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Article ; Online: Complement factor H in AMD: Bridging genetic associations and pathobiology.

Toomey, Christopher B / Johnson, Lincoln V / Bowes Rickman, Catherine

2017 Volume 62, Page(s) 38–57

Abstract: Age-Related Macular Degeneration (AMD) is a complex multifactorial disease characterized in its early stages by lipoprotein accumulations in Bruch's Membrane (BrM), seen on fundoscopic exam as drusen, and in its late forms by neovascularization ("wet") ... ...

Abstract	Age-Related Macular Degeneration (AMD) is a complex multifactorial disease characterized in its early stages by lipoprotein accumulations in Bruch's Membrane (BrM), seen on fundoscopic exam as drusen, and in its late forms by neovascularization ("wet") or geographic atrophy of the Retinal Pigmented Epithelial (RPE) cell layer ("dry"). Genetic studies have strongly supported a relationship between the alternative complement cascade, in particular the common H402 variant in Complement Factor H (CFH) and development of AMD. However, the functional significance of the CFH Y402H polymorphism remains elusive. In this article, we critically review the literature surrounding the functional significance of this polymorphism. Furthermore, based on our group's studies we propose a model in which CFH H402 affects CFH binding to heparan sulfate proteoglycans leading to accelerated lipoprotein accumulation in BrM and drusen progression. We also review the literature on the role of other complement components in AMD pathobiologies, including C3a, C5a and the membrane attack complex (MAC), and on transgenic mouse models developed to interrogate in vivo the effects of the CFH Y402H polymorphism.
MeSH term(s)	Complement Factor H/genetics ; Complement Factor H/physiology ; Complement System Proteins/physiology ; Genetic Association Studies ; Humans ; Macular Degeneration/genetics ; Macular Degeneration/pathology ; Polymorphism, Single Nucleotide ; Retinal Drusen/metabolism ; Retinal Drusen/pathology
Chemical Substances	CFH protein, human ; Complement Factor H (80295-65-4) ; Complement System Proteins (9007-36-7)
Language	English
Publishing date	2017-09-18
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1182683-6
ISSN	1873-1635 ; 1350-9462
ISSN (online)	1873-1635
ISSN	1350-9462
DOI	10.1016/j.preteyeres.2017.09.001
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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: Cellular models and therapies for age-related macular degeneration.

Forest, David L / Johnson, Lincoln V / Clegg, Dennis O

Disease models & mechanisms

2015 Volume 8, Issue 5, Page(s) 421–427

Abstract: Age-related macular degeneration (AMD) is a complex neurodegenerative visual disorder that causes profound physical and psychosocial effects. Visual impairment in AMD is caused by the loss of retinal pigmented epithelium (RPE) cells and the light- ... ...

Abstract	Age-related macular degeneration (AMD) is a complex neurodegenerative visual disorder that causes profound physical and psychosocial effects. Visual impairment in AMD is caused by the loss of retinal pigmented epithelium (RPE) cells and the light-sensitive photoreceptor cells that they support. There is currently no effective treatment for the most common form of this disease (dry AMD). A new approach to treating AMD involves the transplantation of RPE cells derived from either human embryonic or induced pluripotent stem cells. Multiple clinical trials are being initiated using a variety of cell therapies. Although many animal models are available for AMD research, most do not recapitulate all aspects of the disease, hampering progress. However, the use of cultured RPE cells in AMD research is well established and, indeed, some of the more recently described RPE-based models show promise for investigating the molecular mechanisms of AMD and for screening drug candidates. Here, we discuss innovative cell-culture models of AMD and emerging stem-cell-based therapies for the treatment of this vision-robbing disease.
MeSH term(s)	Animals ; Humans ; Macular Degeneration/drug therapy ; Macular Degeneration/pathology ; Macular Degeneration/therapy ; Models, Biological ; Stem Cell Transplantation
Language	English
Publishing date	2015-05
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ISSN	1754-8411
ISSN (online)	1754-8411
DOI	10.1242/dmm.017236
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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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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 ; Online: Age-related macular degeneration and the extracellular matrix.

