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Neuroprotectin D1: A docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress
Open accessAbstract
Docosahexaenoic acid (DHA) is a lipid peroxidation target in oxidative injury to retinal pigment epithelium (RPE) and retina. Photoreceptor and synaptic membranes share the highest content of DHA of all cell membranes. This fatty acid is required for RPE functional integrity; however, it is not known whether specific mediators generated from DHA contribute to its biological significance. We used human ARPE-19 cells and demonstrated the synthesis of 10,17S-docosatriene [neuroprotectin D1 (NPD1)]. This synthesis was enhanced by the calcium ionophore A-23187, by IL-1beta, or by supplying DHA. Under these conditions, there is a time-dependent release of endogenous free DHA followed by NPD1 formation, suggesting that phospholipase A(2) releases the mediator's precursor. Added NPD1 potently counteracted H(2)O(2)/tumor necrosis factor alpha oxidative-stress-triggered apoptotic RPE DNA damage. NPD1 also up-regulated the antiapoptotic proteins Bcl-2 and Bcl-x(L) and decreased proapoptotic Bax and Bad expression. Moreover, NPD1 (50 nM) inhibited oxidative-stress-induced caspase-3 activation. NPD1 also inhibited IL-1beta-stimulated expression of cyclooxygenase 2 promoter transfected into ARPE-19 cells. Overall, NPD1 protected RPE cells from oxidative-stress-induced apoptosis, and we predict that it will similarly protect neurons. This lipid mediator therefore may indirectly contribute to photoreceptor cell survival as well. Because both RPE and photoreceptor cells die in retinal degenerations, our findings contribute to the understanding of retinal cell survival signaling and potentially to the development of new therapeutic strategies.
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“DHA then ends up amounting to more than 50% of OS phospholipid fatty acyl chains and therefore DHA-containing phospholipids in the retina and other cells are reservoirs for docosanoids (Bazan et al., 1984; Mukherjee et al., 2004).”
From Docosanoids and elovanoids from omega-3 fatty acids are pro-homeostatic modulators of inflammatory responses, cell damage and neuroprotection (2018) · cites this paper as Mukherjee et al., 2004
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“In fact, NPD1 also induces the anti-apoptotic Bcl-2 family of proteins Bcl-2 and Bcl-xl in oxidatively challenged human RPE cells (Mukherjee et al., 2004) and promotes cytoprotection.”
From Docosanoids and elovanoids from omega-3 fatty acids are pro-homeostatic modulators of inflammatory responses, cell damage and neuroprotection (2018) · cites this paper as Mukherjee et al., 2004
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InfluentialLipid metabolism and retinal diseases
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Modulating antioxidant systems as a therapeutic approach to retinal degeneration
Ren, X., & Léveillard, T. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102510 · Cited by 35
“rich in polyunsaturated fatty acids that are susceptible to lipid peroxidation [23].”
Synthesis and in vivo evaluation of non-hepatotoxic acetaminophen analogs
Vaccarino, A. L., Paúl, D., Mukherjee, P. K., Turco, E., Marcheselli, V. L., Xu, L., Trudell, M. L., Minguez, J., MATIA, M. P., Sunkel, C. E., et al. (2006) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2006.07.054 · Cited by 34
Das, U. N. (2013) · Clinical Lipidology · doi:10.2217/clp.13.31 · Cited by 33
The role of pro-resolving lipid mediators in ocular diseases
Wei, J., & Gronert, K. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.03.006 · Cited by 31
“A large body of work has shown that NPD1 promotes cell survival of human RPE cells upon exposure to oxidative stress and that 15-LOX is the rate-limiting enzyme for endogenous formation (Mukherjee et al., 2004, 2007; Calandria et al., 2012).”
Lipid Mediator Informatics and Proteomics in Inflammation-Resolution
Lu, Y., Hong, S., Gotlinger, K. H., & Serhan, C. N. (2006) · The Scientific World JOURNAL · doi:10.1100/tsw.2006.118 · Cited by 33
“, PNAS 2004[47] Regulates TH2 cells, apoptosis and raft formation Ariel et al.”
Anti-inflammatory effects of resolvin-D1 on human corneal epithelial cells: in vitro study
Erdinest, N., Ovadia, H., Kormas, R. M., & Solomon, A. (2014) · Journal of Inflammation · doi:10.1186/1476-9255-11-6 · Cited by 32
“The results of the study support previous studies which have shown that RVs are very potent [17,45].”
