Maternal diabetes affects rat offspring retinal structure and function: Sex-specific vulnerabilities at infancy
Maternal diabetes negatively impacts the offspring's brain, but little is known about its effects on the retina, which is also part of the central nervous system. We hypothesized that maternal diabetes adversely influences offspring retina development leading to structural and functional defici...
Saved in:
| Published in: | Life sciences (1973) Vol. 327; p. 121852 |
|---|---|
| Main Authors: | , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
Netherlands
Elsevier Inc
15-08-2023
|
| Subjects: | |
| Online Access: | Get full text |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Maternal diabetes negatively impacts the offspring's brain, but little is known about its effects on the retina, which is also part of the central nervous system. We hypothesized that maternal diabetes adversely influences offspring retina development leading to structural and functional deficits.
Retinal structure and function were evaluated at infancy, by optical coherence tomography and electroretinography, in male and female offspring of control, diabetic and diabetic-treated with insulin Wistar rats.
Maternal diabetes induced a delay in male and female offspring eye-opening, while insulin treatment expedited it. Structural analysis showed that maternal diabetes decreased the thickness of the inner and outer segment layer of photoreceptors in male offspring. Electroretinography also revealed that maternal diabetes decreased the amplitude of scotopic b-wave and flicker response in males, suggesting bipolar cells and cone photoreceptor dysfunction, an effect not observed in females. Conversely, maternal diabetes decreased cone arrestin protein levels in female retinas, while not affecting cone photoreceptor number. Dam insulin therapy was efficient in preventing the offspring photoreceptor changes.
Our results suggest that photoreceptors are affected by maternal diabetes, which may account for visual impairments at infancy. Notably, both male and female offspring presented specific vulnerabilities to hyperglycemia in this sensitive period of development. |
|---|---|
| AbstractList | Maternal diabetes negatively impacts the offspring's brain, but little is known about its effects on the retina, which is also part of the central nervous system. We hypothesized that maternal diabetes adversely influences offspring retina development leading to structural and functional deficits.
Retinal structure and function were evaluated at infancy, by optical coherence tomography and electroretinography, in male and female offspring of control, diabetic and diabetic-treated with insulin Wistar rats.
Maternal diabetes induced a delay in male and female offspring eye-opening, while insulin treatment expedited it. Structural analysis showed that maternal diabetes decreased the thickness of the inner and outer segment layer of photoreceptors in male offspring. Electroretinography also revealed that maternal diabetes decreased the amplitude of scotopic b-wave and flicker response in males, suggesting bipolar cells and cone photoreceptor dysfunction, an effect not observed in females. Conversely, maternal diabetes decreased cone arrestin protein levels in female retinas, while not affecting cone photoreceptor number. Dam insulin therapy was efficient in preventing the offspring photoreceptor changes.
Our results suggest that photoreceptors are affected by maternal diabetes, which may account for visual impairments at infancy. Notably, both male and female offspring presented specific vulnerabilities to hyperglycemia in this sensitive period of development. AIMSMaternal diabetes negatively impacts the offspring's brain, but little is known about its effects on the retina, which is also part of the central nervous system. We hypothesized that maternal diabetes adversely influences offspring retina development leading to structural and functional deficits. MAIN METHODSRetinal structure and function were evaluated at infancy, by optical coherence tomography and electroretinography, in male and female offspring of control, diabetic and diabetic-treated with insulin Wistar rats. KEY FINDINGSMaternal diabetes induced a delay in male and female offspring eye-opening, while insulin treatment expedited it. Structural analysis showed that maternal diabetes decreased the thickness of the inner and outer segment layer of photoreceptors in male offspring. Electroretinography also revealed that maternal diabetes decreased the amplitude of scotopic b-wave and flicker response in males, suggesting bipolar cells and cone photoreceptor dysfunction, an effect not observed in females. Conversely, maternal diabetes decreased cone arrestin protein levels in female retinas, while not affecting cone photoreceptor number. Dam insulin therapy was efficient in preventing the offspring photoreceptor changes. SIGNIFICANCEOur results suggest that photoreceptors are affected by maternal diabetes, which may account for visual impairments at infancy. Notably, both male and female offspring presented specific vulnerabilities to hyperglycemia in this sensitive period of development. |
