Placental diabesity: placental VEGF and CD31 expression according to pregestational BMI and gestational weight gain in women with gestational diabetes.
Gestational diabetes
Gestational weight gain
Obesity
Placenta
Pregnancy
VEGF
Journal
Archives of gynecology and obstetrics
ISSN: 1432-0711
Titre abrégé: Arch Gynecol Obstet
Pays: Germany
ID NLM: 8710213
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
12
02
2022
accepted:
14
06
2022
medline:
1
5
2023
pubmed:
15
7
2022
entrez:
14
7
2022
Statut:
ppublish
Résumé
The aim of this study is to investigate the placental expression of VEGF and CD31 in pregnancies complicated by gestational diabetes (GDM) and the influence of pregestational BMI and gestational weight gain (GWG) on this expression. We prospectively enrolled pregnant women with diagnosis of GDM and healthy controls who delivered in our Center between December 2016 and May 2017. Patients were grouped according to the presence of GDM and we compared pregnancy characteristics, placental VEGF and CD31 expression between the cases and controls. Immunochemistry analysis was performed to assess biomarkers positivity. Positivity of biomarkers was assessed in a dichotomic fashion with positivity set at 5% for VEGF and 1% for CD31. 39 patients matched inclusion criteria, 29 (74.3%) women with GDM and 10 (25.7%) healthy controls. Immunochemistry analysis showed that VEGF was more expressed in placentas from women with GDM compared to controls (21/29, 72.4% vs 2/10, 20%; p = 0.007), and CD31 was more expressed in placentas from women with GDM compared to controls (6/29, 20.7% vs 0/10, 0%; risk difference 0.2). VEGF positivity was associated with the presence of GDM (aOR 22.02, 95% CI 1.13-428.08, p = 0.04), pregestational BMI (aOR 1.53, 1.00-2.34, p = 0.05) and GWG (aOR 1.47, 95% CI 1.03-2.11, p = 0.03). CD31 positivity was associated with the pregestational BMI (aOR 1.47, 95% CI 1.00-2.17, p = 0.05) and with the gestational weight gain (aOR 1.32, 95% CI 1.01-1.72, p = 0.04). Pregnancies complicated by GDM are characterized by increased placental expression of VEGF and CD31, and the expression of these markers is also independently associated to maternal increased pregestational BMI and GWG, defining the concept of "placental diabesity".
Identifiants
pubmed: 35835917
doi: 10.1007/s00404-022-06673-3
pii: 10.1007/s00404-022-06673-3
doi:
Substances chimiques
Vascular Endothelial Growth Factor A
0
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1823-1831Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
International Diabetes Federation (2013) IDF Atlas, 6th edn. International Diabetes Federation, Brussels
Hod M, Kapur A, Sacks DA, Hadar E, Agarwal M, Di Renzo GC, Cabero Roura L, McIntyre HD, Morris JL, Divakar H (2015) The International Federation of Gynecology and Obstetrics (FIGO) Initiative on gestational diabetes mellitus: a pragmatic guide for diagnosis, management, and care. Int J Gynaecol Obstet 131(Suppl 3):S173-211. https://doi.org/10.1016/S0020-7292(15)30033-3 (PMID: 26433807)
doi: 10.1016/S0020-7292(15)30033-3
pubmed: 26433807
Dsouza R, Horyn I, Pavalagantharajah S, Zaffar N, Jacob CE (2019) Maternal body mass index and pregnancy outcomes: a systematic review and metaanalysis. Am J Obstet Gynecol MFM 1(4):100041. https://doi.org/10.1016/j.ajogmf.2019.100041 (Epub 2019 Aug 30. PMID: 33345836)
doi: 10.1016/j.ajogmf.2019.100041
pubmed: 33345836
