The relationship between differential placental protein expressions and insulin resistance: a systematic review and meta-analysis_West China Medical Journal

Authors：

HUANG Pingping ¹ , GE Li ¹ ,  MIAO Haiyan ² , WANG Guandong ¹ , LAI Yuting ¹ , JIANG Xinyong ¹ , CHEN Fan ¹ , PANG Shuqin ¹ , YU Honghong ¹

1. School of Nursing, Fujian University of Traditional Chinese Medicine, Fuzhou, Fujian 350122, P. R. China;
2. Department of Obstetrics and Gynecology, the Second People’s Hospital Affiliated to Fujian University of Traditional Chinese Medicine, Fuzhou, Fujian 350003, P. R. China;

Corresponding author：

MIAO Haiyan, Email: 573764301@qq.com

Keywords：

Gestational diabetes mellitus; Placenta; Placental protein; Insulin resistance; Systematic review

DOI：

10.7507/1002-0179.201911079

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To systematically evaluate the changes in placental protein expressions in gestational diabetes mellitus (GDM) and their correlations with maternal insulin resistance (IR). Methods PubMed, Cochrane Library, Scopus, Web of Science, Embase, China National Knowledge Infrastructure, VIP database, Wanfang Database and CBMdisc were searched for case-control studies published from January 2009 to November 2021, which reported the placental protein expressions in GDM and their correlations with IR. Two researchers independently reviewed the literature, extracted data and evaluated the literature quality. RevMan 5.4 software was used for meta-analysis, and descriptive analysis was performed on data that cannot be combined. Results A total of 19 studies were included, comprising 2 012 patients. The results of meta-analysis showed that: the expression level of retinol binding protein 4 (RBP4) [standard mean difference=2.11, 95% confidence interval (CI) (1.64, 2.58), P<0.000 01] and the positive rate of protein tyrosine phosphatase-1B (PTP1B) [relative risk (RR)=1.56, 95%CI (1.29, 1.88), P<0.000 01] were up-regulated, and the positive rate of insulin receptor substrate 1 (IRS-1) [RR=0.69, 95%CI (0.60, 0.78), P<0.000 01] was down-regulated. The protein expression levels of RBP4 (P<0.000 01) and PTP1B (P<0.000 01) were positively correlated with homeostasis model assessment of insulin resistance (HOMA-IR), while the protein expression levels of IRS-1 (P<0.000 01) and APN (P=0.002) were negatively correlated with HOMA-IR, and glucose transporter 4 (GLUT 4) was not correlated with HOMA-IR (P=0.79). Descriptive analysis found that the expression levels or positive rates of adipocytokines (leptin, resistin), oxidative stress markers (xanthione oxidase, malondialdehyde, 8-isoprostaglandin),inflammatory factors (tumor necrosis factor α, Toll-like receptor 4, Galectin-3, Galectin-2, migration inhibitory factor),fetuin-A, forkhead box transcription factor 1, forkhead box transcription factor 3a and estrogen receptor α in GDM placenta were up-regulated and all were positively correlated with HOMA-IR. The expression levels or positive rates of insulin signaling pathway proteins [phosphoinositide 3-kinase (PI3K), protein kinases B (AKT), phospho-protein kinases B (p-AKT), GLUT 4] were down-regulated, PI3K and AKT were negatively correlatedwith HOMA-IR, while p-Akt had no correlation with HOMA-IR. Conclusions The dysregulation of placental protein expressions may mediate maternal IR exacerbation, thus promote the occurrence and development of GDM and other pregnancy complications. The causal relationship and regulatory mechanism are still unclear, which need to be further studied.

Citation： HUANG Pingping, GE Li, MIAO Haiyan, WANG Guandong, LAI Yuting, JIANG Xinyong, CHEN Fan, PANG Shuqin, YU Honghong. The relationship between differential placental protein expressions and insulin resistance: a systematic review and meta-analysis. West China Medical Journal, 2021, 36(12): 1705-1715. doi: 10.7507/1002-0179.201911079 Copy

