Insulin-mediated immune dysfunction in the development of preeclampsia

Gustav van Niekerk1, Claudia Christowitz1, Anna‐Mart Engelbrecht1
1Department of Physiological Sciences, University of Stellenbosch, Stellenbosch, South Africa

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Bryson CL, Ioannou GN, Rulyak SJ, Critchlow C (2003) Association between gestational diabetes and pregnancy-induced hypertension. Am J Epidemiol 158:1148–1153

Schneider S, Freerksen N, Röhrig S, Hoeft B, Maul H (2012) Gestational diabetes and preeclampsia - similar risk factor profiles? Early Hum Dev 88:179–184

Lee J, Ouh YT, Ahn KH, Hong SC, Oh MJ, Kim HJ, Cho GJ (2017) Preeclampsia: a risk factor for gestational diabetes mellitus in subsequent pregnancy. PLoS One 12:e0178150

Vestgaard M, Sommer MC, Ringholm L et al (2018) Prediction of preeclampsia in type 1 diabetes in early pregnancy by clinical predictors: a systematic review. J Matern Neonatal Med 31:1933–1939

Cavero-Redondo I, Martínez-Vizcaíno V, Soriano-Cano A, Martínez-Hortelano JA, Sanabria-Martínez G, Álvarez-Bueno C (2018) Glycated haemoglobin A1c as a predictor of preeclampsia in type 1 diabetic pregnant women: a systematic review and meta-analysis. Pregnancy Hypertens 14:49–54

Holmes VA, Young IS, Patterson CC, Pearson DWM, Walker JD, Maresh MJA, McCance DR, for the Diabetes and Pre-eclampsia Intervention Trial Study Group (2011) Optimal glycemic control, pre-eclampsia, and gestational hypertension in women with type 1 diabetes in the Diabetes and Pre-Eclampsia Intervention Trial. Diabetes Care 34:1683–1688

Valdés E, Sepúlveda-Martínez Á, Manukián B, Parra-Cordero M (2014) Assessment of pregestational insulin resistance as a risk factor of preeclampsia. Gynecol Obstet Investig 77:111–116

Knight KM, Pressman EK, Hackney DN, Thornburg LL (2012) Perinatal outcomes in type 2 diabetic patients compared with non-diabetic patients matched by body mass index. J Matern Neonatal Med 25:611–615

Persson M, Cnattingius S, Wikström AK, Johansson S (2016) Maternal overweight and obesity and risk of pre-eclampsia in women with type 1 diabetes or type 2 diabetes. Diabetologia. 59:2099–2105

Bantug GR, Galluzzi L, Kroemer G, Hess C (2018) The spectrum of T cell metabolism in health and disease. Nat Rev Immunol 18:19–34

Newton R, Priyadharshini B, Turka LA (2016) Immunometabolism of regulatory T cells. Nat Immunol 17:618–625

Russell DG, Huang L, VanderVen BC (2019) Immunometabolism at the interface between macrophages and pathogens. Nat Rev Immunol 19:291–304

van Niekerk G, Engelbrecht AM (2018) Inflammation-induced metabolic derangements or adaptation: an immunometabolic perspective. Cytokine Growth Factor Rev 43:47–53

van Niekerk G, Christowitz C, Conradie D, Engelbrecht A (2019) Insulin as an immunomodulatory hormone. Cytokine Growth Factor Rev 52:34–44. https://doi.org/10.1016/j.cytogfr.2019.11.006

Harmon AC, Cornelius DC, Amaral LM, Faulkner JL, Cunningham MW Jr, Wallace K, LaMarca B (2016) The role of inflammation in the pathology of preeclampsia. Clin Sci 130:409–419

Hsu P, Nanan RKH (2014) Innate and adaptive immune interactions at the fetal-maternal interface in healthy human pregnancy and pre-eclampsia. Front Immunol 5:125

Laresgoiti-Servitje E (2013) A leading role for the immune system in the pathophysiology of preeclampsia. J Leukoc Biol 94:247–257

Nourollahpour Shiadeh M, Behboodi Moghadam Z, Adam I, Saber V, Bagheri M, Rostami A (2017) Human infectious diseases and risk of preeclampsia: an updated review of the literature. Infection 45:589–600

Egan AM, Vellinga A, Harreiter J et al (2017) Epidemiology of gestational diabetes mellitus according to IADPSG/WHO 2013 criteria among obese pregnant women in Europe. Diabetologia. 60:1913–1921

