengineered Retinal Pigment Epithelium Implant for Geographic Atrophy.

Humayun, Mark S / Clegg, Dennis O / Dayan, Margot S / Kashani, Amir H / Rahhal, Firas M / Avery, Robert L / Salehi-Had, Hani / Chen, Sanford / Chan, Clement / Palejwala, Neal / Ingram, April / Mitra, Debbie / Pennington, Britney O / Hinman, Cassidy / Faynus, Mohamed A / Bailey, Jeffrey K / Johnson, Lincoln V / Lebkowski, Jane S

Ophthalmology

2023

Abstract: Purpose: To report long-term results from a phase 1/2a clinical trial assessment of a scaffold-based human embryonic stem cell-derived retinal pigmented epithelium (RPE) implant in patients with advanced geographic atrophy (GA).: Design: A single-arm, ...

Abstract	Purpose: To report long-term results from a phase 1/2a clinical trial assessment of a scaffold-based human embryonic stem cell-derived retinal pigmented epithelium (RPE) implant in patients with advanced geographic atrophy (GA). Design: A single-arm, open-label phase 1/2a clinical trial approved by the United States Food and Drug Administration. Participants: Patients were 69-85 years of age at the time of enrollment and were legally blind in the treated eye (best-corrected visual acuity [BCVA], ≤ 20/200) as a result of GA involving the fovea. Methods: The clinical trial enrolled 16 patients, 15 of whom underwent implantation successfully. The implant was administered to the worse-seeing eye with the use of a custom subretinal insertion device. The companion nonimplanted eye served as the control. The primary endpoint was at 1 year; thereafter, patients were followed up at least yearly. Main outcome measures: Safety was the primary endpoint of the study. The occurrence and frequency of adverse events (AEs) were determined by scheduled eye examinations, including measurement of BCVA and intraocular pressure and multimodal imaging. Serum antibody titers were collected to monitor systemic humoral immune responses to the implanted cells. Results: At a median follow-up of 3 years, fundus photography revealed no migration of the implant. No unanticipated, severe, implant-related AEs occurred, and the most common anticipated severe AE (severe retinal hemorrhage) was eliminated in the second cohort (9 patients) through improved intraoperative hemostasis. Nonsevere, transient retinal hemorrhages were noted either during or after surgery in all patients as anticipated for a subretinal surgical procedure. Throughout the median 3-year follow-up, results show that implanted eyes were more likely to improve by > 5 letters of BCVA and were less likely to worsen by > 5 letters compared with nonimplanted eyes. Conclusions: This report details the long-term follow-up of patients with GA to receive a scaffold-based stem cell-derived bioengineered RPE implant. Results show that the implant, at a median 3-year follow-up, is safe and well tolerated in patients with advanced dry age-related macular degeneration. The safety profile, along with the early indication of efficacy, warrants further clinical evaluation of this novel approach for the treatment of GA. Financial disclosure(s): Proprietary or commercial disclosure may be found in the Footnotes and Disclosures at the end of this article.
Language	English
Publishing date	2023-12-30
Publishing country	United States
Document type	Journal Article
ZDB-ID	392083-5
ISSN	1549-4713 ; 0161-6420
ISSN (online)	1549-4713
ISSN	0161-6420
DOI	10.1016/j.ophtha.2023.12.028
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Ul II Zs.83: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 2021: Bestellungen von Artikeln über das Online-Bestellformular ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Xeno-free cryopreservation of adherent retinal pigmented epithelium yields viable and functional cells in vitro and in vivo.

Pennington, Britney O / Bailey, Jeffrey K / Faynus, Mohamed A / Hinman, Cassidy / Hee, Mitchell N / Ritts, Rory / Nadar, Vignesh / Zhu, Danhong / Mitra, Debbie / Martinez-Camarillo, Juan Carlos / Lin, Tai-Chi / Thomas, Biju B / Hinton, David R / Humayun, Mark S / Lebkowski, Jane / Johnson, Lincoln V / Clegg, Dennis O

Scientific reports

2021 Volume 11, Issue 1, Page(s) 6286

Abstract: Age-related macular degeneration (AMD) is the primary cause of blindness in adults over 60 years of age, and clinical trials are currently assessing the therapeutic potential of retinal pigmented epithelial (RPE) cell monolayers on implantable scaffolds ... ...