1.	Nguyen-Ngo C, Jayabalan N, Salomon C, et al. Molecular pathways disrupted by gestational diabetes mellitus. J Mol Endocrinol, 2019, 63(3): R51-R72.
2.	Powe CE. Early pregnancy biochemical predictors of gestational diabetes mellitus. Curr Diab Rep, 2017, 17(2): 12.
3.	Liang Z, Zhou M, Xu XK, et al. Is chemerin associated with gestational diabetes mellitus? An evidence-based clinical research from Chinese women. J Obstet Gynaecol, 2018, 38(4): 482-487.
4.	Wedekind L, Belkacemi L. Altered cytokine network in gestational diabetes mellitus affects maternal insulin and placental-fetal development. J Diabetes Complications, 2016, 30(7): 1393-1400.
5.	Xu Y, Jin B, Sun L, et al. The expression of FoxO1 in placenta and omental adipose tissue of gestational diabetes mellitus. Exp Clin Endocrinol Diabetes, 2014, 122(5): 287-294.
6.	张凌燕, 张晓姗, 折开娥, 等. 妊娠期糖尿病孕妇血清和胎盘组织中 FOXO3a 的表达水平及其与胰岛素抵抗的关系. 中国妇幼保健, 2018, 33(19): 4405-4408.
7.	高秀秀, 甘旭培, 徐先明. 妊娠期糖尿病孕妇胎盘中视黄醇结合蛋白 4 表达与胰岛素抵抗和胰岛素分泌功能的相关性. 现代妇产科进展, 2016, 25(10): 750-753.
8.	Liu B, Xu Y, Voss C, et al. Altered protein expression in gestational diabetes mellitus placentas provides insight into insulin resistance and coagulation/fibrinolysis pathways. PLoS One, 2012, 7(9): e44701.
9.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
10.	Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions (Version 5.1. 0). (2011-03-20)[2019-11-01]. http://handbook-5-1.cochrane.org/.
11.	葛芳君, 赵磊, 刘俊, 等. 基于 Pearson 相关系数的老年人社会支持与心理健康相关性研究的 Meta 分析. 中国循证医学杂志, 2012, 12(11): 1320-1329.
12.	Tsiligianni I, Kocks J, Tzanakis N, et al. Factors that influence disease-specific quality of life or health status in patients with COPD: a review and meta-analysis of Pearson correlations. Prim Care Respir J, 2011, 20(3): 257-268.
13.	夏雨果, 陈秋, 汤志梅, 等. 氧化应激产物 MDA 与生育力和精子参数相关性的 Meta 分析. 海南医学, 2018, 29(9): 1316-1320.
14.	曾丽, 王佳琳, 左敏, 等. 中国老年人睡眠质量与社会支持相关性的 Meta 分析. 中国循证医学杂志, 2021, 21(4): 401-406.
15.	李凡, 王如萍, 况雪静, 等. 胎盘组织中 GLUT4、RBP4 表达与妊娠糖尿病发病的关系. 临床和实验医学杂志, 2020, 19(12): 1319-1322.
16.	郭永, 付竹梅. 妊娠期糖尿病孕妇中视黄醇结合蛋白 4 的表达与胰岛素抵抗的关系. 潍坊医学院学报, 2017, 39(2): 108-110.
17.	任宏珍. 妊娠期糖尿病产妇胎盘组织中蛋白酪氨酸磷酸酶 1B 的表达及其与胰岛素抵抗和炎症应激的相关性. 中国妇幼保健, 2018, 33(16): 3679-3683.
18.	王丽娜, 崔文华, 梁珊, 等. 妊娠期糖尿病患者胎盘组织胰岛素受体底物 1、蛋白酪氨酸磷酸酶 1B 表达及意义. 山东医药, 2015, 55(40): 56-58.
19.	高晓丽. 蛋白酪氨酸磷酸酶 1B 与妊娠期糖尿病的相关性研究. 天津: 天津医科大学, 2010.
20.	冯卫红, 王艳霞, 计静, 等. IRS-1 和 GLUT4 在妊娠期糖尿病患者胎盘组织中的表达水平及其临床意义. 中国妇产科临床杂志, 2020, 21(3): 251-253.
21.	马宗丽, 秦智娟, 肖黎明, 等. 妊娠期糖尿病产妇胎盘组织中 TLR4/MyD88/NF-κB 的表达及其与胰岛素抵抗的相关性. 中国临床研究, 2020, 33(12): 1620-1623.
22.	禤文婷, 陈丽霞, 黎美金, 等. Galectin-2 在妊娠期糖尿病患者中的表达及其与胰岛素抵抗的关系. 医学信息, 2020, 33(16): 72-74.