Frühbeck G, Catalán V, Rodríguez A, Gómez-Ambrosi J (2018) Adiponectin-leptin ratio: a promising index to estimate adipose tissue dysfunction. Relation with obesity-associated cardiometabolic risk. Adipocyte 7:57–62

La Cava A (2017) Leptin in inflammation and autoimmunity. Cytokine 98:51–58

Naylor C, Petri WA (2016) Leptin regulation of immune responses. Trends Mol Med 22:88–98

Procaccini C, De Rosa V, Galgani M et al (2010) An oscillatory switch in mTOR kinase activity sets regulatory t cell responsiveness. Immunity. 33:929–941

Eghbal-Fard S, Yousefi M, Heydarlou H, Ahmadi M, Taghavi S, Movasaghpour A, Jadidi-Niaragh F, Yousefi B, Dolati S, Hojjat-Farsangi M, Rikhtegar R, Nouri M, Aghebati-Maleki L (2019) The imbalance of Th17/Treg axis involved in the pathogenesis of preeclampsia. J Cell Physiol 234:5106–5116

Darmochwal-Kolarz D, Kludka-Sternik M, Tabarkiewicz J, Kolarz B, Rolinski J, Leszczynska-Gorzelak B, Oleszczuk J (2012) The predominance of Th17 lymphocytes and decreased number and function of Treg cells in preeclampsia. J Reprod Immunol 93:75–81

Asghar A, Sheikh N (2017) Role of immune cells in obesity induced low grade inflammation and insulin resistance. Cell Immunol 315:18–26

Wu D, Wong CK, Han JM, Orban PC, Huang Q, Gillies J, Mojibian M, Gibson WT, Levings MK (2020) T reg–specific insulin receptor deletion prevents diet-induced and age-associated metabolic syndrome. J Exp Med. https://doi.org/10.1084/jem.20191542

Simpson S, Smith L, Bowe J (2018) Placental peptides regulating islet adaptation to pregnancy: clinical potential in gestational diabetes mellitus. Curr Opin Pharmacol 43:59–65

Pham MN, Hawa MI, Pfleger C et al (2011) Pro- and anti-inflammatory cytokines in latent autoimmune diabetes in adults, type 1 and type 2 diabetes patients: action LADA 4. Diabetologia. 54:1630–1638

Snell-Bergeon JK, West NA, Mayer-Davis EJ, Liese AD, Marcovina SM, D'Agostino RB Jr, Hamman RF, Dabelea D (2010) Inflammatory markers are increased in youth with type 1 diabetes: the SEARCH case-control study. J Clin Endocrinol Metab 95:2868–2876

Ramasamy R, Yan SF, Schmidt AM (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243:88–102

Chen W, Zhang Y, Yue C, Ye Y, Chen P, Peng W, Wang Y (2017) Accumulation of advanced glycation end products involved in inflammation and contributing to severe preeclampsia, in maternal blood, umbilical blood and placental tissues. Gynecol Obstet Investig 82:388–397

Huang SCC, Everts B, Ivanova Y, O'Sullivan D, Nascimento M, Smith AM, Beatty W, Love-Gregory L, Lam WY, O'Neill CM, Yan C, du H, Abumrad NA, Urban JF Jr, Artyomov MN, Pearce EL, Pearce EJ (2014) Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat Immunol 15:846–855

Han JM, Patterson SJ, Speck M, Ehses JA, Levings MK (2014) Insulin inhibits IL-10–mediated regulatory T cell function: implications for obesity. J Immunol 192:623–629

Sauer S, Bruno L, Hertweck A, Finlay D, Leleu M, Spivakov M, Knight ZA, Cobb BS, Cantrell D, O'Connor E, Shokat KM, Fisher AG, Merkenschlager M (2008) T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc Natl Acad Sci U S A 105:7797–7802

Tsai S, Clemente-Casares X, Zhou AC et al (2018) Insulin receptor-mediated stimulation boosts T cell immunity during inflammation and infection. Cell Metab 28:922–934.e4

Alqudah A, McKinley MC, McNally R et al (2018) Risk of pre-eclampsia in women taking metformin: a systematic review and meta-analysis. Diabet Med 35:160–172

Romero R, Erez O, Hüttemann M, Maymon E, Panaitescu B, Conde-Agudelo A, Pacora P, Yoon BH, Grossman LI (2017) Metformin, the aspirin of the 21st century: its role in gestational diabetes mellitus, prevention of preeclampsia and cancer, and the promotion of longevity. Am J Obstet Gynecol 217:282–302