Geng, X. H., Yang, B., Li, R., Teng, T., LaDu, M. J., Sun, G. Y., Greenlief, C. M., & Lee, J. C. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-01805-4 · Cited by 33
Biochemical and therapeutic effects of Omega-3 fatty acids in sickle cell disease
Daak, A. A., López-Toledano, M. A., & Heeney, M. M. (2020) · Complementary Therapies in Medicine · doi:10.1016/j.ctim.2020.102482 · Cited by 31
Neuroprotectin D1 Protects Against Postoperative Delirium-Like Behavior in Aged Mice
Zhou, Y., Wang, J., Li, X., Li, K., Chen, L., Zhang, Z., & Peng, M. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.582674 · Cited by 33
“NPD1 shares biological activities with other lipid mediators such as resolvins and maresins, including accelerating nonphlogistic macrophage phagocytosis, inhibiting neutrophil infiltration, and regulating the production of cytokines and chemokines (Serhan et al., 2002; Mukherjee et al., 2004; Hong et al., 2014).”
Breaking the cycle: the role of omega-3 polyunsaturated fatty acids in inflammation-driven cancers
Patterson, W. L., & Georgel, P. T. (2014) · Biochemistry and Cell Biology · doi:10.1139/bcb-2013-0127 · Cited by 32
“(Bazan 2005; Mukherjee et al. 2004) While this antiapoptotic effect is beneficial in neurodegenerative conditions such as Alzheimer’s, it could be quite harmful in cancers.”
Pohl, E. E., Voltchenko, A. M., & Rupprecht, A. (2008) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2008.01.025 · Cited by 31
“025 (neuroprotectins) [2,3], bactericide and anti-cancer defence [4,5].”
Infectious neutrophil deployment is regulated by resolvin D4
Libreros, S., Nshimiyimana, R., Lee, B., & Serhan, C. N. (2023) · Blood · doi:10.1182/blood.2022019145 · Cited by 30
Berressem, D., Koch, K. A., Franke, N., Klein, J., & Eckert, G. P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167329 · Cited by 33
Zirpoli, H., Sosunov, S. A., Niatsetskaya, Z. V., Mayurasakorn, K., Kollareth, D. J. M., Serhan, C. N., Ten, V. S., & Deckelbaum, R. J. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113495 · Cited by 32
Bioactive Oxylipins Profile in Marine Microalgae
Linares-Maurizi, A., Réversat, G., Awad, R., Bultel‐Poncé, V., Oger, C., Galano, J., Balas, L., Durbec, A., Bertrand‐Michel, J., Durand, T., et al. (2023) · Marine Drugs · doi:10.3390/md21030136 · Cited by 31
“The lipoxygenase-catalyzed derivatives of ALA, such as EPA (resolvins E) and DHA (resolvins D, protectins), have been reported to display anti-inflammatory properties [23] in nano and picomolar levels [24,25].”
Immunomodulation of microglia by docosahexaenoic acid and eicosapentaenoic acid
Hjorth, E., & Freund‐Levi, Y. (2012) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32835017cc · Cited by 32
“It is possible that conversion of v-3 FAs to PRFs is required for the activation of PPAR-g upon exposure to v-3 FAs – a hypothesis yet to be tested.”
InfluentialGonzález‐Herrero, M. E. R., Ruiz, M. R., López-Román, F. J., Sánchez, J. M. M., & Domingo, J. C. (2018) · Clinical ophthalmology · doi:10.2147/opth.s157635 · Cited by 31
“…( ω -3 PUFAs), particularly docosahexaenoic acid (DHA), 12–22 as well as the xanthophylls, lutein and zeaxanthin, 23–25 are involved in the molecular pathways implicated in DR (Figure 1) 15,17,23–34 and support the rationale of dietary supplementation with DHA and xanthophyll carotenoids in DR.”