23.	杨云萍, 刘春玲. 半乳糖凝集素 3 在妊娠期糖尿病孕妇中表达及与胰岛素抵抗关系. 中国计划生育学杂志, 2019, 27(1): 77-79, 83.
24.	郑林, 李超, 齐卫红, 等. 巨噬细胞移动抑制因子基因在胎盘组织中表达与妊娠期糖尿病的相关性. 中华医学杂志, 2017, 97(43): 3388-3391.
25.	李华珍, 袁俏奇, 罗利, 等. 妊娠期糖尿病产妇胎盘与血清脂联素水平的相关性. 中南医学科学杂志, 2016, 44(3): 255-257.
26.	左婵. 探讨脂联素在妊娠期糖尿病发病机制中的相关作用. 湛江: 广东医学院, 2012.
27.	李明. PI3K/AKT 信号通路与妊娠期糖尿病胰岛素抵抗的关系. 天津: 天津医科大学, 2010.
28.	曹聪明, 丁红涛, 李妙荣. 妊娠期糖尿病患者胎盘组织中胎球蛋白 A 的表达及其与胰岛素抵抗的关系. 中国医师进修杂志, 2014, 37(27): 7-9.
29.	周玉彬, 李超, 乔炳龙, 等. 妊娠期糖尿病患者胎盘组织中雌激素与雌激素受体α水平变化及相关因素分析. 中华糖尿病杂志, 2017, 9(11): 688-692.
30.	Shang M, Dong X, Hou L. Correlation of adipokines and markers of oxidative stress in women with gestational diabetes mellitus and their newborns. J Obstet Gynaecol Res, 2018, 44(4): 637-646.
31.	Johns EC, Denison FC, Norman JE, et al. Gestational diabetes mellitus: mechanisms, treatment, and complications. Trends in Endocrinol Metab, 2018, 29(11): 743-754.
32.	Koning SH, Hoogenberg K, Lutgers HL, et al. Gestational diabetes mellitus: current knowledge and unmet needs. J Diabetes, 2016, 8(6): 770-781.
33.	Feng H, Su R, Song Y, et al. Positive correlation between enhanced expression of TLR4/MyD88/NF-κB with insulin resistance in placentae of gestational diabetes mellitus. PloS one, 2016, 11(6): e0157185.
34.	Plows JF, Stanley JL, Baker PN, et al. The pathophysiology of gestational diabetes mellitus. Int J Mol Sci, 2018, 19(11): 3342.
35.	Low Birth Weight and Nephron Number Working Group. The impact of kidney development on the life course: a consensus document for action. Nephron, 2017, 136(1): 3-49.
36.	Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest, 2005, 115(5): 1111-1119.
37.	Liang ZX, Du MK, Fang Q, et al. Significance of RBP4 in patients with gestational diabetes mellitus: a case-control study of Han Chinese women. Gynecol Endocrinol, 2014, 30(2): 161-164.
38.	刘嗣超, 刘星. PAI-1、GLUT1 及 RBP4 在妊娠期糖尿病患者胎盘组织中的表达及临床意义. 中国妇幼保健, 2019, 34(19): 4430-4433.
39.	Pérez-Pérez A, Maymó J, Gambino Y, et al. Insulin enhances leptin expression in human trophoblastic cells. Biol Reprod, 2013, 89(1): 20.
40.	Pérez-Pérez A, Guadix P, Maymó J, et al. Insulin and leptin signaling in placenta from gestational diabetic subjects. Horm Metab Res, 2016, 48(1): 62-69.
41.	Hu S, Liu Q, Huang X, et al. Serum level and polymorphisms of retinol-binding protein-4 and risk for gestational diabetes mellitus: a meta-analysis. BMC Pregnancy Childbirth, 2016, 16: 52.
42.	Sudharshana Murthy KA, Bhandiwada A, Chandan SL, et al. Evaluation of oxidative stress and proinflammatory cytokines in gestational diabetes mellitus and their correlation with pregnancy outcome. Indian J Endocrinol Metab, 2018, 22(1): 79-84.
