Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice

Retinopathy of prematurity (ROP) with early vessel loss (Phase I) followed by uncontrolled vessel growth (Phase II) causes visual impairment in premature infants. Although supplementation with omega-3 (n-3) docosahexaenoic acid (DHA) alone shows mixed results in preventing ROP, supplementation with...

Full description

Saved in:
Bibliographic Details
Main Authors: Myriam Boeck, Hitomi Yagi, Pia Lundgren, Aldina Pivodic, Anders K. Nilsson, Yan Zeng, Chuck T. Chen, Taku Kasai, Deokho Lee, Shen Nian, Victoria Hirst, Katherine Neilsen, Chaomei Wang, Jeff Lee, Mathew Yu, Andrew McCutcheon, Sasha A. Singh, Masanori Aikawa, Richard P. Bazinet, Zhongjie Fu, Ann Hellström, Lois EH Smith
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Pharmacological Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1043661825003020
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849245962105520128
author Myriam Boeck
Hitomi Yagi
Pia Lundgren
Aldina Pivodic
Anders K. Nilsson
Yan Zeng
Chuck T. Chen
Taku Kasai
Deokho Lee
Shen Nian
Victoria Hirst
Katherine Neilsen
Chaomei Wang
Jeff Lee
Mathew Yu
Andrew McCutcheon
Sasha A. Singh
Masanori Aikawa
Richard P. Bazinet
Zhongjie Fu
Ann Hellström
Lois EH Smith
author_facet Myriam Boeck
Hitomi Yagi
Pia Lundgren
Aldina Pivodic
Anders K. Nilsson
Yan Zeng
Chuck T. Chen
Taku Kasai
Deokho Lee
Shen Nian
Victoria Hirst
Katherine Neilsen
Chaomei Wang
Jeff Lee
Mathew Yu
Andrew McCutcheon
Sasha A. Singh
Masanori Aikawa
Richard P. Bazinet
Zhongjie Fu
Ann Hellström
Lois EH Smith
author_sort Myriam Boeck
collection DOAJ
description Retinopathy of prematurity (ROP) with early vessel loss (Phase I) followed by uncontrolled vessel growth (Phase II) causes visual impairment in premature infants. Although supplementation with omega-3 (n-3) docosahexaenoic acid (DHA) alone shows mixed results in preventing ROP, supplementation with both n-3 DHA and n-6 arachidonic acid (ARA) in early postnatal life reduces severe ROP by 50 % (Mega Donna Mega study). In the Mega Donna Mega study, 146 (72.6 %) of 201 included infants had at least one hyperglycemic episode during the first 14 days of life, which is a strong ROP risk factor. We therefore evaluated the protective effects and mechanisms of combined dietary n-3 DHA and n-6 ARA in a neonatal mouse model of hyperglycemia-induced suppression of retinal vascular development (Phase I ROP). At postnatal day (P) 10, retinal vessel growth was improved in pups from mothers on diets enriched with 1 % DHA + 2 % ARA vs. 3 % DHA. Lipid changes in pup plasma and RPE complex (retinal pigment epithelium with choroid and sclera) were in accordance with maternal diets' DHA and ARA levels, indicating that milk lipids reflected maternal diets. Proteomic retinal analysis revealed increased abundances of proteins related to mitochondrial respiration and glucose metabolism with the combined diet. Inhibition of mitochondrial ATP synthase negated the protective effects of the combined diet. In conclusion, combined DHA+ARA oral maternal supplementation protects against hyperglycemia-induced retinopathy in mouse neonates (Phase I ROP model) through enhanced retinal metabolism, suggesting the potential of balanced lipid supplementation for ROP prevention.
format Article
id doaj-art-5f031c8acb7d4c7595799ba861112a4d
institution Kabale University
issn 1096-1186
language English
publishDate 2025-09-01
publisher Elsevier
record_format Article
series Pharmacological Research
spelling doaj-art-5f031c8acb7d4c7595799ba861112a4d2025-08-20T03:58:40ZengElsevierPharmacological Research1096-11862025-09-0121910787710.1016/j.phrs.2025.107877Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal miceMyriam Boeck0Hitomi Yagi1Pia Lundgren2Aldina Pivodic3Anders K. Nilsson4Yan Zeng5Chuck T. Chen6Taku Kasai7Deokho Lee8Shen Nian9Victoria Hirst10Katherine Neilsen11Chaomei Wang12Jeff Lee13Mathew Yu14Andrew McCutcheon15Sasha A. Singh16Masanori Aikawa17Richard P. Bazinet18Zhongjie Fu19Ann Hellström20Lois EH Smith21Department of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Ophthalmology, Keio University School of Medicine, Tokyo 160-8582, JapanThe Sahlgrenska Centre for Pediatric Ophthalmology Research, Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg 416 85, SwedenThe Sahlgrenska Centre for Pediatric Ophthalmology Research, Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg 416 85, SwedenThe Sahlgrenska Centre for Pediatric Ophthalmology Research, Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg 416 85, SwedenDepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Nutritional Sciences, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, CanadaCenter for Interdisciplinary Cardiovascular Sciences, Division of Cardiovascular Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Nutritional Sciences, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, CanadaDepartment of Nutritional Sciences, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, CanadaCenter for Interdisciplinary Cardiovascular Sciences, Division of Cardiovascular Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USACenter for Interdisciplinary Cardiovascular Sciences, Division of Cardiovascular Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Excellence