Ryan, V. H., Primiani, C. T., Rao, J. S., Ahn, K., Rapoport, S. I., & Blanchard, H. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100858 · Cited by 32
Effect of α-Linolenic Acid on Streptozotocin-induced Diabetic Retinopathy Indices In Vivo
Shen, J., Ma, Q., Shen, S., Xu, G., & Das, U. N. (2013) · Archives of Medical Research · doi:10.1016/j.arcmed.2013.09.010 · Cited by 30
Soory, M. (2010) · Cancers · doi:10.3390/cancers2020670 · Cited by 31
Calandria, J. M., Mukherjee, P. K., Vaccari, J. C. D. R., Zhu, M., Petasis, N. A., & Bazan, N. G. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.287078 · Cited by 31
“Positive Hoechst staining was characterized by high intensity, size reduction, and high circularity, which are distinctive features of the apoptotic shrinking nuclei (24).”
InfluentialClasses of Lipid Mediators and Their Effects on Vascular Inflammation in Atherosclerosis
Lubrano, V., Ndreu, R., & Balzan, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021637 · Cited by 33
“PD: Protectins are biosynthesized via a lipoxygenase-mediated pathway from Docosahex enoic acid and t is conver ed into a intermediate that co ains 17S-hydroxyperoxide, and successively, by leukocytes, into 10,17 Dihydroxy-docosahexaenoic acid, known as PD1 [162,163] or neuroprotection [164], for its protective role i…”
Cardoso, H. D., Passos, P. P., Lagranha, C. J., Ferraz, A. C., dos Santos, E. F., Oliveira, R. F. S., Oliveira, P. E. L., Santos, R. D. C. F., de Santana, D. F., Borba, J. M. C., et al. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00249 · Cited by 29
“Moreover, the DHA-derived docosanoid, named neuroprotectin D1, protects human retinal pigment epithelial cells from OS (Mukherjee et al., 2004) as well as inhibits brain ischemia-reperfusion-mediated leukocyte infiltration and proinflammatory gene expression (Marcheselli et al., 2003).”
Eady, T. N., Khoutorova, L., Atkins, K. D., Bazan, N. G., & Belayev, L. (2012) · Experimental & Translational Stroke Medicine · doi:10.1186/2040-7378-4-19 · Cited by 30
“NPD1 is a potent inhibitor of polymorphonuclear leukocyte infiltration and pro-inflammatory gene expression, and an overall mediator of neuroprotection [6,21].”
InfluentialDescorbeth, M., Figueroa, K. F., Serrano‐Illán, M., & León, M. A. D. (2018) · Brain and Behavior · doi:10.1002/brb3.1123 · Cited by 30
Fatty acid-derived lipid mediators and blood platelet aggregation
Lagarde, M., Chen, P., Véricel, E., & Guichardant, M. (2010) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2010.02.017 · Cited by 29
“Among the dihydroxydocosatrienes, a focus has been put on 10(R),17(S)-diOH-docosa4Z,7Z,11E,13E,15Z,19Z-hexaenoic acid, called protectin D1 (PD1) when described as a peripheral anti-inflammatory agent, or neuroprotectin D1 (NPD1) when described as a neuroprotective agent [36,37].”
Light, lipids and photoreceptor survival: live or let die?
German, O. L., Agnolazza, D. L., Politi, L. E., & Rotstein, N. P. (2015) · Photochemical & Photobiological Sciences · doi:10.1039/c5pp00194c · Cited by 31
How plausible is the use of dietaryn-3 PUFA in the adjuvant therapy of cancer?
Serini, S., Vasconcelos, R. O., Fasano, E., & Calviello, G. (2016) · Nutrition Research Reviews · doi:10.1017/s0954422416000044 · Cited by 30
Subramanian, P., Mendez, E. F., & Becerra, S. P. (2016) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-19039 · Cited by 29
“Furthermore, Mukherjee et al.(24) have reported an apoptotic mechanism via caspase activation with a combination of TNF-a (10 ng/mL) and 400 to 800 lM H2O2 in an ARPE-19 cell model of oxidative stress.”
Diacylglycerol Kinase Epsilon Modulates Rapid Kindling Epileptogenesis
Musto, A. E., & Bazan, N. G. (2006) · Epilepsia · doi:10.1111/j.1528-1167.2006.00418.x · Cited by 29
“Knowing how the intrinsic regulatory mechanisms of these enzymes operate during kindling epileptogenesis is critical, because these lipid mediators also modulate the neuroprotection and repair of the nervous system (35,36).”