43.	Tabák AG, Carstensen M, Witte DR, et al. Adiponectin trajectories before type 2 diabetes diagnosis: WhitehallⅡstudy. Diabetes Care, 2012, 35(12): 2540-2547.
44.	Siddiqui K, George TP, Nawaz SS, et al. Serum adipokines (adiponectin and resistin) correlation in developing gestational diabetes mellitus: pilot study. Gynecol Endocrinol, 2018, 34(6): 502-506.
45.	Asemi Z, Jazayeri S, Najafi M, et al. Association between markers of systemic inflammation, oxidative stress, lipid profiles, and insulin resistance in pregnant women. ARYA Atheroscler, 2013, 9(3): 172-178.
46.	Kirwan JP, Hauguel-De Mouzon S, Lepercq J, et al. TNF-alpha is a predictor of insulin resistance in human pregnancy. Diabetes, 2002, 51(7): 2207-2213.
47.	Xu J, Zhao YH, Chen YP, et al. Maternal circulating concentrations of tumor necrosis factor-alpha, leptin, and adiponectin in gestational diabetes mellitus: a systematic review and meta-analysis. Sci World J, 2014, 2014: 926932.
48.	赵莉莉, 杨筱青. 妊娠期糖尿病 TNF-α与 VCAM-1 的表达及相关性研究. 医学研究杂志, 2019, 48(4): 78-82.
49.	Khambule L, George JA. The role of inflammation in the development of GDM and the use of markers of inflammation in GDM screening. Adv Exp Med Biol, 2019, 1134: 217-242.
50.	杨娟, 佘美华. FoxO1 在 2 型糖尿病中的作用及其研究进展. 中南医学科学杂志, 2017, 45(3): 307-311.
51.	侯少聪, 李平平. 半乳糖苷凝集素 Galectin3 直接诱发胰岛素抵抗. 中国细胞生物学学报, 2017, 39(5): 537-541.
52.	Hepp P, Unverdorben L, Hutter S, et al. Placental galectin-2 expression in gestational diabetes: a systematic, histological analysis. Int J Mol Sci, 2020, 21(7): 2404.
53.	冯慧, 马京梅, 杨慧霞. 妊娠期糖尿病孕妇足月胎盘 Toll 样受体 4 的表达分布. 中华围产医学杂志, 2016, 19(5): 350-354.
54.	王运林, 姚培伟, 张晓婷. 炎性因子 hs-CRP、MIF 和 RANTES 在不同糖代谢人群中的表达及其与胰岛素抵抗的关系. 广东医学, 2015, 36(12): 1897-1899.
55.	李高振, 宋晓燕. 巨噬细胞移动抑制因子及肿瘤坏死因子-α在妊娠期糖尿病临床诊断中的应用价值. 实用临床医药杂志, 2017, 21(23): 86-87.
56.	Shang M, Zhao J, Yang L, et al. Oxidative stress and antioxidant status in women with gestational diabetes mellitus diagnosed by IADPSG criteria. Diabetes Res Clin Pract, 2015, 109(2): 404-410.
57.	张亚楠, 陈保民, 高阳, 等. FoxO3a 转录因子与机体氧化应激损伤的研究进展. 医学研究生学报, 2016, 29(3): 327-331.
58.	杨猛, 高天虹. 蛋白酪氨酸磷酸酶 1B (PTP1B) 抑制剂的研究进展. 河南化工, 2015, 32(1): 11-15.
59.	Akbas H, Kahraman S, Sak S, et al. Minor variant of AHSG gene 767C> G polymorphism may decrease the risk of gestational diabetes mellitus. J Obstet Gynaecol, 2020, 40(3): 303-307.
60.	王雨艳, 黄达, 沈秀敏, 等. 雌激素受体和孕激素受体在妊娠期高血压疾病胎盘组织中的表达. 解剖科学进展, 2015, 21(6): 621-623.
61.	Barros RP, Morani A, Moriscot A, et al. Insulin resistance of pregnancy involves estrogen-induced repression of muscle GLUT4. Mol Cell Endocrinol, 2008, 295(1/2): 24-31.