in Vascular Biology, Division of Cardiovascular Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA; Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USADepartment of Nutritional Sciences, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, CanadaDepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USAThe Sahlgrenska Centre for Pediatric Ophthalmology Research, Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg 416 85, SwedenDepartment of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA; Correspondence to: Department of Ophthalmology, Boston Children’s Hospital, Harvard Medical School, 3 Blackfan Circle, CLS 18, Boston, MA 02115, USA.Retinopathy of prematurity (ROP) with early vessel loss (Phase I) followed by uncontrolled vessel growth (Phase II) causes visual impairment in premature infants. Although supplementation with omega-3 (n-3) docosahexaenoic acid (DHA) alone shows mixed results in preventing ROP, supplementation with both n-3 DHA and n-6 arachidonic acid (ARA) in early postnatal life reduces severe ROP by 50 % (Mega Donna Mega study). In the Mega Donna Mega study, 146 (72.6 %) of 201 included infants had at least one hyperglycemic episode during the first 14 days of life, which is a strong ROP risk factor. We therefore evaluated the protective effects and mechanisms of combined dietary n-3 DHA and n-6 ARA in a neonatal mouse model of hyperglycemia-induced suppression of retinal vascular development (Phase I ROP). At postnatal day (P) 10, retinal vessel growth was improved in pups from mothers on diets enriched with 1 % DHA + 2 % ARA vs. 3 % DHA. Lipid changes in pup plasma and RPE complex (retinal pigment epithelium with choroid and sclera) were in accordance with maternal diets' DHA and ARA levels, indicating that milk lipids reflected maternal diets. Proteomic retinal analysis revealed increased abundances of proteins related to mitochondrial respiration and glucose metabolism with the combined diet. Inhibition of mitochondrial ATP synthase negated the protective effects of the combined diet. In conclusion, combined DHA+ARA oral maternal supplementation protects against hyperglycemia-induced retinopathy in mouse neonates (Phase I ROP model) through enhanced retinal metabolism, suggesting the potential of balanced lipid supplementation for ROP prevention.http://www.sciencedirect.com/science/article/pii/S1043661825003020Postnatal hyperglycemiaRetinopathy of prematurityDHAARARetinal vasculature
spellingShingle Myriam Boeck
Hitomi Yagi
Pia Lundgren
Aldina Pivodic
Anders K. Nilsson
Yan Zeng
Chuck T. Chen
Taku Kasai
Deokho Lee
Shen Nian
Victoria Hirst
Katherine Neilsen
Chaomei Wang
Jeff Lee
Mathew Yu
Andrew McCutcheon
Sasha A. Singh
Masanori Aikawa
Richard P. Bazinet
Zhongjie Fu
Ann Hellström
Lois EH Smith
Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice
Pharmacological Research
Postnatal hyperglycemia
Retinopathy of prematurity
DHA
ARA
Retinal vasculature
title Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice
title_full Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice
title_fullStr Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice
title_full_unstemmed Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice
title_short Combined dietary omega-3 and omega-6 fatty acids protect against hyperglycemia-associated retinopathy in neonatal mice
title_sort combined dietary omega 3 and omega 6 fatty acids protect against hyperglycemia associated retinopathy in neonatal mice
topic Postnatal hyperglycemia
Retinopathy of prematurity
DHA
ARA
Retinal vasculature
url http://www.sciencedirect.com/science/article/pii/S1043661825003020
work_keys_str_mv AT myriamboeck combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT hitomiyagi combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT pialundgren combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT aldinapivodic combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT andersknilsson combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT yanzeng combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT chucktchen combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT takukasai combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT deokholee combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT shennian combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT victoriahirst combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT katherineneilsen combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT chaomeiwang combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT jefflee combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT mathewyu combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT andrewmccutcheon combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT sashaasingh combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT masanoriaikawa combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT richardpbazinet combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT zhongjiefu combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT annhellstrom combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice
AT loisehsmith combineddietaryomega3andomega6fattyacidsprotectagainsthyperglycemiaassociatedretinopathyinneonatalmice