Pharmacological protection of retinal pigmented epithelial cells by sulindac involves PPAR-α
Sur, A., Kesaraju, S., Prentice, H. M., Ayyanathan, K., Baronas-Lowell, D. M., Zhu, D., Hinton, D. R., Blanks, J. C., & Weissbach, H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419576111 · Cited by 28
“DHA has been shown to be critical for maintaining the integrity of photoreceptors (34), and its protective effect on RPE cells to oxidative stress is mediated by neuroprotectin D1 (NPD1), a derivative of DHA, that possesses antiapoptotic and antiinflammatory properties (35, 36).”
Halapin, N., & Bazan, N. G. (2010) · Neurochemical Research · doi:10.1007/s11064-010-0351-8 · Cited by 28
“the stereoselective, pro-survival lipid mediator neuroprotectin D1 (NPD1: 10R,17S-dihydroxy-docosa-4Z,7Z,11E, 13E,15Z,19Z-hexaenoic acid) [24].”
Do Nutritional Supplements Have a Role in Age Macular Degeneration Prevention?
Pinazo-Duran, M. D., Gómez‐Ulla, F., Arias, L., Araiz, J., Casaroli-Marano, R. P., Gallego‐Pinazo, R., García‐Medina, J. J., Gálvez, M. I. L., Manzanas, L., Salas, A., et al. (2014) · Journal of Ophthalmology · doi:10.1155/2014/901686 · Cited by 28
“Other oxidant agents can also be used to generate stress, for example, paraquad [110].”
Neuroprotection by Docosahexaenoic Acid in Brain Injury
Kim, H. (2014) · Military Medicine · doi:10.7205/milmed-d-14-00162 · Cited by 28
Cell-Cell Interaction in the Transcellular Biosynthesis of Novel ω-3-Derived Lipid Mediators
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Molecular Pharmacology of Inflammation Resolution in Atherosclerosis
Kotlyarov, S. N., & Котлярова, А. А. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094808 · Cited by 31
“Sci. 2022, 23, 4808 21 of 34 CysLT1 receptor cysteinyl leukotriene receptor 1 DHA docosahexaenoic acid DRV1 resolvin D1 receptor EETs epoxyeicosatrienoic acids eNOS endothelial nitric oxide synthase EPA eicosapentaenoic acid ERK extracellular-signal-regulated kinase FLAP five lipoxygenase activating protein fMLFK N-fo…”
Metadata
- Authors
- Mukherjee, P. K., Marcheselli, V. L., Serhan, C. N., & Bazan, N. G.
- Affiliations
- Louisiana State University (US)
- Corresponding author
- Bazan, Nicolas G.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2004-05-19
- Volume
- 101
- Issue
- 22
- Pages
- 8491-8496
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC420421
- OpenAlex
- W1739691545
- Cited by
- 753
- References
- 50
- Citations by year
- 2026: 22 · 2025: 14 · 2024: 13 · 2023: 14 · 2022: 24 · 2021: 20 · 2020: 34 · 2019: 23 · 2018: 25 · 2017: 34 · 2016: 24 · 2015: 35 · 2014: 42 · 2013: 52 · 2012: 42
- FWCI
- 44.10
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Huntsman Cancer Institute
- University of Leicester
- National Institutes of Health (4r37gm038765-19, GM 38765)
- National Eye Institute (EY05121, R01EY005121)
- National Institute of General Medical Sciences (GM 38765, R01GM038765, R37-GM038765)
- National Center for Research Resources (P20RR-16816, P20RR016816)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Health Sciences › Medicine › Biochemistry (medical) › Antioxidant Activity and Oxidative Stress
- Keywords
- neuroprotectin D1, docosahexaenoic acid, retinal pigment epithelium, oxidative stress, apoptosis, phospholipase A2, cyclooxygenase-2, Bcl-2 family proteins, caspase-3, IL-1β, photoreceptor survival, retinal degeneration, lipid mediators
- MeSH terms
- Cell Line, Docosahexaenoic Acids, Epithelial Cells, Humans, Interleukin-1, Isoenzymes, Membrane Proteins, Pigment Epithelium of Eye, Prostaglandin-Endoperoxide Synthases, Lipid Peroxidation, Molecular Structure, Apoptosis, Oxidative Stress, Proto-Oncogene Proteins c-bcl-2, Caspases, Cyclooxygenase 2, Caspase 3, DNA Fragmentation
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