| ArticleNumber | 121852 |
| Author | Gaspar, Rita Realinho, Ana M. Correia, Raquel G. Baptista, Filipa I. Ambrósio, António F. Boia, Raquel Paiva, Beatriz |
| Author_xml | – sequence: 1 givenname: Ana M. surname: Realinho fullname: Realinho, Ana M. organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal – sequence: 2 givenname: Raquel surname: Boia fullname: Boia, Raquel organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal – sequence: 3 givenname: Beatriz surname: Paiva fullname: Paiva, Beatriz organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal – sequence: 4 givenname: Raquel G. surname: Correia fullname: Correia, Raquel G. organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal – sequence: 5 givenname: Rita surname: Gaspar fullname: Gaspar, Rita organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal – sequence: 6 givenname: António F. surname: Ambrósio fullname: Ambrósio, António F. organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal – sequence: 7 givenname: Filipa I. surname: Baptista fullname: Baptista, Filipa I. email: fibaptista@fmed.uc.pt organization: Univ Coimbra, Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, Coimbra, Portugal |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37321535$$D View this record in MEDLINE/PubMed |
| BookMark | eNp9kEtPGzEURq0KBCHlB3RTeclmwrUdz6NdIdSXBGIBXVt37OvK0cST2p4I_n0nCmXJ6m7OPdJ3LthJHCMx9knASoCorzerweeVBKlWQopWyw9sIdqmq6BW4oQtAOS6UhL0ObvIeQMAWjfqjJ2rRkmhlV6w8R4LpYgDdwF7KpQ5ek-2ZJ6w8NH7vEsh_uGJSjhguaTJlikRx-i4n6ItYYxf-CM9V3lHNvhg-X4aIiXswxBKOCgLD9FjtC8f2anHIdPl612y39-_Pd3-rO4efvy6vbmrrNKqVNI3CsCjk5Kgb5sahXTW0dp389LGoesaC1ADqrXCzmpYt9T10mtRo-9ILdnV0btL49-JcjHbkC0NA0Yap2xkKxupO6G7GRVH1KYx50TezIu3mF6MAHPobDZm7mwOnc2x8_zz-VU_9Vtybx__w87A1yNA88h9oGSyDRQtuZDmusaN4R39P50dkXE |
| CitedBy_id | crossref_primary_10_1111_eci_14266 |
| Cites_doi | 10.4239/wjd.v6.i3.412 10.2337/dc17-0592 10.1016/S0002-9394(98)00016-6 10.7554/eLife.32337 10.1016/S0896-6273(01)00470-6 10.1093/bmb/60.1.173 10.1007/s00125-019-4923-0 10.1038/s41419-020-2593-y 10.1242/jcs.259187 10.1007/s10571-019-00658-8 10.1016/j.physbeh.2012.08.001 10.1002/glia.22858 10.1159/000146872 10.1001/jama.2015.2707 10.1111/j.1755-3768.1993.tb04652.x 10.1111/j.1464-5491.2011.03285.x 10.1159/000455904 10.1073/pnas.0907660106 10.1007/s11892-014-0569-y 10.1016/j.jchemneu.2018.03.005 10.3389/fncel.2014.00129 10.1111/j.1464-5491.2010.03024.x 10.1016/j.neuroscience.2016.01.025 10.2337/diab.37.12.1671 10.1113/jphysiol.2002.019703 10.1177/153537020322800204 10.2147/EB.S383231 10.1186/s13064-019-0137-x 10.1186/s12974-017-0859-9 10.1542/peds.2011-2583 10.1016/j.ajo.2010.06.036 10.1371/journal.pone.0061861 10.1016/j.neuroscience.2010.06.021 10.1038/s41598-019-41009-3 10.1016/j.exer.2014.07.011 10.1146/annurev-vision-091517-034425 |
| ContentType | Journal Article |
| Copyright | 2023 Elsevier Inc. Copyright © 2023. Published by Elsevier Inc. |
| Copyright_xml | – notice: 2023 Elsevier Inc. – notice: Copyright © 2023. Published by Elsevier Inc. |
| DBID | NPM AAYXX CITATION 7X8 |
| DOI | 10.1016/j.lfs.2023.121852 |
| DatabaseName | PubMed CrossRef MEDLINE - Academic |
| DatabaseTitle | PubMed CrossRef MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic PubMed |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Sciences (General) Biology |
| EISSN | 1879-0631 |
| EndPage | 121852 |
| ExternalDocumentID | 10_1016_j_lfs_2023_121852 37321535 S0024320523004873 |
| Genre | Journal Article |
| GroupedDBID | --- --K --M -~X .~1 0R~ 1B1 1RT 1~. 4.4 457 5GY 5RE 5VS 6TJ 7-5 71M 8P~ 9JM AABNK AACTN AAEDT AAEDW AAIAV AAIKJ AAKOC AALRI AAOAW AAQFI AATCM AAXUO ABFNM ABFRF ABJNI ABLJU ABLVK ABMAC ABMZM ABYKQ ABZDS ACDAQ ACGFO ACGFS ACIUM ACIWK ACPRK ACRLP ADBBV ADEZE AEBSH AEFWE AEKER AENEX AFKWA AFRAH AFTJW AFXIZ AGUBO AGYEJ AIEXJ AIKHN AITUG AJOXV AJRQY ALCLG ALMA_UNASSIGNED_HOLDINGS AMFUW AMRAJ ANZVX AXJTR BKOJK BLXMC BNPGV C45 CNWQP CS3 DU5 EBS EFJIC EFLBG EO8 EO9 EP2 EP3 F5P FDB FIRID FNPLU FYGXN G-Q GBLVA IH2 IHE J1W K-O KOM L7B LCYCR M34 M41 MO0 N9A O-L O9- OAUVE OGGZJ OVD OZT P-8 P-9 P2P PC. Q38 ROL RPZ SDF SDG SDP SES SEW SPCBC SSH SSP SSZ T5K TEORI YZZ ~G- AAHBH AAXKI AFJKZ AKRWK NPM RIG .55 .GJ 29L 3O- 53G AAQXK AAYXX ABTAH ABXDB ADMUD AFFNX AGHFR AHHHB ASPBG AVWKF AZFZN CITATION EJD FEDTE FGOYB G-2 HMG HMT HVGLF HZ~ H~9 J5H MVM R2- SIN SPT WUQ X7M Y6R YYP ZGI ZKB ZXP ZY4 7X8 |
| ID | FETCH-LOGICAL-c353t-2f7300fad22e0b876a12dcde4f91217dad97c0060a343a9c5048e9b2f516af9e3 |