1. Nguyen-Ngo C, Jayabalan N, Salomon C, et al. Molecular pathways disrupted by gestational diabetes mellitus. J Mol Endocrinol, 2019, 63(3): R51-R72.
2. Powe CE. Early pregnancy biochemical predictors of gestational diabetes mellitus. Curr Diab Rep, 2017, 17(2): 12.
3. Liang Z, Zhou M, Xu XK, et al. Is chemerin associated with gestational diabetes mellitus? An evidence-based clinical research from Chinese women. J Obstet Gynaecol, 2018, 38(4): 482-487.
4. Wedekind L, Belkacemi L. Altered cytokine network in gestational diabetes mellitus affects maternal insulin and placental-fetal development. J Diabetes Complications, 2016, 30(7): 1393-1400.
5. Xu Y, Jin B, Sun L, et al. The expression of FoxO1 in placenta and omental adipose tissue of gestational diabetes mellitus. Exp Clin Endocrinol Diabetes, 2014, 122(5): 287-294.
6. 张凌燕, 张晓姗, 折开娥, 等. 妊娠期糖尿病孕妇血清和胎盘组织中 FOXO3a 的表达水平及其与胰岛素抵抗的关系. 中国妇幼保健, 2018, 33(19): 4405-4408.
7. 高秀秀, 甘旭培, 徐先明. 妊娠期糖尿病孕妇胎盘中视黄醇结合蛋白 4 表达与胰岛素抵抗和胰岛素分泌功能的相关性. 现代妇产科进展, 2016, 25(10): 750-753.
8. Liu B, Xu Y, Voss C, et al. Altered protein expression in gestational diabetes mellitus placentas provides insight into insulin resistance and coagulation/fibrinolysis pathways. PLoS One, 2012, 7(9): e44701.
9. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
10. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions (Version 5.1. 0). (2011-03-20)[2019-11-01]. http://handbook-5-1.cochrane.org/.
11. 葛芳君, 赵磊, 刘俊, 等. 基于 Pearson 相关系数的老年人社会支持与心理健康相关性研究的 Meta 分析. 中国循证医学杂志, 2012, 12(11): 1320-1329.
12. Tsiligianni I, Kocks J, Tzanakis N, et al. Factors that influence disease-specific quality of life or health status in patients with COPD: a review and meta-analysis of Pearson correlations. Prim Care Respir J, 2011, 20(3): 257-268.
13. 夏雨果, 陈秋, 汤志梅, 等. 氧化应激产物 MDA 与生育力和精子参数相关性的 Meta 分析. 海南医学, 2018, 29(9): 1316-1320.
14. 曾丽, 王佳琳, 左敏, 等. 中国老年人睡眠质量与社会支持相关性的 Meta 分析. 中国循证医学杂志, 2021, 21(4): 401-406.
15. 李凡, 王如萍, 况雪静, 等. 胎盘组织中 GLUT4、RBP4 表达与妊娠糖尿病发病的关系. 临床和实验医学杂志, 2020, 19(12): 1319-1322.
16. 郭永, 付竹梅. 妊娠期糖尿病孕妇中视黄醇结合蛋白 4 的表达与胰岛素抵抗的关系. 潍坊医学院学报, 2017, 39(2): 108-110.
17. 任宏珍. 妊娠期糖尿病产妇胎盘组织中蛋白酪氨酸磷酸酶 1B 的表达及其与胰岛素抵抗和炎症应激的相关性. 中国妇幼保健, 2018, 33(16): 3679-3683.
18. 王丽娜, 崔文华, 梁珊, 等. 妊娠期糖尿病患者胎盘组织胰岛素受体底物 1、蛋白酪氨酸磷酸酶 1B 表达及意义. 山东医药, 2015, 55(40): 56-58.
19. 高晓丽. 蛋白酪氨酸磷酸酶 1B 与妊娠期糖尿病的相关性研究. 天津: 天津医科大学, 2010.
20. 冯卫红, 王艳霞, 计静, 等. IRS-1 和 GLUT4 在妊娠期糖尿病患者胎盘组织中的表达水平及其临床意义. 中国妇产科临床杂志, 2020, 21(3): 251-253.
21. 马宗丽, 秦智娟, 肖黎明, 等. 妊娠期糖尿病产妇胎盘组织中 TLR4/MyD88/NF-κB 的表达及其与胰岛素抵抗的相关性. 中国临床研究, 2020, 33(12): 1620-1623.
22. 禤文婷, 陈丽霞, 黎美金, 等. Galectin-2 在妊娠期糖尿病患者中的表达及其与胰岛素抵抗的关系. 医学信息, 2020, 33(16): 72-74.
23. 杨云萍, 刘春玲. 半乳糖凝集素 3 在妊娠期糖尿病孕妇中表达及与胰岛素抵抗关系. 中国计划生育学杂志, 2019, 27(1): 77-79, 83.
24. 郑林, 李超, 齐卫红, 等. 巨噬细胞移动抑制因子基因在胎盘组织中表达与妊娠期糖尿病的相关性. 中华医学杂志, 2017, 97(43): 3388-3391.