Bellos I, Fitrou G, Pergialiotis V, Perrea DN, Daskalakis G (2019) Serum levels of adipokines in gestational diabetes: a systematic review. J Endocrinol Invest 42(6):621–631. https://doi.org/10.1007/s40618-018-0973-2 (Epub 2018 Nov 3. PMID: 30392100)
doi: 10.1007/s40618-018-0973-2
pubmed: 30392100
Champion ML, Harper LM (2020) Gestational weight gain: update on outcomes and interventions. Curr Diab Rep 20(3):11. https://doi.org/10.1007/s11892-020-1296-1
doi: 10.1007/s11892-020-1296-1
pubmed: 32108283
Licht P, Russu V, Lehmeyer S, Wissentheit T, Siebzehnrübl E, Wildt L (2003) Cycle dependency of intrauterine vascular endothelial growth factor levels is correlated with decidualization and corpus luteum function. Fertil Steril 80(5):1228–1233. https://doi.org/10.1016/s0015-0282(03)02165-4 (PMID: 14607580)
doi: 10.1016/s0015-0282(03)02165-4
pubmed: 14607580
Goodman C, Jeyendran RS, Coulam CB (2008) Vascular endothelial growth factor gene polymorphism and implantation failure. Reprod Biomed Online 16(5):720–723. https://doi.org/10.1016/s1472-6483(10)60487-7 (PMID: 18492378)
doi: 10.1016/s1472-6483(10)60487-7
pubmed: 18492378
Zeng H, Hu L, Xie H et al (2021) Polymorphisms of vascular endothelial growth factor and recurrent implantation failure: a systematic review and meta-analysis. Arch Gynecol Obstet 304:297–307. https://doi.org/10.1007/s00404-021-06072-0
doi: 10.1007/s00404-021-06072-0
pubmed: 33891207
Augustine G, Pulikkathodi M, Renjith S, Jithesh TK (2016) A study of placental histological changes in gestational diabetes mellitus on account of fetal hypoxia. Int J Med Sci Public Heal 5:2457. https://doi.org/10.5455/ijmsph.2016.29042016494
doi: 10.5455/ijmsph.2016.29042016494
Madhuri K, Jyothi I (2017) A study on placental morphology in gesatational diabetes. J Evid Based Med Healthc 4:71–75. https://doi.org/10.18410/jebmh/2017/14
doi: 10.18410/jebmh/2017/14
Mitanchez D, Yzydorczyk C, Siddeek B et al (2015) The offspring of the diabetic mother—short- and long-term implications. Best Pract Res Clin Obstet Gynaecol 29:256–269
doi: 10.1016/j.bpobgyn.2014.08.004
pubmed: 25267399
Magee TR, Ross MG, Wedekind L, Desai M, Kjos S, Belkacemi L (2014) Gestational diabetes mellitus alters apoptotic and inflammatory gene expression of trophobasts from human term placenta. J Diabetes Complications 28(4):448–459. https://doi.org/10.1016/j.jdiacomp.2014.03.010 (Epub 2014 Mar 24. PMID: 24768206; PMCID: PMC4166519)
doi: 10.1016/j.jdiacomp.2014.03.010
pubmed: 24768206
pmcid: 4166519
Li HP, Chen X, Li MQ (2013) Gestational diabetes induces chronic hypoxia stress and excessive inflammatory response in murine placenta. Int J Clin Exp Pathol 6(4):650–659 (Epub 2013 Mar 15. PMID: 23573311; PMCID: PMC3606854)
pubmed: 23573311
pmcid: 3606854
Woodfin A, Voisin MB, Nourshargh S (2007) PECAM-1: a multi-functional molecule in inflammation and vascular biology. Arterioscler Thromb Vasc Biol 27(12):2514–2523. https://doi.org/10.1161/ATVBAHA.107.151456 (Epub 2007 Sep 13. PMID: 17872453)
doi: 10.1161/ATVBAHA.107.151456
pubmed: 17872453
Meng Q, Shao L, Luo X, Mu Y, Xu W, Gao L, Xu H, Cui Y (2016) Expressions of VEGF-A and VEGFR-2 in placentae from GDM pregnancies. Reprod Biol Endocrinol 14(1):61. https://doi.org/10.1186/s12958-016-0191-8 (PMID: 27645229; PMCID: PMC5029036)
doi: 10.1186/s12958-016-0191-8
pubmed: 27645229
pmcid: 5029036
Troncoso F, Acurio J, Herlitz K, Aguayo C, Bertoglia P, Guzman-Gutierrez E, Loyola M, Gonzalez M, Rezgaoui M, Desoye G, Escudero C (2017) Gestational diabetes mellitus is associated with increased pro-migratory activation of vascular endothelial growth factor receptor 2 and reduced expression of vascular endothelial growth factor receptor 1. PLoS ONE 12(8):e0182509. https://doi.org/10.1371/journal.pone.0182509 (PMID: 28817576; PMCID: PMC5560693)