Yang M, Ding Y, Wang Y et al (2017) Metformin regulates of Th17/treg cell balance and reduces hyperplastic synovium via activating AMPK and inhibiting mTOR in a collagen-induced arthritis rat model. Int J Clin Exp Med 10:11479–11487

Michalek RD, Gerriets VA, Jacobs SR, Macintyre AN, MacIver NJ, Mason EF, Sullivan SA, Nichols AG, Rathmell JC (2011) Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4 + T cell subsets. J Immunol 186:3299–3303

Nagai S, Kurebayashi Y, Koyasu S (2013) Role of PI3K/Akt and mTOR complexes in Th17 cell differentiation. Ann N Y Acad Sci 1280:30–34

Mungamuri SK, Yang X, Thor AD, Somasundaram K (2006) Survival signaling by Notch1: mammalian target of rapamycin (mTOR)-dependent inhibition of p53. Cancer Res 66:4715–4724 66/9/4715

Jensen F, Wallukat G, Herse F, Budner O, el-Mousleh T, Costa SD, Dechend R, Zenclussen AC (2012) CD19 +CD5 + cells as indicators of preeclampsia. Hypertension. 59:861–868

Nandagopal N, Ali AK, Komal AK, Lee SH (2014) The critical role of IL-15-PI3K-mTOR pathway in natural killer cell effector functions. Front Immunol. https://doi.org/10.3389/fimmu.2014.00187

Fukui A, Yokota M, Funamizu A, Nakamua R, Fukuhara R, Yamada K, Kimura H, Fukuyama A, Kamoi M, Tanaka K, Mizunuma H (2012) Changes of NK cells in preeclampsia. Am J Reprod Immunol 67:278–286

Taylor EB, Sasser JM (2017) Natural killer cells and T lymphocytes in pregnancy and pre-eclampsia. Clin Sci 131:2911–2917

Shin J, Wang S, Deng W, Wu J, Gao J, Zhong XP (2014) Mechanistic target of rapamycin complex 1 is critical for invariant natural killer T-cell development and effector function. Proc Natl Acad Sci U S A 111:E776–E783

Zegeye MM, Lindkvist M, Fälker K et al (2018) Activation of the JAK/STAT3 and PI3K/AKT pathways are crucial for IL-6 trans-signaling-mediated pro-inflammatory response in human vascular endothelial cells. Cell Commun Signal 16:1–10. https://doi.org/10.1186/s12964-018-0268-4

Wei SC, Duffy CR, Allison JP (2018) Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov 8:1069–1086

Wykes MN, Lewin SR (2018) Immune checkpoint blockade in infectious diseases. Nat Rev Immunol 18:91–104

Postow MA, Sidlow R, Hellmann MD (2018) Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med 378:158–168

Miko E, Meggyes M, Doba K et al (2019) Immune checkpoint molecules in reproductive immunology. Front Immunol 10:846

Okkenhaug K, Vanhaesebroeck B (2003) PI3K in lymphocyte development, differentiation and activation. Nat Rev Immunol 3:317–330

Yokosuka T, Takamatsu M, Kobayashi-Imanishi W, Hashimoto-Tane A, Azuma M, Saito T (2012) Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 209:1201–1217

Hui E, Cheung J, Zhu J et al (2017) T cell costimulatory receptor CD28 is a primary target for PD-1-mediated inhibition. Science (80- ). https://doi.org/10.1126/science.aaf1292

Meggyes M, Miko E, Lajko A, Csiszar B, Sandor B, Matrai P, Tamas P, Szereday L (2019) Involvement of the PD-1/PD-L1 co-inhibitory pathway in the pathogenesis of the inflammatory stage of early-onset preeclampsia. Int J Mol Sci. https://doi.org/10.3390/ijms20030583

Rowshanravan B, Halliday N, Sansom DM (2018) CTLA-4: a moving target in immunotherapy. Blood 131:58–67

Parry RV, Chemnitz JM, Frauwirth KA, Lanfranco AR, Braunstein I, Kobayashi SV, Linsley PS, Thompson CB, Riley JL (2005) CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol 25:9543–9553

Hancock ML, Meyer RC, Mistry M et al (2019) Insulin receptor associates with promoters genome-wide and regulates gene expression. Cell 177:722–736.e22