| ISSN | 0024-3205 |
| IngestDate | Fri Oct 25 03:56:17 EDT 2024 Thu Sep 26 16:09:29 EDT 2024 Wed Oct 16 00:39:02 EDT 2024 Fri Feb 23 02:36:10 EST 2024 |
| IsPeerReviewed | true |
| IsScholarly | true |
| Keywords | Maternal diabetes Offspring retina Neurodevelopment Photoreceptors Sex differences Insulin therapy |
| Language | English |
| License | Copyright © 2023. Published by Elsevier Inc. |
| LinkModel | OpenURL |
| MergedId | FETCHMERGED-LOGICAL-c353t-2f7300fad22e0b876a12dcde4f91217dad97c0060a343a9c5048e9b2f516af9e3 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| PMID | 37321535 |
| PQID | 2827259159 |
| PQPubID | 23479 |
| PageCount | 1 |
| ParticipantIDs | proquest_miscellaneous_2827259159 crossref_primary_10_1016_j_lfs_2023_121852 pubmed_primary_37321535 elsevier_sciencedirect_doi_10_1016_j_lfs_2023_121852 |
| PublicationCentury | 2000 |
| PublicationDate | 2023-08-15 |
| PublicationDateYYYYMMDD | 2023-08-15 |
| PublicationDate_xml | – month: 08 year: 2023 text: 2023-08-15 day: 15 |
| PublicationDecade | 2020 |
| PublicationPlace | Netherlands |
| PublicationPlace_xml | – name: Netherlands |
| PublicationTitle | Life sciences (1973) |
| PublicationTitleAlternate | Life Sci |
| PublicationYear | 2023 |
| Publisher | Elsevier Inc |
| Publisher_xml | – name: Elsevier Inc |
| References | Van Lieshout, Voruganti (bb0025) 2008; 33 Tian, Copenhagen (bb0135) 2001; 32 Ruiz-Palacios, Ruiz-Alcaraz, Sanchez-Campillo, Larque (bb0110) 2017; 70 Sousa, Correia, Cruz, Martins, Rodrigues, Gomes, Ambrosio, Baptista (bb0040) 2020; 5 Gaspar, Baptista, Galvao, Castilho, Cunha, Ambrosio (bb0180) 2010; 169 Silverman, Wong (bb0070) 2018; 4 Temple, Hardiman, Pellegrini, Horrocks, Martinez-Cengotitabengoa (bb0030) 2011; 28 Guan, Cao, Liu, Zhao, Fu, Yu (bb0080) 2017; 6 Hami, Shojae, Vafaee-Nezhad, Lotfi, Kheradmand, Haghir (bb0005) 2015; 6 Siman, Naeser, Eriksson (bb0175) 1993; 71 Saszik, Robson, Frishman (bb0155) 2002; 543 Landau, Bajka, Kirchschlager (bb0045) 1998; 125 Vuong, Odero, Rozbacher, Stevenson, Kereliuk, Pereira, Dolinsky, Kauppinen (bb0150) 2017; 14 Fiess, Brandt, Mildenberger, Urschitz, Wagner, Grabitz, Hoffmann, Pfeiffer, Schuster (bb0165) 2022; 14 Tariq, Samarawickrama, Li, Huynh, Burlutsky, Mitchell (bb0050) 2010; 150 Bourque, Kuny, Reyes, Davidge, Sauve (bb0160) 2013; 8 Yamamoto, Benham, Dewey, Sanchez, Murphy, Feig, Donovan (bb0010) 2019; 62 Ji, Chen, Sundquist, Sundquist (bb0015) 2018; 41 Titialii-Torres, Morris (bb0065) 2022; 135 Li, Jiang, Samuel (bb0085) 2019; 14 Rochefort, Garaschuk, Milos, Narushima, Marandi, Pichler, Kovalchuk, Konnerth (bb0130) 2009; 106 Paolicelli, Bisht, Tremblay (bb0075) 2014; 8 Kiss, Woodside, Felicio, Anselmo-Franci, Damasceno (bb0140) 2012; 107 Xiang, Wang, Martinez, Walthall, Curry, Page, Buchanan, Coleman, Getahun (bb0020) 2015; 313 Boia, Salinas-Navarro, Gallego-Ortega, Galindo-Romero, Aires, Agudo-Barriuso, Ambrosio, Vidal-Sanz, Santiago (bb0190) 2020; 11 Alves, Boia, Campos, Martins, Nunes, Madeira, Santiago, Pereira, Reis, Ambrosio (bb0195) 2018; 24 Giavini, Prati (bb0170) 1990; 137 Canavan, Goldspink (bb0115) 1988; 37 Piazza, Segabinazi, de Meireles, Mega, Spindler, Augustin, Salvalaggio, Achaval, Kruse, Coirini (bb0095) 2019; 39 Krakowiak, Walker, Bremer, Baker, Ozonoff, Hansen, Hertz-Picciotto (bb0055) 2012; 129 Van Assche, Holemans, Aerts (bb0100) 2001; 60 Vafaei-Nezhad, Hami, Sadeghi, Ghaemi, Hosseini, Abedini, Haghir (bb0120) 2016; 318 Baptista, Pinto, Elvas, Martins, Almeida, Ambrosio (bb0185) 2014; 127 Kinney, Rabe, Jensen, Steger (bb0090) 2003; 228 Araujo, Keating, Martel (bb0105) 2015; 15 Singh, Castillo, Brown, Kaslin, Dwyer, Gibert (bb0060) 2019; 9 Nielsen, Andersen, Lundbye-Christensen (bb0035) 2010; 27 Sato (bb0145) 2015; 63 Sadeghi, Esfandiary, Hami, Khanahmad, Hejazi, Mardani, Razavi (bb0125) 2018; 91 Silverman (10.1016/j.lfs.2023.121852_bb0070) 2018; 4 Tian (10.1016/j.lfs.2023.121852_bb0135) 2001; 32 Titialii-Torres (10.1016/j.lfs.2023.121852_bb0065) 2022; 135 Van Assche (10.1016/j.lfs.2023.121852_bb0100) 2001; 60 Siman (10.1016/j.lfs.2023.121852_bb0175) 1993; 71 Sato (10.1016/j.lfs.2023.121852_bb0145) 2015; 63 Yamamoto (10.1016/j.lfs.2023.121852_bb0010) 2019; 62 Tariq (10.1016/j.lfs.2023.121852_bb0050) 2010; 150 Araujo (10.1016/j.lfs.2023.121852_bb0105) 2015; 15 Gaspar (10.1016/j.lfs.2023.121852_bb0180) 2010; 169 Vuong (10.1016/j.lfs.2023.121852_bb0150) 2017; 14 Xiang (10.1016/j.lfs.2023.121852_bb0020) 2015; 313 Fiess (10.1016/j.lfs.2023.121852_bb0165) 2022; 14 Saszik (10.1016/j.lfs.2023.121852_bb0155) 2002; 543 Piazza (10.1016/j.lfs.2023.121852_bb0095) 2019; 39 Bourque (10.1016/j.lfs.2023.121852_bb0160) 2013; 8 Paolicelli (10.1016/j.lfs.2023.121852_bb0075) 2014; 8 Kiss (10.1016/j.lfs.2023.121852_bb0140) 2012; 107 Guan (10.1016/j.lfs.2023.121852_bb0080) 