doi: 10.1371/journal.pone.0182509
pubmed: 28817576
pmcid: 5560693
Zhou J, Ni X, Huang X, Yao J, He Q, Wang K, Duan T (2016) Potential role of hyperglycemia in fetoplacental endothelial dysfunction in gestational Diabetes mellitus. Cell Physiol Biochem 39(4):1317–1328. https://doi.org/10.1159/000447836 (Epub 2016 Sep 8. PMID: 27606810)
doi: 10.1159/000447836
pubmed: 27606810
Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy: a World Health Organization Guideline (2014) Diabetes Research and Clinical Practice. 103(3):341–363. https://doi.org/10.1016/j.diabres.2013.10.012 (PMID: 24847517)
Wang Q, Sun L, Yan J, Wang S, Zhang J, Zheng X (2017) Expression of vascular endothelial growth factor and caspase-3 in mucinous breast carcinoma and infiltrating ductal carcinoma-not otherwise specified, and the correlation with disease-free survival. Oncol Lett 14:4890–4896
doi: 10.3892/ol.2017.6744
pubmed: 29085497
pmcid: 5649581
Bursac Z, Gauss CH, Williams DK et al (2008) Purposeful selection of variables in logistic regression. Source Code Biol Med 3:17. https://doi.org/10.1186/1751-0473-3-17
doi: 10.1186/1751-0473-3-17
pubmed: 19087314
pmcid: 2633005
Highman TJ, Friedman JE, Huston LP, Wong WW, Catalano PM (1998) Longitudinal changes in maternal serum leptin concentrations, body composition, and resting metabolic rate in pregnancy. Am J Obstet Gynecol 178(5):1010–1015. https://doi.org/10.1016/s0002-9378(98)70540-x (PMID: 9609576)
doi: 10.1016/s0002-9378(98)70540-x
pubmed: 9609576
Brelje TC, Scharp DW, Lacy PE, Ogren L, Talamantes F, Robertson M, Friesen HG, Sorenson RL (1993) Effect of homologous placental lactogens, prolactins, and growth hormones on islet B-cell division and insulin secretion in rat, mouse, and human islets: implication for placental lactogen regulation of islet function during pregnancy. Endocrinology 132(2):879–887. https://doi.org/10.1210/endo.132.2.8425500 (PMID: 8425500)
doi: 10.1210/endo.132.2.8425500
pubmed: 8425500
Rieck S, Kaestner KH (2010) Expansion of beta-cell mass in response to pregnancy. Trends Endocrinol Metab 21(3):151–158. https://doi.org/10.1016/j.tem.2009.11.001 (Epub 2009 Dec 16. PMID: 20015659; PMCID: PMC3627215)
doi: 10.1016/j.tem.2009.11.001
pubmed: 20015659
Ashcroft FM, Rohm M, Clark A, Brereton MF (2017) Is type 2 diabetes a glycogen storage disease of pancreatic β cells? Cell Metab 26(1):17–23. https://doi.org/10.1016/j.cmet.2017.05.014 (PMID: 28683284; PMCID: PMC5890904)
doi: 10.1016/j.cmet.2017.05.014
pubmed: 28683284
pmcid: 5890904
Khambule L, George JA (2019) The Role of inflammation in the development of GDM and the use of markers of inflammation in GDM screening. Adv Exp Med Biol 1134:217–242. https://doi.org/10.1007/978-3-030-12668-1_12 (PMID: 30919340)
doi: 10.1007/978-3-030-12668-1_12
pubmed: 30919340
Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N (2014) Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract 105(2):141–150. https://doi.org/10.1016/j.diabres.2014.04.006 (Epub 2014 Apr 13. PMID: 24798950)
doi: 10.1016/j.diabres.2014.04.006
pubmed: 24798950
Lawrence T (2009) The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 1(6):a001651. https://doi.org/10.1101/cshperspect.a001651 (PMID: 20457564; PMCID: PMC2882124)
doi: 10.1101/cshperspect.a001651
pubmed: 20457564
pmcid: 2882124