Johnson, Lincoln V / Anderson, Don H

The New England journal of medicine

2004 Volume 351, Issue 4, Page(s) 320–322

MeSH term(s)	Bruch Membrane/metabolism ; Bruch Membrane/pathology ; Calcium-Binding Proteins/genetics ; Calcium-Binding Proteins/metabolism ; Extracellular Matrix/metabolism ; Extracellular Matrix Proteins/genetics ; Extracellular Matrix Proteins/metabolism ; Humans ; Macular Degeneration/genetics ; Macular Degeneration/metabolism ; Macular Degeneration/pathology ; Mutation ; Pigment Epithelium of Eye/pathology ; Recombinant Proteins/genetics ; Recombinant Proteins/metabolism ; Retinal Drusen
Chemical Substances	Calcium-Binding Proteins ; Extracellular Matrix Proteins ; FBLN5 protein, human ; Recombinant Proteins ; fibulin
Language	English
Publishing date	2004-07-22
Publishing country	United States
Document type	Comment ; Journal Article
ZDB-ID	207154-x
ISSN	1533-4406 ; 0028-4793
ISSN (online)	1533-4406
ISSN	0028-4793
DOI	10.1056/NEJMp048131
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Article ; Online: Accumulation of extracellular RGR-d in Bruch's membrane and close association with drusen at intercapillary regions.

Kochounian, Harold / Johnson, Lincoln V / Fong, Henry K W

Experimental eye research

2009 Volume 88, Issue 6, Page(s) 1129–1136

Abstract: Human retinal pigment epithelial (RPE) cells synthesize an extraneous splice isoform of retinal G protein-coupled receptor (RGR). In this study, we analyzed the exon-skipping variant of RGR (RGR-d) that is found in extracellular deposits. RPE-choroid ... ...

Abstract	Human retinal pigment epithelial (RPE) cells synthesize an extraneous splice isoform of retinal G protein-coupled receptor (RGR). In this study, we analyzed the exon-skipping variant of RGR (RGR-d) that is found in extracellular deposits. RPE-choroid tissue sections were prepared from postmortem human eyes from donors of various ages. RGR-d was analyzed in drusen and Bruch's membrane by immunohistochemical localization. Extracellular RGR-d is present in most drusen, including hard, soft, confluent and early-stage. Initial drusen formation is known to be preferentially associated with the intercapillary regions of Bruch's membrane. We corroborated this significant association of drusen, including early-stage drusen, with the intercapillary regions. The distribution of extracellular RGR-d in Bruch's membrane differs in old and young donors. In older persons, nodes of concentrated RGR-d accumulate at intercapillary loci, predominantly at the lateral edges of the capillaries of the choriocapillaris. RGR-d loci at the lateral capillary wall appear numerous in old, but not young, donors. Intensely immunostained RGR-d loci can be found at the base of early-stage drusen mounds in the older donors and may precede the formation of these drusen.
MeSH term(s)	Adolescent ; Aged ; Aged, 80 and over ; Aging/metabolism ; Bruch Membrane/metabolism ; Extracellular Space/metabolism ; Eye Proteins/genetics ; Eye Proteins/metabolism ; Humans ; Protein Isoforms/genetics ; Protein Isoforms/metabolism ; Receptors, G-Protein-Coupled/genetics ; Receptors, G-Protein-Coupled/metabolism ; Retinal Drusen/metabolism ; Retinal Pigment Epithelium/metabolism ; Young Adult
Chemical Substances	Eye Proteins ; G protein-coupled receptor RGR ; Protein Isoforms ; Receptors, G-Protein-Coupled
Language	English
Publishing date	2009-02-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80122-7
ISSN	1096-0007 ; 0014-4835
ISSN (online)	1096-0007
ISSN	0014-4835
DOI	10.1016/j.exer.2009.01.019
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Article ; Online: Peptide redesign for inhibition of the complement system: Targeting age-related macular degeneration.

Mohan, Rohith R / Cabrera, Andrea P / Harrison, Reed E S / Gorham, Ronald D / Johnson, Lincoln V / Ghosh, Kaustabh / Morikis, Dimitrios

Molecular vision

2016 Volume 22, Page(s) 1280–1290

Abstract: Purpose: To redesign a complement-inhibiting peptide with the potential to become a therapeutic for dry and wet age-related macular degeneration (AMD).: Methods: We present a new potent peptide (Peptide 2) of the compstatin family. The peptide is ... ...