2017; 6 Vafaei-Nezhad (10.1016/j.lfs.2023.121852_bb0120) 2016; 318 Landau (10.1016/j.lfs.2023.121852_bb0045) 1998; 125 Temple (10.1016/j.lfs.2023.121852_bb0030) 2011; 28 Rochefort (10.1016/j.lfs.2023.121852_bb0130) 2009; 106 Baptista (10.1016/j.lfs.2023.121852_bb0185) 2014; 127 Van Lieshout (10.1016/j.lfs.2023.121852_bb0025) 2008; 33 Singh (10.1016/j.lfs.2023.121852_bb0060) 2019; 9 Sousa (10.1016/j.lfs.2023.121852_bb0040) 2020; 5 Hami (10.1016/j.lfs.2023.121852_bb0005) 2015; 6 Ji (10.1016/j.lfs.2023.121852_bb0015) 2018; 41 Ruiz-Palacios (10.1016/j.lfs.2023.121852_bb0110) 2017; 70 Alves (10.1016/j.lfs.2023.121852_bb0195) 2018; 24 Nielsen (10.1016/j.lfs.2023.121852_bb0035) 2010; 27 Sadeghi (10.1016/j.lfs.2023.121852_bb0125) 2018; 91 Kinney (10.1016/j.lfs.2023.121852_bb0090) 2003; 228 Krakowiak (10.1016/j.lfs.2023.121852_bb0055) 2012; 129 Canavan (10.1016/j.lfs.2023.121852_bb0115) 1988; 37 Boia (10.1016/j.lfs.2023.121852_bb0190) 2020; 11 Giavini (10.1016/j.lfs.2023.121852_bb0170) 1990; 137 Li (10.1016/j.lfs.2023.121852_bb0085) 2019; 14 |
| References_xml | – volume: 60 start-page: 173 year: 2001 end-page: 182 ident: bb0100 article-title: Long-term consequences for offspring of diabetes during pregnancy publication-title: Br. Med. Bull. contributor: fullname: Aerts – volume: 228 start-page: 152 year: 2003 end-page: 159 ident: bb0090 article-title: Maternal hyperglycemia leads to gender-dependent deficits in learning and memory in offspring publication-title: Exp. Biol. Med. (Maywood) contributor: fullname: Steger – volume: 318 start-page: 122 year: 2016 end-page: 133 ident: bb0120 article-title: The impacts of diabetes in pregnancy on hippocampal synaptogenesis in rat neonates publication-title: Neuroscience contributor: fullname: Haghir – volume: 62 start-page: 1561 year: 2019 end-page: 1574 ident: bb0010 article-title: Neurocognitive and behavioural outcomes in offspring exposed to maternal pre-existing diabetes: a systematic review and meta-analysis publication-title: Diabetologia contributor: fullname: Donovan – volume: 14 start-page: 80 year: 2017 ident: bb0150 article-title: Exposure to gestational diabetes mellitus induces neuroinflammation, derangement of hippocampal neurons, and cognitive changes in rat offspring publication-title: J. Neuroinflammation contributor: fullname: Kauppinen – volume: 14 start-page: 127 year: 2022 end-page: 135 ident: bb0165 article-title: Adults born small for gestational age at term have thinner peripapillary retinal nerve fiber layers than controls publication-title: Eye Brain contributor: fullname: Schuster – volume: 9 start-page: 4121 year: 2019 ident: bb0060 article-title: High glucose levels affect retinal patterning during zebrafish embryogenesis publication-title: Sci. Rep. contributor: fullname: Gibert – volume: 6 year: 2017 ident: bb0080 article-title: Eye opening differentially modulates inhibitory synaptic transmission in the developing visual cortex publication-title: Elife contributor: fullname: Yu – volume: 169 start-page: 1589 year: 2010 end-page: 1600 ident: bb0180 article-title: Diabetes differentially affects the content of exocytotic proteins in hippocampal and retinal nerve terminals publication-title: Neuroscience contributor: fullname: Ambrosio – volume: 135 year: 2022 ident: bb0065 article-title: Embryonic hyperglycemia perturbs the development of specific retinal cell types, including photoreceptors publication-title: J. Cell Sci. contributor: fullname: Morris – volume: 125 start-page: 605 year: 1998 end-page: 611 ident: bb0045 article-title: Topless optic disks in children of mothers with type I diabetes mellitus publication-title: Am J. Ophthalmol. contributor: fullname: Kirchschlager – volume: 5 year: 2020 ident: bb0040 article-title: Sex differences in offspring neurodevelopment, cognitive performance and microglia morphology associated with maternal diabetes: putative targets for insulin therapy publication-title: Brain Behav. Immun. Health contributor: fullname: Baptista – volume: 137 start-page: 132 year: 1990 end-page: 136 ident: bb0170 article-title: Morphogenesis of diabetes-induced congenital cataract in the rat publication-title: Acta Anat. (Basel) contributor: fullname: Prati – volume: 32 start-page: 439 year: 2001 end-page: 449 ident: bb0135 article-title: Visual deprivation alters development of synaptic function in inner retina after eye opening publication-title: Neuron contributor: fullname: Copenhagen – volume: 4 start-page: 45 year: 2018 end-page: 77 ident: bb0070 article-title: Microglia in the retina: roles in development, maturity, and disease publication-title: Annu. Rev. Vis. Sci. contributor: fullname: Wong – volume: 70 start-page: 16 year: 2017 end-page: 25 ident: bb0110 article-title: Role of insulin in placental transport of nutrients in gestational