Kesten D, Horovitz-Fried M, Brutman-Barazani T, Sampson SR (2018) Insulin-induced translocation of IR to the nucleus in insulin responsive cells requires a nuclear translocation sequence. Biochim Biophys Acta, Mol Cell Res 1865:551–559

Desoye G, Hartmann M, Jones CJP, Wolf HJ, Kohnen G, Kosakke G, Kaufmann P (1997) Location of insulin receptors in the placenta and its progenitor tissues. Microsc Res Tech 38:63–75

Ruiz-Palacios M, Ruiz-Alcaraz AJ, Sanchez-Campillo M, Larqué E (2017) Role of insulin in placental transport of nutrients in gestational diabetes mellitus. Ann Nutr Metab 70:16–25

Ohnishi M, Tokuda M, Masaki T, Fujimura T, Tai Y, Itano T, Matsui H, Ishida T, Konishi R, Takahara J (1995) Involvement of annexin-I in glucose-induced insulin secretion in rat pancreatic islets. Endocrinology. 136:2421–2426

Hong SH, Won JH, Yoo SA, Auh CK, Park YM (2002) Effect of annexin I on insulin secretion through surface binding sites in rat pancreatic islets. FEBS Lett 532:17–20

D’Acunto CW, Gbelcova H, Festa M, Ruml T (2014) The complex understanding of annexin A1 phosphorylation. Cell Signal 26:173–178

Jeong IK, Oh SH, Chung JH, Min YK, Lee MS, Lee MK, Kim KW (2002) The stimulatory effect of IL-1β on the insulin secretion of rat pancreatic islet is not related with iNOS pathway. Exp Mol Med 34:12–17

Eizirik DL, Sandler S, Welsh N, Juntti-Berggren L, Berggren PO (1995) Interleukin-1β-induced stimulation of insulin release in mouse pancreatic islets is related to diacylglycerol production and protein kinase C activation. Mol Cell Endocrinol 111:159–165

Burke SJ, Batdorf HM, Burk DH, Martin TM, Mendoza T, Stadler K, Alami W, Karlstad MD, Robson MJ, Blakely RD, Mynatt RL, Collier JJ (2018) Pancreatic deletion of the interleukin-1 receptor disrupts whole body glucose homeostasis and promotes islet β-cell de-differentiation. Mol Metab 14:95–107

Kurauti MA, Costa JM, Ferreira SM et al (2017) Interleukin-6 increases the expression and activity of insulin degrading enzyme. Sci Rep. https://doi.org/10.1038/srep46750

Ratter JM, van Heck JIP, Rooijackers HMM et al (2021) Insulin acutely activates metabolism of primary human monocytes and promotes a proinflammatory phenotype. J Leukoc Biol. https://doi.org/10.1002/JLB.3AB0120-019RR

Ieronymaki E, Theodorakis EM, Lyroni K, Vergadi E, Lagoudaki E, al-Qahtani A, Aznaourova M, Neofotistou-Themeli E, Eliopoulos AG, Vaporidi K, Tsatsanis C (2019) Insulin resistance in macrophages alters their metabolism and promotes an M2-like phenotype. J Immunol 202:1786–1797

Madsen RR, Vanhaesebroeck B (2020) Cracking the context-specific PI3K signaling code. Sci Signal 13(613):eaay2940. https://doi.org/10.1126/scisignal.aay2940

Li P, Wei J, Gao X, Wei B, Lin H, Huang R, Niu Y, Lim K, Jing K, Chu J (2017) Insulin promotes the proliferation of human umbilical cord matrix-derived mesenchymal stem cells by activating the Akt-cyclin D1 axis. Stem Cells Int 2017:1–10

Shrader CD, Bailey KM, Konat GW, Cilento EV, Reilly FD (2009) Insulin enhances proliferation and viability of human umbilical vein endothelial cells. Arch Dermatol Res 301:159–166

Karar J, Maity A (2011) PI3K/AKT/mTOR pathway in angiogenesis. Front Mol Neurosci. https://doi.org/10.3389/fnmol.2011.00051

Lisonkova S, Joseph KS (2013) Incidence of preeclampsia: risk factors and outcomes associated with early-versus late-onset disease. Am J Obstet Gynecol 209:544.e1–544.e12

Kc K, Shakya S, Zhang H (2015) Gestational diabetes mellitus and macrosomia: a literature review. Ann Nutr Metab 66(Suppl 2):14–20