Abstract	Purpose: To redesign a complement-inhibiting peptide with the potential to become a therapeutic for dry and wet age-related macular degeneration (AMD). Methods: We present a new potent peptide (Peptide 2) of the compstatin family. The peptide is developed by rational design, based on a mechanistic binding hypothesis, and structural and physicochemical properties derived from molecular dynamics (MD) simulation. The inhibitory activity, efficacy, and solubility of Peptide 2 are evaluated using a hemolytic assay, a human RPE cell-based assay, and ultraviolet (UV) absorption properties, respectively, and compared to the respective properties of its parent peptide (Peptide 1). Results: The sequence of Peptide 2 contains an arginine-serine N-terminal extension (a characteristic of parent Peptide 1) and a novel 8-polyethylene glycol (PEG) block C-terminal extension. Peptide 2 has significantly improved aqueous solubility compared to Peptide 1 and comparable complement inhibitory activity. In addition, Peptide 2 is more efficacious in inhibiting complement activation in a cell-based model that mimics the pathobiology of dry AMD. Conclusions: We have designed a new peptide analog of compstatin that combines N-terminal polar amino acid extensions and C-terminal PEGylation extensions. This peptide demonstrates significantly improved aqueous solubility and complement inhibitory efficacy, compared to the parent peptide. The new peptide overcomes the aggregation limitation for clinical translation of previous compstatin analogs and is a candidate to become a therapeutic for the treatment of AMD.
Language	English
Publishing date	2016
Publishing country	United States
Document type	Journal Article
ZDB-ID	2017540-1
ISSN	1090-0535 ; 1090-0535
ISSN (online)	1090-0535
ISSN	1090-0535
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Article ; Online: One-Year Follow-Up in a Phase 1/2a Clinical Trial of an Allogeneic RPE Cell Bioengineered Implant for Advanced Dry Age-Related Macular Degeneration.

Translational vision science & technology

2021 Volume 10, Issue 10, Page(s) 13

Abstract: Purpose: To report 1-year follow-up of a phase 1/2a clinical trial testing a composite subretinal implant having polarized human embryonic stem cell (hESC)-derived retinal pigment epithelium (RPE) cells on an ultrathin parylene substrate in subjects ... ...

Abstract	Purpose: To report 1-year follow-up of a phase 1/2a clinical trial testing a composite subretinal implant having polarized human embryonic stem cell (hESC)-derived retinal pigment epithelium (RPE) cells on an ultrathin parylene substrate in subjects with advanced non-neovascular age-related macular degeneration (NNAMD). Methods: The phase 1/2a clinical trial included 16 subjects in two cohorts. The main endpoint was safety assessed at 365 days using ophthalmic and systemic exams. Pseudophakic subjects with geographic atrophy (GA) and severe vision loss were eligible. Low-dose tacrolimus immunosuppression was utilized for 68 days in the peri-implantation period. The implant was delivered to the worst seeing eye with a custom subretinal insertion device in an outpatient setting. A data safety monitoring committee reviewed all results. Results: The treated eyes of all subjects were legally blind with a baseline best-corrected visual acuity (BCVA) of ≤ 20/200. There were no unexpected serious adverse events. Four subjects in cohort 1 had serious ocular adverse events, including retinal hemorrhage, edema, focal retinal detachment, or RPE detachment, which was mitigated in cohort 2 using improved hemostasis during surgery. Although this study was not powered to assess efficacy, treated eyes from four subjects showed an increased BCVA of >5 letters (6-13 letters). A larger proportion of treated eyes experienced a >5-letter gain when compared with the untreated eye (27% vs. 7%; P = not significant) and a larger proportion of nonimplanted eyes demonstrated a >5-letter loss (47% vs. 33%; P = not significant). Conclusions: Outpatient delivery of the implant can be performed routinely. At 1 year, the implant is safe and well tolerated in subjects with advanced dry AMD. Translational relevance: This work describes the first clinical trial, to our knowledge, of a novel implant for advanced dry AMD.
MeSH term(s)	Follow-Up Studies ; Geographic Atrophy/therapy ; Hematopoietic Stem Cell Transplantation ; Humans ; Macular Degeneration/therapy ; Visual Acuity
Language	English
Publishing date	2021-10-06
Publishing country	United States
Document type	Clinical Trial, Phase I ; Clinical Trial, Phase II ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2674602-5
ISSN	2164-2591 ; 2164-2591
ISSN (online)	2164-2591
ISSN	2164-2591
DOI	10.1167/tvst.10.10.13
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