diabetes mellitus publication-title: Ann. Nutr. Metab. contributor: fullname: Larque – volume: 41 start-page: 770 year: 2018 end-page: 774 ident: bb0015 article-title: Type 1 diabetes in parents and risk of attention deficit/hyperactivity disorder in offspring: a population-based study in Sweden publication-title: Diabetes Care contributor: fullname: Sundquist – volume: 15 start-page: 569 year: 2015 ident: bb0105 article-title: Impact of gestational diabetes mellitus in the maternal-to-fetal transport of nutrients publication-title: Curr. Diab. Rep. contributor: fullname: Martel – volume: 37 start-page: 1671 year: 1988 end-page: 1677 ident: bb0115 article-title: Maternal diabetes in rats. II. Effects on fetal growth and protein turnover publication-title: Diabetes contributor: fullname: Goldspink – volume: 27 start-page: 786 year: 2010 end-page: 790 ident: bb0035 article-title: Maternal blood glucose in diabetic pregnancies and cognitive performance in offspring in young adulthood: a Danish cohort study publication-title: Diabet. Med. contributor: fullname: Lundbye-Christensen – volume: 39 start-page: 401 year: 2019 end-page: 414 ident: bb0095 article-title: Severe uncontrolled maternal hyperglycemia induces microsomia and neurodevelopment delay accompanied by apoptosis, cellular survival, and neuroinflammatory deregulation in rat offspring hippocampus publication-title: Cell. Mol. Neurobiol. contributor: fullname: Coirini – volume: 106 start-page: 15049 year: 2009 end-page: 15054 ident: bb0130 article-title: Sparsification of neuronal activity in the visual cortex at eye-opening publication-title: Proc. Natl. Acad. Sci. U. S. A. contributor: fullname: Konnerth – volume: 129 start-page: e1121 year: 2012 end-page: e1128 ident: bb0055 article-title: Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders publication-title: Pediatrics contributor: fullname: Hertz-Picciotto – volume: 24 start-page: 353 year: 2018 end-page: 366 ident: bb0195 article-title: Subtle thinning of retinal layers without overt vascular and inflammatory alterations in a rat model of prediabetes publication-title: Mol. Vis. contributor: fullname: Ambrosio – volume: 543 start-page: 899 year: 2002 end-page: 916 ident: bb0155 article-title: The scotopic threshold response of the dark-adapted electroretinogram of the mouse publication-title: J. Physiol. contributor: fullname: Frishman – volume: 91 start-page: 27 year: 2018 end-page: 34 ident: bb0125 article-title: The effects of maternal diabetes and insulin treatment on neurogenesis in the developing hippocampus of male rats publication-title: J. Chem. Neuroanat. contributor: fullname: Razavi – volume: 33 start-page: 395 year: 2008 end-page: 404 ident: bb0025 article-title: Diabetes mellitus during pregnancy and increased risk of schizophrenia in offspring: a review of the evidence and putative mechanisms publication-title: J. Psychiatry Neurosci. contributor: fullname: Voruganti – volume: 127 start-page: 91 year: 2014 end-page: 103 ident: bb0185 article-title: Diabetes induces changes in KIF1A, KIF5B and dynein distribution in the rat retina: implications for axonal transport publication-title: Exp. Eye Res. contributor: fullname: Ambrosio – volume: 150 start-page: 883 year: 2010 end-page: 887 ident: bb0050 article-title: Retinal thickness in the offspring of diabetic pregnancies publication-title: Am J. Ophthalmol. contributor: fullname: Mitchell – volume: 71 start-page: 629 year: 1993 end-page: 636 ident: bb0175 article-title: Increased lenticular aldose reductase activity and high incidence of congenital cataract in the offspring of diabetic rats publication-title: Acta Ophthalmol. contributor: fullname: Eriksson – volume: 313 start-page: 1425 year: 2015 end-page: 1434 ident: bb0020 article-title: Association of maternal diabetes with autism in offspring publication-title: JAMA contributor: fullname: Getahun – volume: 14 start-page: 12 year: 2019 ident: bb0085 article-title: Microglia in the developing retina publication-title: Neural Dev. contributor: fullname: Samuel – volume: 8 start-page: 129 year: 2014 ident: bb0075 article-title: Fractalkine regulation of microglial physiology and consequences on the brain and behavior publication-title: Front. Cell. Neurosci. contributor: fullname: Tremblay – volume: 28 start-page: 845 year: 2011 end-page: 848 ident: bb0030 article-title: Cognitive function in 6- to 12-year-old offspring of women with type 1 diabetes publication-title: Diabet. Med. contributor: fullname: Martinez-Cengotitabengoa – volume: 6 start-page: 412 year: 2015 end-page: 422 ident: bb0005 article-title: Some of the experimental and clinical aspects of the effects of the maternal diabetes on developing hippocampus publication-title: World J. Diabetes contributor: fullname: Haghir – volume: 63 start-page: 1394 