Stephens JM, Lee J, Pilch PF (1997) Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J Biol Chem 272(2):971–976. https://doi.org/10.1074/jbc.272.2.971 (PMID: 8995390)
doi: 10.1074/jbc.272.2.971
pubmed: 8995390
Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM (1994) Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci USA 91(11):4854–4858. https://doi.org/10.1073/pnas.91.11.4854 (PMID: 8197147; PMCID: PMC43887)
doi: 10.1073/pnas.91.11.4854
pubmed: 8197147
pmcid: 43887
Kinalski M, Telejko B, Kuźmicki M, Kretowski A, Kinalska I (2005) Tumor necrosis factor alpha system and plasma adiponectin concentration in women with gestational diabetes. Horm Metab Res 37(7):450–454. https://doi.org/10.1055/s-2005-870238 (PMID: 16034719)
doi: 10.1055/s-2005-870238
pubmed: 16034719
Huynh J, Dawson D, Roberts D, Bentley-Lewis R (2015) A systematic review of placental pathology in maternal diabetes mellitus. Placenta 36(2):101–114. https://doi.org/10.1016/j.placenta.2014.11.021 (Epub 2014 Dec 5. PMID: 25524060; PMCID: PMC4339292)
doi: 10.1016/j.placenta.2014.11.021
pubmed: 25524060
Fadini GP, Albiero M, Bonora BM, Avogaro A (2019) Angiogenic abnormalities in diabetes mellitus: mechanistic and clinical aspects. J Clin Endocrinol Metab 104(11):5431–5444. https://doi.org/10.1210/jc.2019-00980 (PMID: 31211371)
doi: 10.1210/jc.2019-00980
pubmed: 31211371
Djelmiš J, Desoye G, Ivaniševic M (eds) (2005) Diabetology of pregnancy. Front Diabetes. 17:110–126 https://doi.org/10.1159/000087407
Thangarajah H, Vial IN, Grogan RH, Yao D, Shi Y, Januszyk M, Galiano RD, Chang EI, Galvez MG, Glotzbach JP, Wong VW, Brownlee M, Gurtner GC (2010) HIF-1a dysfunction in diabetes. Cell Cycle 9(1):75–79
doi: 10.4161/cc.9.1.10371
pubmed: 20016290
Venneri MA, Barbagallo F, Fiore D, De Gaetano R, Giannetta E, Sbardella E, Pozza C, Campolo F, Naro F, Lenzi A, Isidori AM (2019) PDE5 inhibition stimulates Tie2-expressing monocytes and angiopoietin-1 restoring angiogenic homeostasis in diabetes. J Clin Endocrinol Metab 104(7):2623–2636
doi: 10.1210/jc.2018-02525
pubmed: 31102457
Okamoto T, Tanaka S, Stan AC, Koike T, Kase M, Makita Z, Sawa H, Nagashima K (2002) Advanced glycation end products induce angiogenesis in vivo. Microvasc Res 63:186–195
doi: 10.1006/mvre.2001.2371
pubmed: 11866542
Hellström M, Gerhardt H, Kalén M, Li X, Eriksson U, Wolburg H, Betsholtz C (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153:543–553
doi: 10.1083/jcb.153.3.543
pubmed: 11331305
pmcid: 2190573
Warmke N, Griffin KJ, Cubbon RM (2016) Pericytes in diabetes associated vascular disease. J Diabetes Complications 30(8):1643–1650
doi: 10.1016/j.jdiacomp.2016.08.005
pubmed: 27592245
Davis LE, Widness JA, Brace RA (2003) Renal and placental secretion of erythropoietin during anemia or hypoxia in the ovine fetus. Am J Obstet Gynecol 189:1764–1770
doi: 10.1016/S0002-9378(03)00874-3
pubmed: 14710111
Benyo DF, Conrad KP (1999) Expression of the erythropoietin receptor by trophoblast cells in the human placenta. Biol Reprod 60:861–870
doi: 10.1095/biolreprod60.4.861
Kim SY, Sappenfield W, Sharma AJ, Wilson HG, Bish CL, Salihu HM, England LJ (2013) Racial/ethnic differences in the prevalence of gestational diabetes mellitus and maternal overweight and obesity, by nativity, Florida, 2004–2007. Obesity (Silver Spring) 21(1):E33-40. https://doi.org/10.1002/oby.20025 (PMID: 23404915; PMCID: PMC4392762)
doi: 10.1002/oby.20025
pubmed: 23404915
Grieger JA, Leemaqz SY, Knight EJ et al (2022) Relative importance of metabolic syndrome components for developing gestational diabetes. Arch Gynecol Obstet 305:995–1002. https://doi.org/10.1007/s00404-021-06279-1