Abstract	Age-related macular degeneration (AMD) is the primary cause of blindness in adults over 60 years of age, and clinical trials are currently assessing the therapeutic potential of retinal pigmented epithelial (RPE) cell monolayers on implantable scaffolds to treat this disease. However, challenges related to the culture, long-term storage, and long-distance transport of such implants currently limit the widespread use of adherent RPE cells as therapeutics. Here we report a xeno-free protocol to cryopreserve a confluent monolayer of clinical-grade, human embryonic stem cell-derived RPE cells on a parylene scaffold (REPS) that yields viable, polarized, and functional RPE cells post-thaw. Thawed cells exhibit ≥ 95% viability, have morphology, pigmentation, and gene expression characteristic of mature RPE cells, and secrete the neuroprotective protein, pigment epithelium-derived factor (PEDF). Stability under liquid nitrogen (LN
MeSH term(s)	Animals ; Cell Differentiation ; Cell Line ; Cell Survival ; Cryopreservation/methods ; Disease Models, Animal ; Epithelial Cells/cytology ; Epithelial Cells/metabolism ; Epithelial Cells/transplantation ; Eye Proteins/metabolism ; Human Embryonic Stem Cells/cytology ; Humans ; Macular Degeneration/therapy ; Nerve Growth Factors/metabolism ; Polymers ; Rats ; Rats, Nude ; Regenerative Medicine/methods ; Retinal Pigment Epithelium/cytology ; Retinal Pigment Epithelium/metabolism ; Retinal Pigment Epithelium/transplantation ; Serpins/metabolism ; Specimen Handling/methods ; Stem Cell Transplantation/methods ; Tissue Scaffolds ; Treatment Outcome ; Xylenes
Chemical Substances	Eye Proteins ; Nerve Growth Factors ; Polymers ; Serpins ; Xylenes ; pigment epithelium-derived factor ; parylene (25722-33-2)
Language	English
Publishing date	2021-03-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-85631-6
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Article ; Online: Survival of an HLA-mismatched, bioengineered RPE implant in dry age-related macular degeneration.

Stem cell reports

2022 Volume 17, Issue 3, Page(s) 448–458

Abstract: Cell-based therapies face challenges, including poor cell survival, immune rejection, and integration into pathologic tissue. We conducted an open-label phase 1/2a clinical trial to assess the safety and preliminary efficacy of a subretinal implant ... ...

Abstract	Cell-based therapies face challenges, including poor cell survival, immune rejection, and integration into pathologic tissue. We conducted an open-label phase 1/2a clinical trial to assess the safety and preliminary efficacy of a subretinal implant consisting of a polarized monolayer of allogeneic human embryonic stem cell-derived retinal pigmented epithelium (RPE) cells in subjects with geographic atrophy (GA) secondary to dry age-related macular degeneration. Postmortem histology from one subject with very advanced disease shows the presence of donor RPE cells 2 years after implantation by immunoreactivity for RPE65 and donor-specific human leukocyte antigen (HLA) class I molecules. Markers of RPE cell polarity and phagocytosis suggest donor RPE function. Further histologic examination demonstrated CD34
MeSH term(s)	Geographic Atrophy/therapy ; Human Embryonic Stem Cells/pathology ; Humans ; Macular Degeneration/pathology ; Macular Degeneration/therapy ; Prostheses and Implants/adverse effects ; Retinal Pigment Epithelium/pathology
Language	English
Publishing date	2022-02-03
Publishing country	United States
Document type	Clinical Trial, Phase I ; Clinical Trial, Phase II ; Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2022.01.001
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Article: Multiple R-Like Genes Are Negatively Regulated by BON1 and BON3 in Arabidopsis

Li, Yongqing / Pennington, Britney O / Hua, Jian

Molecular plant-microbe interactions : MPMI. 2009 July, v. 22, no. 7

2009

Abstract: The Arabidopsis thaliana genome contains more than 200 rapidly evolved resistance (R)-like genes coding for nucleotide binding leucine-rich repeat (NB-LRR) and their related proteins. A dozen of them are shown to play key roles in plant responses to ... ...

Abstract	The Arabidopsis thaliana genome contains more than 200 rapidly evolved resistance (R)-like genes coding for nucleotide binding leucine-rich repeat (NB-LRR) and their related proteins. A dozen of them are shown to play key roles in plant responses to biotic attacks, and they need to be repressed in the absence of biotic stresses to prevent activation of defense responses that are usually detrimental to plant growth and development. Here, we show that the Arabidopsis BON1 and BON3 genes, two members of the evolutionarily conserved copine, are negative regulators of several R-like genes. At least four such genes of the Toll-interleukin-1 receptor-like (TIR)-NB-LRR or TIR-NB type were identified through their activities in triggering cell death in the absence of the BON1 and BON3 function and their natural variations between two Arabidopsis accessions, Col-0 and Ws-2. These so-named lesion cell death (LCD) genes contribute quantitatively to the phenotypes of enhanced defense response and cell death in the bon1bon3 mutant. Further, their activation in the bon1bon3 mutants appears to be through different regulatory modes, and BON1 and BON3 may repress the transcript accumulation or protein activities of these R-like genes.
Keywords	Arabidopsis thaliana ; genome ; genetic resistance ; DNA-binding domains ; DNA-binding proteins ; plant proteins ; plant growth ; gene expression regulation ; regulatory sequences ; apoptosis ; phenotype ; messenger RNA ; transcription (genetics)
Language	English
Dates of publication	2009-07
Size	p. 840-848.
Document type	Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-22-7-0840
Database	NAL-Catalogue (AGRICOLA)

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