year: 2015 end-page: 1405 ident: bb0145 article-title: Effects of microglia on neurogenesis publication-title: Glia contributor: fullname: Sato – volume: 8 year: 2013 ident: bb0160 article-title: Prenatal hypoxia is associated with long-term retinal dysfunction in rats publication-title: PLoS One contributor: fullname: Sauve – volume: 11 start-page: 401 year: 2020 ident: bb0190 article-title: Activation of adenosine A(3) receptor protects retinal ganglion cells from degeneration induced by ocular hypertension publication-title: Cell Death Dis. contributor: fullname: Santiago – volume: 107 start-page: 292 year: 2012 end-page: 300 ident: bb0140 article-title: Impact of maternal mild hyperglycemia on maternal care and offspring development and behavior of Wistar rats publication-title: Physiol. Behav. contributor: fullname: Damasceno – volume: 33 start-page: 395 year: 2008 ident: 10.1016/j.lfs.2023.121852_bb0025 article-title: Diabetes mellitus during pregnancy and increased risk of schizophrenia in offspring: a review of the evidence and putative mechanisms publication-title: J. Psychiatry Neurosci. contributor: fullname: Van Lieshout – volume: 6 start-page: 412 year: 2015 ident: 10.1016/j.lfs.2023.121852_bb0005 article-title: Some of the experimental and clinical aspects of the effects of the maternal diabetes on developing hippocampus publication-title: World J. Diabetes doi: 10.4239/wjd.v6.i3.412 contributor: fullname: Hami – volume: 41 start-page: 770 year: 2018 ident: 10.1016/j.lfs.2023.121852_bb0015 article-title: Type 1 diabetes in parents and risk of attention deficit/hyperactivity disorder in offspring: a population-based study in Sweden publication-title: Diabetes Care doi: 10.2337/dc17-0592 contributor: fullname: Ji – volume: 125 start-page: 605 year: 1998 ident: 10.1016/j.lfs.2023.121852_bb0045 article-title: Topless optic disks in children of mothers with type I diabetes mellitus publication-title: Am J. Ophthalmol. doi: 10.1016/S0002-9394(98)00016-6 contributor: fullname: Landau – volume: 6 year: 2017 ident: 10.1016/j.lfs.2023.121852_bb0080 article-title: Eye opening differentially modulates inhibitory synaptic transmission in the developing visual cortex publication-title: Elife doi: 10.7554/eLife.32337 contributor: fullname: Guan – volume: 32 start-page: 439 year: 2001 ident: 10.1016/j.lfs.2023.121852_bb0135 article-title: Visual deprivation alters development of synaptic function in inner retina after eye opening publication-title: Neuron doi: 10.1016/S0896-6273(01)00470-6 contributor: fullname: Tian – volume: 24 start-page: 353 year: 2018 ident: 10.1016/j.lfs.2023.121852_bb0195 article-title: Subtle thinning of retinal layers without overt vascular and inflammatory alterations in a rat model of prediabetes publication-title: Mol. Vis. contributor: fullname: Alves – volume: 60 start-page: 173 year: 2001 ident: 10.1016/j.lfs.2023.121852_bb0100 article-title: Long-term consequences for offspring of diabetes during pregnancy publication-title: Br. Med. Bull. doi: 10.1093/bmb/60.1.173 contributor: fullname: Van Assche – volume: 62 start-page: 1561 year: 2019 ident: 10.1016/j.lfs.2023.121852_bb0010 article-title: Neurocognitive and behavioural outcomes in offspring exposed to maternal pre-existing diabetes: a systematic review and meta-analysis publication-title: Diabetologia doi: 10.1007/s00125-019-4923-0 contributor: fullname: Yamamoto – volume: 11 start-page: 401 year: 2020 ident: 10.1016/j.lfs.2023.121852_bb0190 article-title: Activation of adenosine A(3) receptor protects retinal ganglion cells from degeneration induced by ocular hypertension publication-title: Cell Death Dis. doi: 10.1038/s41419-020-2593-y contributor: fullname: Boia – volume: 135 year: 2022 ident: 10.1016/j.lfs.2023.121852_bb0065 article-title: Embryonic hyperglycemia perturbs the development of specific retinal cell types, including photoreceptors publication-title: J. Cell Sci. doi: 10.1242/jcs.259187 contributor: fullname: Titialii-Torres – volume: 39 start-page: 401 year: 2019 ident: 10.1016/j.lfs.2023.121852_bb0095 article-title: Severe uncontrolled maternal hyperglycemia induces microsomia and neurodevelopment delay accompanied by apoptosis, cellular survival, and neuroinflammatory deregulation in rat offspring hippocampus publication-title: Cell. Mol. Neurobiol. doi: 10.1007/s10571-019-00658-8 contributor: fullname: Piazza – volume: 107 start-page: 292 year: 2012 ident: 10.1016/j.lfs.2023.121852_bb0140 article-title: Impact of maternal mild hyperglycemia on maternal care and offspring development and behavior of Wistar rats publication-title: Physiol. Behav. doi: 10.1016/j.physbeh.2012.08.001 contributor: fullname: Kiss – volume: 63 start-page: 1394 year: 2015 ident: 10.1016/j.lfs.2023.121852_bb0145 article-title: Effects of microglia on neurogenesis