doi: 10.1007/s00404-021-06279-1
pubmed: 34655325
Xi F, Chen H, Chen Q et al (2021) Second-trimester and third-trimester maternal lipid profiles significantly correlated to LGA and macrosomia. Arch Gynecol Obstet 304:885–894. https://doi.org/10.1007/s00404-021-06010-0
doi: 10.1007/s00404-021-06010-0
pubmed: 33651156
Yoles I, Sheiner E, Wainstock T (2021) First pregnancy risk factors and future gestational diabetes mellitus. Arch Gynecol Obstet 304:929–934. https://doi.org/10.1007/s00404-021-06024-8
doi: 10.1007/s00404-021-06024-8
pubmed: 33811260
López-Tinoco C, Roca M, Fernández-Deudero A, García-Valero A, Bugatto F, Aguilar-Diosdado M, Bartha JL (2012) Cytokine profile, metabolic syndrome and cardiovascular disease risk in women with late-onset gestational diabetes mellitus. Cytokine 58(1):14–19. https://doi.org/10.1016/j.cyto.2011.12.004 (Epub 2011 Dec 24. PMID: 22200508)
doi: 10.1016/j.cyto.2011.12.004
pubmed: 22200508
Richardson AC, Carpenter MW (2007) Inflammatory mediators in gestational diabetes mellitus. Obstet Gynecol Clin North Am 34(2):213–224. https://doi.org/10.1016/j.ogc.2007.04.001 (PMID: 17572268)
doi: 10.1016/j.ogc.2007.04.001
pubmed: 17572268
Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112(12):1796–1808. https://doi.org/10.1172/JCI19246 (PMID: 14679176; PMCID: PMC296995)
doi: 10.1172/JCI19246
pubmed: 14679176
pmcid: 296995
Gregor MF, Hotamisligil GS (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29:415–445. https://doi.org/10.1146/annurev-immunol-031210-101322 (PMID: 21219177)
doi: 10.1146/annurev-immunol-031210-101322
pubmed: 21219177
Bergmann K, Sypniewska G (2013) Diabetes as a complication of adipose tissue dysfunction. Is there a role for potential new biomarkers? Clin Chem Lab Med 51(1):177–185. https://doi.org/10.1515/cclm-2012-0490 (PMID: 23241684)
doi: 10.1515/cclm-2012-0490
pubmed: 23241684
Dubova EA, Pavlov KA, Borovkova EI, Bayramova MA, Makarov IO, Shchegolev AI (2011) Vascular endothelial growth factor and its receptors in the placenta of pregnant women with obesity. Bull Exp Biol Med 151(2):253–258. https://doi.org/10.1007/s10517-011-1302-3 (PMID: 22238763.51)
doi: 10.1007/s10517-011-1302-3
pubmed: 22238763
Yi QY, Deng G, Chen N et al (2016) Metformin inhibits development of diabetic retinopathy through inducing alternative splicing of VEGF-A. Am J Transl Res 8(9):3947–3954
pubmed: 27725874
pmcid: 5040692
Joe SG, Yoon YH, Choi JA, Koh J-Y (2015) Anti-angiogenic effect of metformin in mouse oxygen-induced retinopathy is mediated by reducing levels of the vascular endothelial growth factor receptor Flk-1. PLoS ONE 10(3):e0119708. https://doi.org/10.1371/journal.pone.0119708
doi: 10.1371/journal.pone.0119708
pubmed: 25785990
pmcid: 4364739
Zhang K, Han ES, Dellinger TH, Lu J, Nam S, Anderson RA, Yim JH, Wen W (2017) Cinnamon extract reduces VEGF expression via suppressing HIF-1α gene expression and inhibits tumor growth in mice. Mol Carcinog 56(2):436–446. https://doi.org/10.1002/mc.22506
doi: 10.1002/mc.22506
pubmed: 27253180
Hosni A, El-Twab SA, Abdul-Hamid M, Prinsen E, AbdElgawad H, Abdel-Moneim A, Beemster GTS (2021) Cinnamaldehyde mitigates placental vascular dysfunction of gestational diabetes and protects from the associated fetal hypoxia by modulating placental angiogenesis, metabolic activity and oxidative stress. Pharmacol Res 165:105426. https://doi.org/10.1016/j.phrs.2021.105426
doi: 10.1016/j.phrs.2021.105426
pubmed: 33453370