TY - JOUR
T1 - Cytochrome P450 monooxygenase lipid metabolites are significant second messengers in the resolution of choroidal neovascularization
AU - Hasegawa, Eiichi
AU - Inafuku, Saori
AU - Mulki, Lama
AU - Okunuki, Yoko
AU - Yanai, Ryoji
AU - Smith, Kaylee E.
AU - Kim, Clifford B.
AU - Klokman, Garrett
AU - Bielenberg, Diane R.
AU - Puli, Narender
AU - Falck, John R.
AU - Husain, Deeba
AU - Miller, Joan W.
AU - Edin, Matthew L.
AU - Zeldin, Darryl C.
AU - Lee, Kin Sing Stephen
AU - Hammock, Bruce D.
AU - Schunck, Wolf Hagen
AU - Connor, Kip M.
N1 - Funding Information:
ACKNOWLEDGMENTS. This study was supported by a Special Scholar Award (to K.M.C.), a Medical Student Fellowship Grant (to C.B.K.), and an unrestricted grant (to J.W.M.) from Research to Prevent Blindness. Special thanks go to Department of Ophthalmology, Harvard University, and Massachusetts Eye and Ear Infirmary for supporting this research (K.M.C.); the Massachusetts Lions Eye Research Fund (K.M.C.); the BrightFocus Foundation (K.M.C.); Grant R01EY022084/S1 (to K.M.C.); partial support (to K.M.C.) from the West Coast Metabolomics Center (NIH 1U24DK097154); a fellowship from the Japan Society for the Promotion of Science Postdoctoral Fellowships for Research Abroad (to E.H.); the Intramural Program of the NIH, National Institute of Environmental Health Sciences (NIEHS) (Z01 ES025034 to D.C.Z.); the Robert A. Welch Foundation (I-0011 to J.R.F.); and NIH (HL111392 to J.R.F.). Partial support was supplied by NIEHS (R01ES002710 to B.D.H.), NIEHS/Superfund Research Program (P42 ES004699 to B.D.H.), and the NIH (K99ES024806 and R00ES024806 to K.S.S.L.).
Publisher Copyright:
© 2017, National Academy of Sciences. All rights reserved.
PY - 2017/9/5
Y1 - 2017/9/5
N2 - Age-related macular degeneration (AMD) is the most common cause of blindness for individuals age 50 and above in the developed world. Abnormal growth of choroidal blood vessels, or choroidal neovascularization (CNV), is a hallmark of the neovascular (wet) form of advanced AMD and leads to significant vision loss. A growing body of evidence supports a strong link between neovascular disease and inflammation. Metabolites of long-chain polyunsaturated fatty acids derived from the cytochrome P450 (CYP) monooxygenase pathway serve as vital second messengers that regulate a number of hormones and growth factors involved in inflammation and vascular function. Using transgenic mice with altered CYP lipid biosynthetic pathways in a mouse model of laser-induced CNV, we characterized the role of these lipid metabolites in regulating neovascular disease. We discovered that the CYP-derived lipid metabolites epoxydocosapentaenoic acids (EDPs) and epoxyeicosatetraenoic acids (EEQs) are vital in dampening CNV severity. Specifically, overexpression of the monooxygenase CYP2C8 or genetic ablation or inhibition of the soluble epoxide hydrolase (sEH) enzyme led to increased levels of EDP and EEQ with attenuated CNV development. In contrast, when we promoted the degradation of these CYP-derived metabolites by transgenic overexpression of sEH, the protective effect against CNV was lost. We found that these molecules work in part through their ability to regulate the expression of key leukocyte adhesion molecules, on both leukocytes and endothelial cells, thereby mediating leukocyte recruitment. These results suggest that CYP lipid signaling molecules and their regulators are potential therapeutic targets in neovascular diseases.
AB - Age-related macular degeneration (AMD) is the most common cause of blindness for individuals age 50 and above in the developed world. Abnormal growth of choroidal blood vessels, or choroidal neovascularization (CNV), is a hallmark of the neovascular (wet) form of advanced AMD and leads to significant vision loss. A growing body of evidence supports a strong link between neovascular disease and inflammation. Metabolites of long-chain polyunsaturated fatty acids derived from the cytochrome P450 (CYP) monooxygenase pathway serve as vital second messengers that regulate a number of hormones and growth factors involved in inflammation and vascular function. Using transgenic mice with altered CYP lipid biosynthetic pathways in a mouse model of laser-induced CNV, we characterized the role of these lipid metabolites in regulating neovascular disease. We discovered that the CYP-derived lipid metabolites epoxydocosapentaenoic acids (EDPs) and epoxyeicosatetraenoic acids (EEQs) are vital in dampening CNV severity. Specifically, overexpression of the monooxygenase CYP2C8 or genetic ablation or inhibition of the soluble epoxide hydrolase (sEH) enzyme led to increased levels of EDP and EEQ with attenuated CNV development. In contrast, when we promoted the degradation of these CYP-derived metabolites by transgenic overexpression of sEH, the protective effect against CNV was lost. We found that these molecules work in part through their ability to regulate the expression of key leukocyte adhesion molecules, on both leukocytes and endothelial cells, thereby mediating leukocyte recruitment. These results suggest that CYP lipid signaling molecules and their regulators are potential therapeutic targets in neovascular diseases.
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U2 - 10.1073/pnas.1620898114
DO - 10.1073/pnas.1620898114
M3 - Article
C2 - 28827330
AN - SCOPUS:85029220481
SN - 0027-8424
VL - 114
SP - E7545-E7553
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 36
ER -