publication-title: Glia doi: 10.1002/glia.22858 contributor: fullname: Sato – volume: 137 start-page: 132 year: 1990 ident: 10.1016/j.lfs.2023.121852_bb0170 article-title: Morphogenesis of diabetes-induced congenital cataract in the rat publication-title: Acta Anat. (Basel) doi: 10.1159/000146872 contributor: fullname: Giavini – volume: 313 start-page: 1425 year: 2015 ident: 10.1016/j.lfs.2023.121852_bb0020 article-title: Association of maternal diabetes with autism in offspring publication-title: JAMA doi: 10.1001/jama.2015.2707 contributor: fullname: Xiang – volume: 71 start-page: 629 year: 1993 ident: 10.1016/j.lfs.2023.121852_bb0175 article-title: Increased lenticular aldose reductase activity and high incidence of congenital cataract in the offspring of diabetic rats publication-title: Acta Ophthalmol. doi: 10.1111/j.1755-3768.1993.tb04652.x contributor: fullname: Siman – volume: 28 start-page: 845 year: 2011 ident: 10.1016/j.lfs.2023.121852_bb0030 article-title: Cognitive function in 6- to 12-year-old offspring of women with type 1 diabetes publication-title: Diabet. Med. doi: 10.1111/j.1464-5491.2011.03285.x contributor: fullname: Temple – volume: 70 start-page: 16 year: 2017 ident: 10.1016/j.lfs.2023.121852_bb0110 article-title: Role of insulin in placental transport of nutrients in gestational diabetes mellitus publication-title: Ann. Nutr. Metab. doi: 10.1159/000455904 contributor: fullname: Ruiz-Palacios – volume: 106 start-page: 15049 year: 2009 ident: 10.1016/j.lfs.2023.121852_bb0130 article-title: Sparsification of neuronal activity in the visual cortex at eye-opening publication-title: Proc. Natl. Acad. Sci. U. S. A. doi: 10.1073/pnas.0907660106 contributor: fullname: Rochefort – volume: 15 start-page: 569 year: 2015 ident: 10.1016/j.lfs.2023.121852_bb0105 article-title: Impact of gestational diabetes mellitus in the maternal-to-fetal transport of nutrients publication-title: Curr. Diab. Rep. doi: 10.1007/s11892-014-0569-y contributor: fullname: Araujo – volume: 91 start-page: 27 year: 2018 ident: 10.1016/j.lfs.2023.121852_bb0125 article-title: The effects of maternal diabetes and insulin treatment on neurogenesis in the developing hippocampus of male rats publication-title: J. Chem. Neuroanat. doi: 10.1016/j.jchemneu.2018.03.005 contributor: fullname: Sadeghi – volume: 5 year: 2020 ident: 10.1016/j.lfs.2023.121852_bb0040 article-title: Sex differences in offspring neurodevelopment, cognitive performance and microglia morphology associated with maternal diabetes: putative targets for insulin therapy publication-title: Brain Behav. Immun. Health contributor: fullname: Sousa – volume: 8 start-page: 129 year: 2014 ident: 10.1016/j.lfs.2023.121852_bb0075 article-title: Fractalkine regulation of microglial physiology and consequences on the brain and behavior publication-title: Front. Cell. Neurosci. doi: 10.3389/fncel.2014.00129 contributor: fullname: Paolicelli – volume: 27 start-page: 786 year: 2010 ident: 10.1016/j.lfs.2023.121852_bb0035 article-title: Maternal blood glucose in diabetic pregnancies and cognitive performance in offspring in young adulthood: a Danish cohort study publication-title: Diabet. Med. doi: 10.1111/j.1464-5491.2010.03024.x contributor: fullname: Nielsen – volume: 318 start-page: 122 year: 2016 ident: 10.1016/j.lfs.2023.121852_bb0120 article-title: The impacts of diabetes in pregnancy on hippocampal synaptogenesis in rat neonates publication-title: Neuroscience doi: 10.1016/j.neuroscience.2016.01.025 contributor: fullname: Vafaei-Nezhad – volume: 37 start-page: 1671 year: 1988 ident: 10.1016/j.lfs.2023.121852_bb0115 article-title: Maternal diabetes in rats. II. Effects on fetal growth and protein turnover publication-title: Diabetes doi: 10.2337/diab.37.12.1671 contributor: fullname: Canavan – volume: 543 start-page: 899 year: 2002 ident: 10.1016/j.lfs.2023.121852_bb0155 article-title: The scotopic threshold response of the dark-adapted electroretinogram of the mouse publication-title: J. Physiol. doi: 10.1113/jphysiol.2002.019703 contributor: fullname: Saszik – volume: 228 start-page: 152 year: 2003 ident: 10.1016/j.lfs.2023.121852_bb0090 article-title: Maternal hyperglycemia leads to gender-dependent deficits in learning and memory in offspring publication-title: Exp. Biol. Med. (Maywood) doi: 10.1177/153537020322800204 contributor: fullname: Kinney – volume: 14 start-page: 127 year: 2022 ident: 10.1016/j.lfs.2023.121852_bb0165 article-title: Adults born small for gestational age at term have thinner peripapillary retinal nerve fiber layers than controls publication-title: Eye Brain doi: 10.2147/EB.S383231 contributor: fullname: Fiess – volume: 14 start-page: 12 year: 2019 ident: 10.1016/j.lfs.2023.121852_bb0085 article-title: Microglia in the developing retina publication-title: Neural Dev. doi: 