25. 李华珍, 袁俏奇, 罗利, 等. 妊娠期糖尿病产妇胎盘与血清脂联素水平的相关性. 中南医学科学杂志, 2016, 44(3): 255-257.
26. 左婵. 探讨脂联素在妊娠期糖尿病发病机制中的相关作用. 湛江: 广东医学院, 2012.
27. 李明. PI3K/AKT 信号通路与妊娠期糖尿病胰岛素抵抗的关系. 天津: 天津医科大学, 2010.
28. 曹聪明, 丁红涛, 李妙荣. 妊娠期糖尿病患者胎盘组织中胎球蛋白 A 的表达及其与胰岛素抵抗的关系. 中国医师进修杂志, 2014, 37(27): 7-9.
29. 周玉彬, 李超, 乔炳龙, 等. 妊娠期糖尿病患者胎盘组织中雌激素与雌激素受体α水平变化及相关因素分析. 中华糖尿病杂志, 2017, 9(11): 688-692.
30. Shang M, Dong X, Hou L. Correlation of adipokines and markers of oxidative stress in women with gestational diabetes mellitus and their newborns. J Obstet Gynaecol Res, 2018, 44(4): 637-646.
31. Johns EC, Denison FC, Norman JE, et al. Gestational diabetes mellitus: mechanisms, treatment, and complications. Trends in Endocrinol Metab, 2018, 29(11): 743-754.
32. Koning SH, Hoogenberg K, Lutgers HL, et al. Gestational diabetes mellitus: current knowledge and unmet needs. J Diabetes, 2016, 8(6): 770-781.
33. Feng H, Su R, Song Y, et al. Positive correlation between enhanced expression of TLR4/MyD88/NF-κB with insulin resistance in placentae of gestational diabetes mellitus. PloS one, 2016, 11(6): e0157185.
34. Plows JF, Stanley JL, Baker PN, et al. The pathophysiology of gestational diabetes mellitus. Int J Mol Sci, 2018, 19(11): 3342.
35. Low Birth Weight and Nephron Number Working Group. The impact of kidney development on the life course: a consensus document for action. Nephron, 2017, 136(1): 3-49.
36. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest, 2005, 115(5): 1111-1119.
37. Liang ZX, Du MK, Fang Q, et al. Significance of RBP4 in patients with gestational diabetes mellitus: a case-control study of Han Chinese women. Gynecol Endocrinol, 2014, 30(2): 161-164.
38. 刘嗣超, 刘星. PAI-1、GLUT1 及 RBP4 在妊娠期糖尿病患者胎盘组织中的表达及临床意义. 中国妇幼保健, 2019, 34(19): 4430-4433.
39. Pérez-Pérez A, Maymó J, Gambino Y, et al. Insulin enhances leptin expression in human trophoblastic cells. Biol Reprod, 2013, 89(1): 20.
40. Pérez-Pérez A, Guadix P, Maymó J, et al. Insulin and leptin signaling in placenta from gestational diabetic subjects. Horm Metab Res, 2016, 48(1): 62-69.
41. Hu S, Liu Q, Huang X, et al. Serum level and polymorphisms of retinol-binding protein-4 and risk for gestational diabetes mellitus: a meta-analysis. BMC Pregnancy Childbirth, 2016, 16: 52.
42. Sudharshana Murthy KA, Bhandiwada A, Chandan SL, et al. Evaluation of oxidative stress and proinflammatory cytokines in gestational diabetes mellitus and their correlation with pregnancy outcome. Indian J Endocrinol Metab, 2018, 22(1): 79-84.
43. Tabák AG, Carstensen M, Witte DR, et al. Adiponectin trajectories before type 2 diabetes diagnosis: WhitehallⅡstudy. Diabetes Care, 2012, 35(12): 2540-2547.
