Oxidative damage-induced inflammation initiates age-related macular degeneration
Open accessAbstract
Oxidative damage and inflammation are postulated to be involved in age-related macular degeneration (AMD). However, the molecular signal(s) linking oxidation to inflammation in this late-onset disease is unknown. Here we describe AMD-like lesions in mice after immunization with mouse serum albumin adducted with carboxyethylpyrrole, a unique oxidation fragment of docosahexaenoic acid that has previously been found adducting proteins in drusen from AMD donor eye tissues and in plasma samples from individuals with AMD. Immunized mice develop antibodies to this hapten, fix complement component-3 in Bruch's membrane, accumulate drusen below the retinal pigment epithelium during aging, and develop lesions in the retinal pigment epithelium mimicking geographic atrophy, the blinding end-stage condition characteristic of the dry form of AMD. We hypothesize that these mice are sensitized to the generation of carboxyethylpyrrole adducts in the outer retina, where docosahexaenoic acid is abundant and conditions for oxidative damage are permissive. This new model provides a platform for dissecting the molecular pathology of oxidative damage in the outer retina and the immune response contributing to AMD.
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Mice with mutations making them prone to oxidative stress or dysregulation of the complement pathway have been presented as models of AMD.
“and mice with mutations making them prone to oxidative stress or dysregulation of the complement pathway have been presented as models of AMD (Imamura et al., 2006; Justilien et al., 2007; Hollyfield et al., 2008; Ufret-Vincenty et al., 2010).”
From Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis (2015) · cites this paper as Hollyfield et al., 2008
The CEP-mouse model demonstrates the role of oxidative damage in inducing inflammation and eventually GA-like lesions.
“In addition, the CEP-mouse model demonstrates the role of oxidative damage in inducing inflammation and eventually GA-like lesions (72).”
From Unraveling a Multifactorial Late-Onset Disease: From Genetic Susceptibility to Disease Mechanisms for Age-Related Macular Degeneration (2009) · cites this paper as [72]
Serum albumin is one of the major proteins modified with CEP.
“Serum albumin is one of the major proteins modified with CEP”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
Immunization of mice with CEP-modified mouse serum albumin generates a strong immunologic response against endogenous CEP adducts in the outer retina.
“immunize mice with CEP-modified mouse serum albumin, generating a strong immunologic response against endogenous CEP adducts in the outer retina”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
RPE cells in CEP-immunized mice had vesiculation, pyknosis, lysis, and areas of RPE loss with overlying swollen photoreceptors.
“The RPE cells in CEP-immunized mice had vesiculation, pyknosis, lysis, and areas of RPE loss with overlying swollen photoreceptors.”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
Compared to age-matched controls, CEP-immunized mice have significant BlamD accumulation throughout the retina.
“Compared to age-matched controls, CEP-immunized mice have significant BlamD accumulation throughout the retina.”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
Fundoscopy of CEP-immunized mice revealed patchy, reticular changes that were not present in controls.
“Fundoscopy of immunized mice revealed patchy, reticular changes that were not present in controls”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
Bruch's membrane was significantly thicker (about 3 fold) in CEP-immunized mice.
“Bruch’s membrane was significantly thicker (about 3 fold) in immunized mice.”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
CEP-immunized mice had C3d in Bruch's membrane, signifying that an intact immune system responds to CEP immunization with sub-RPE complement deposition, a feature of AMD.
“Immunized mice had C3d, a C3b degradation product in Bruch’s membrane, signifying that an intact immune system responds to CEP immunization with sub-RPE complement deposition, a well-known feature of AMD”
From Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD) (2010) · cites this paper as Hollyfield et al., 2008
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- Authors
- Hollyfield, J. G., Bonilha, V. L., Rayborn, M. E., Yang, X., Shadrach, K. G., Lu, L., Ufret, R. L., Salomon, R. G., & Perez, V. L.
- Affiliations
- Cleveland Clinic Lerner College of Medicine (US)
- Case Western Reserve University (US)
- Corresponding author
- Hollyfield, Joe G
- Perez, Victor L
- Venue
- Nature Medicine
- Published
- 2008-01-27
- Volume
- 14
- Issue
- 2
- Pages
- 194-198
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC2748836
- OpenAlex
- W2064170412
- Cited by
- 710
- References
- 31
- Citations by year
- 2026: 18 · 2025: 23 · 2024: 25 · 2023: 24 · 2022: 28 · 2021: 39 · 2020: 32 · 2019: 32 · 2018: 23 · 2017: 34 · 2016: 40 · 2015: 48 · 2014: 61 · 2013: 50 · 2012: 69
- FWCI
- 55.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Eye Institute (R21EY017153, R56EY014240, R56EY10240, R24EY015638, K08EY014912, R01EY014240)
- National Institute of General Medical Sciences (R01-GM21249, R01GM021249)
- Topics
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
- Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
- Keywords
- age-related macular degeneration, oxidative damage, inflammation, docosahexaenoic acid, protein adducts, drusen, geographic atrophy, retinal pigment epithelium, Bruch's membrane, complement C3, mouse model, outer retina, dry age-related macular degeneration
- MeSH terms
- Aging, Animals, Antibodies, Antigens, Immunization, Inflammation, Macular Degeneration, Mice, Inbred BALB C, Mice, Inbred C57BL, Pigment Epithelium of Eye, Pyrroles, Time Factors, Complement C3d, Bruch Membrane, Titrimetry, Oxidative Stress, Protein Transport, Mice
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