10.1186/s13064-019-0137-x contributor: fullname: Li – volume: 14 start-page: 80 year: 2017 ident: 10.1016/j.lfs.2023.121852_bb0150 article-title: Exposure to gestational diabetes mellitus induces neuroinflammation, derangement of hippocampal neurons, and cognitive changes in rat offspring publication-title: J. Neuroinflammation doi: 10.1186/s12974-017-0859-9 contributor: fullname: Vuong – volume: 129 start-page: e1121 year: 2012 ident: 10.1016/j.lfs.2023.121852_bb0055 article-title: Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders publication-title: Pediatrics doi: 10.1542/peds.2011-2583 contributor: fullname: Krakowiak – volume: 150 start-page: 883 year: 2010 ident: 10.1016/j.lfs.2023.121852_bb0050 article-title: Retinal thickness in the offspring of diabetic pregnancies publication-title: Am J. Ophthalmol. doi: 10.1016/j.ajo.2010.06.036 contributor: fullname: Tariq – volume: 8 year: 2013 ident: 10.1016/j.lfs.2023.121852_bb0160 article-title: Prenatal hypoxia is associated with long-term retinal dysfunction in rats publication-title: PLoS One doi: 10.1371/journal.pone.0061861 contributor: fullname: Bourque – volume: 169 start-page: 1589 year: 2010 ident: 10.1016/j.lfs.2023.121852_bb0180 article-title: Diabetes differentially affects the content of exocytotic proteins in hippocampal and retinal nerve terminals publication-title: Neuroscience doi: 10.1016/j.neuroscience.2010.06.021 contributor: fullname: Gaspar – volume: 9 start-page: 4121 year: 2019 ident: 10.1016/j.lfs.2023.121852_bb0060 article-title: High glucose levels affect retinal patterning during zebrafish embryogenesis publication-title: Sci. Rep. doi: 10.1038/s41598-019-41009-3 contributor: fullname: Singh – volume: 127 start-page: 91 year: 2014 ident: 10.1016/j.lfs.2023.121852_bb0185 article-title: Diabetes induces changes in KIF1A, KIF5B and dynein distribution in the rat retina: implications for axonal transport publication-title: Exp. Eye Res. doi: 10.1016/j.exer.2014.07.011 contributor: fullname: Baptista – volume: 4 start-page: 45 year: 2018 ident: 10.1016/j.lfs.2023.121852_bb0070 article-title: Microglia in the retina: roles in development, maturity, and disease publication-title: Annu. Rev. Vis. Sci. doi: 10.1146/annurev-vision-091517-034425 contributor: fullname: Silverman |
| SSID | ssj0005573 |
| Score | 2.466523 |
| Snippet | Maternal diabetes negatively impacts the offspring's brain, but little is known about its effects on the retina, which is also part of the central nervous... AIMSMaternal diabetes negatively impacts the offspring's brain, but little is known about its effects on the retina, which is also part of the central nervous... |
| SourceID | proquest crossref pubmed elsevier |
| SourceType | Aggregation Database Index Database Publisher |
| StartPage | 121852 |
| SubjectTerms | Insulin therapy Maternal diabetes Neurodevelopment Offspring retina Photoreceptors Sex differences |
| Title | Maternal diabetes affects rat offspring retinal structure and function: Sex-specific vulnerabilities at infancy |
| URI | https://dx.doi.org/10.1016/j.lfs.2023.121852 https://www.ncbi.nlm.nih.gov/pubmed/37321535 https://search.proquest.com/docview/2827259159 |
| Volume | 327 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3da9RAEF-uLYIvYutHzy9W8EENOXK7yW3Wt6LnF1akV6FvYZPs4pWSE-oV9a93JrObxJOKCr6EEPJFfr_Mzs7O_IaxRzoFnK2CSU7i0hhH6Lh0zsRZrXVdJlKapG1iu1DvT_IX83Q-GoVk9_7Yf0UajgHWWDn7F2h3N4UDsA-YwxZQh-0f4X5oSNa5j6oan7IBWKNiBK3ERli92FCxyLpfRsBhLqR7LOzXGAsxMZkoulifoT51m0q7xJtiawGHpnno3r5bOhv5QZU0oLQahnKPwC1dNp-otKYx0eGkCwesKGv3yMBA1WV9fDDLC-oNbbGVwPduxQR7igwviF5NhvELITEgSxWcFFQLhTU_5X2i6xBLkdB5lmxzrlAwwQ8a3nhLUhb4ZSCgmMTp5MyhJruQqKKRk1buhr72ohVlFG14HMyZkltsR4DVAqO5c_BmfvK2zxjKfMKCf7ewSN6mC2486DI357JpTOvOHF9n1_w8hB8QgXbZyDZ77Ap1Jv22x3a9zT_nj70w-ZMbbBW4xQO3uOcWB27xjlvcc4t33OLALR649YwPmcU3mMXhTp5ZN9nHl_Pj569j37AjrmQmv8TCYfcDZ2ohbFLCOGumoq5qmzoNX0XVptaqQgUgI1NpdJXB97a6FC6bzozTVt5i282qsfuMT7XTylqh8hrMSTnLRVWJmdFTg06rzcbsafi-xWfSZSlCwuJpAWAUCEZBYIxZGhAo_D9ADmMBdPndZQ8DWgUYXVxJM41dreGkXCiRaZgKjNltgrF7C6kkuNEyu_NvD73LrvZ_yT22DUDZ-2zrvF4_8Hz8AcwJrVQ |
| link.rule.ids | 315,782,786,27933,27934 |
| linkProvider | Elsevier |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Maternal+diabetes+affects+rat+offspring+retinal+structure+and+function%3A+Sex-specific+vulnerabilities+at+infancy&rft.jtitle=Life+sciences+%281973%29&rft.au=Realinho%2C+Ana+M.&rft.au=Boia%2C+Raquel&rft.au=Paiva%2C+Beatriz&rft.au=Correia%2C+Raquel+G.&rft.date=2023-08-15&rft.pub=Elsevier+Inc&rft.issn=0024-3205&rft.eissn=1879-0631&rft.volume=327&rft_id=info:doi/10.1016%2Fj.lfs.2023.121852&rft.externalDocID=S0024320523004873 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0024-3205&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0024-3205&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0024-3205&client=summon |