44. Siddiqui K, George TP, Nawaz SS, et al. Serum adipokines (adiponectin and resistin) correlation in developing gestational diabetes mellitus: pilot study. Gynecol Endocrinol, 2018, 34(6): 502-506.
45. Asemi Z, Jazayeri S, Najafi M, et al. Association between markers of systemic inflammation, oxidative stress, lipid profiles, and insulin resistance in pregnant women. ARYA Atheroscler, 2013, 9(3): 172-178.
46. Kirwan JP, Hauguel-De Mouzon S, Lepercq J, et al. TNF-alpha is a predictor of insulin resistance in human pregnancy. Diabetes, 2002, 51(7): 2207-2213.
47. Xu J, Zhao YH, Chen YP, et al. Maternal circulating concentrations of tumor necrosis factor-alpha, leptin, and adiponectin in gestational diabetes mellitus: a systematic review and meta-analysis. Sci World J, 2014, 2014: 926932.
48. 赵莉莉, 杨筱青. 妊娠期糖尿病 TNF-α与 VCAM-1 的表达及相关性研究. 医学研究杂志, 2019, 48(4): 78-82.
49. Khambule L, George JA. The role of inflammation in the development of GDM and the use of markers of inflammation in GDM screening. Adv Exp Med Biol, 2019, 1134: 217-242.
50. 杨娟, 佘美华. FoxO1 在 2 型糖尿病中的作用及其研究进展. 中南医学科学杂志, 2017, 45(3): 307-311.
51. 侯少聪, 李平平. 半乳糖苷凝集素 Galectin3 直接诱发胰岛素抵抗. 中国细胞生物学学报, 2017, 39(5): 537-541.
52. Hepp P, Unverdorben L, Hutter S, et al. Placental galectin-2 expression in gestational diabetes: a systematic, histological analysis. Int J Mol Sci, 2020, 21(7): 2404.
53. 冯慧, 马京梅, 杨慧霞. 妊娠期糖尿病孕妇足月胎盘 Toll 样受体 4 的表达分布. 中华围产医学杂志, 2016, 19(5): 350-354.
54. 王运林, 姚培伟, 张晓婷. 炎性因子 hs-CRP、MIF 和 RANTES 在不同糖代谢人群中的表达及其与胰岛素抵抗的关系. 广东医学, 2015, 36(12): 1897-1899.
55. 李高振, 宋晓燕. 巨噬细胞移动抑制因子及肿瘤坏死因子-α在妊娠期糖尿病临床诊断中的应用价值. 实用临床医药杂志, 2017, 21(23): 86-87.
56. Shang M, Zhao J, Yang L, et al. Oxidative stress and antioxidant status in women with gestational diabetes mellitus diagnosed by IADPSG criteria. Diabetes Res Clin Pract, 2015, 109(2): 404-410.
57. 张亚楠, 陈保民, 高阳, 等. FoxO3a 转录因子与机体氧化应激损伤的研究进展. 医学研究生学报, 2016, 29(3): 327-331.
58. 杨猛, 高天虹. 蛋白酪氨酸磷酸酶 1B (PTP1B) 抑制剂的研究进展. 河南化工, 2015, 32(1): 11-15.
59. Akbas H, Kahraman S, Sak S, et al. Minor variant of AHSG gene 767C> G polymorphism may decrease the risk of gestational diabetes mellitus. J Obstet Gynaecol, 2020, 40(3): 303-307.
60. 王雨艳, 黄达, 沈秀敏, 等. 雌激素受体和孕激素受体在妊娠期高血压疾病胎盘组织中的表达. 解剖科学进展, 2015, 21(6): 621-623.
61. Barros RP, Morani A, Moriscot A, et al. Insulin resistance of pregnancy involves estrogen-induced repression of muscle GLUT4. Mol Cell Endocrinol, 2008, 295(1/2): 24-31.

Previous Article
The clinical and pathological characteristics of advanced colorectal adenomatous polyps
Next Article
Thoughts on the construction of internet hospitals from the perspective of PDCA

West China Medical Journal

The relationship between differential placental protein expressions and insulin resistance: a systematic review and meta-analysis

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content