{"id":77182,"date":"2024-03-19T14:32:17","date_gmt":"2024-03-19T14:32:17","guid":{"rendered":"https:\/\/touchendocrinology.com\/?p=77182"},"modified":"2024-04-30T16:05:37","modified_gmt":"2024-04-30T15:05:37","slug":"the-placental-role-in-gestational-diabetes-mellitus-a-molecular-perspective","status":"publish","type":"post","link":"https:\/\/touchendocrinology.com\/diabetes\/journal-articles\/the-placental-role-in-gestational-diabetes-mellitus-a-molecular-perspective\/","title":{"rendered":"The Placental Role in Gestational Diabetes Mellitus: A Molecular Perspective"},"content":{"rendered":"
Gestational diabetes mellitus (GDM) is generally defined as \u201cany degree of glucose tolerance with onset or first recognition during pregnancy\u201d.1<\/sup><\/span>\u00a0It currently is one of the diseases with the highest morbidity among pregnant women.2<\/sup><\/span>\u00a0Determining its prevalence has been a real challenge for the scientific community due to multiple modifications in the diagnostic criteria established in 1964 by O\u2019Sullivan and Mahan.3<\/sup><\/span>\u00a0Globally, its prevalence ranges from 1% to 14%.2<\/sup><\/span>\u00a0Nevertheless, in a systematic review and meta-analysis\u00a0providing updated estimates of<\/span>\u00a0gestational diabetes in Latin American in 2022, the reported prevalence was 8.5%.4<\/sup><\/span><\/p>\n GDM is a multifactorial disease in which both genetic and environmental components play a crucial role in its aetiopathogenesis.5<\/sup><\/span>\u00a0It is characterized by the inability to compensate for the physiological insulin resistance (IR) generated by hormonal and inflammatory changes that normally occur during pregnancy.6<\/sup><\/span>\u00a0The hyperglycaemia that occurs in GDM has multiple consequences for both the mother and the foetus, not only during intrauterine life but also during childbirth, the perinatal period and beyond.7,8<\/sup><\/span>\u00a0About 50% of women diagnosed with GDM during pregnancy will develop type 2 diabetes mellitus (T2DM) in the future.9<\/sup><\/span>\u00a0Furthermore, foetuses from mothers with GDM can present with short-term complications, such as macrosomia, shoulder dystocia and neonatal hypoglycaemia. These children also have a greater risk of developing obesity and T2DM in adulthood.6<\/sup><\/span><\/p>\n Many maternal and foetal complications of GDM have been attributed to abnormal placental development and anatomical and functional alterations.10<\/sup><\/span>\u00a0The placenta is a complex organ that separates the maternal and foetal circulations due to its anatomical configuration. As a result, it is exposed to multiple maternal and foetal substrates. Recent studies also highlight the role of certain regulators that are responsible for placental malfunctioning and GDM development.11,12<\/sup><\/span>\u00a0These studies mention several placental hormones, pro-inflammatory molecules, endothelial cell dysfunction and maternal adipose tissues, as well as the interruption of several molecular pathways, such as nuclear factor kappa-light-chain enhancer of activated B cells (NF-\u03baB), peroxisome proliferator-activated receptors (PPARs), sirtuins, 5\u2019 AMP-activated protein kinase (AMPK), glycogen synthase kinase 3 (GSK-3), inflammasome and endoplasmic reticulum stress.13\u201315<\/sup><\/span><\/p>\n This review aims to illustrate the role of the placenta in the development of GDM from a molecular perspective. We start by describing the pro-inflammatory factors and changes in different hormones, such as the placental lactogen, PGH and adipokines, which precede the anatomical disturbances leading to alterations in the placental endothelial and angiogenic factors and transporters. Finally, we explore their impact on foetal development.<\/p>\n Glucose is the primary energy substrate needed for foetal and placental growth. Since foetal gluconeogenesis is minimal during gestation, pregnant women undergo several physiological changes in their metabolic, renal, immune, cardiovascular, haematologic and respiratory systems to guarantee a continuous and adequate supply of glucose to the foetus (Figure 1<\/em><\/span>).16,17<\/sup><\/span>\u00a0Regarding metabolic changes, the onset of physiological IR, which increases as the pregnancy progresses, is necessary to originate a maternal\u2013foetal glucose transfer system via facilitated diffusion, mainly through the glucose transporter 1 (GLUT1).18,19<\/sup><\/span><\/p>\n In a normal pregnancy, there is an increase in insulin sensitivity during the first half of the pregnancy. Subsequently, a decrease in insulin sensitivity of up to 60% has been observed.20<\/sup><\/span>\u00a0This is followed by reversible compensatory changes in pancreatic beta cells, perhaps involving an increase in their number (hyperplasia) and size (hypertrophy) due to higher levels of oestrogen, progesterone, human placental lactogen (hPL), prolactin (PRL), kisspeptin and cortisol, among other growth factors.21<\/sup><\/span><\/p>\n Both hPL and PRL exert their effects via prolactin receptors (PRLRs), which are specifically expressed in pancreatic beta cells. The intracellular mechanisms of these receptors involve the regulation of pro-proliferative and anti-apoptotic pathways via the Janus kinase 2-signal transducer and activator of transcription 5 (JAK2\/STAT5) pathway, mitogen-activated protein kinase (MAPK), phosphatidylinositol 3-kinase (PI3K), and protein kinase B (AKT).22 <\/sup><\/span>Furthermore, there is an increase in glucokinase synthesis, resulting in a decrease in glucose-induced insulin secretion threshold, leading to hyperinsulinaemia, which allows the maintenance of euglycaemia during pregnancy.19,23<\/sup><\/span>\u00a0Studies show that the increase in hPL-dependent insulin secretion is mediated by increased levels of enzymes regulating serotonin synthesis, such as tryptophan hydroxylase 1 and 2.24<\/sup><\/span>\u00a0Likewise, there is hypertrophy and compensatory hyperplasia of pancreatic beta cells in the mother as a physiological adaptation to hPL pregnancy. When gestation ends, the pancreatic beta-cell mass starts to regress until it reaches normal conditions.25<\/sup><\/span>\u00a0Although the mechanisms responsible for these processes are not yet completely understood, it is known that, after childbirth, the beta-cell mass is reduced via apoptosis.26<\/sup><\/span>\u00a0Other studies suggest that this is due to a reduction in their size and proliferation.27<\/sup><\/span>\u00a0However, these processes are yet to be demonstrated in humans.28<\/sup><\/span><\/p>\n In women who are obese, pancreatic beta cell dysfunction \u2013 including the inability of beta cells to undergo adaptive changes after the first trimester of pregnancy \u2013 may create a pro-inflammatory environment, which is capable of disrupting the appropriate response before the endocrine signs of pregnancy, increasing the risk of developing GDM.29<\/sup><\/span>\u00a0This phenomenon may be explained by an increase in platelet-derived growth factor\u00a0<\/span>because the levels of this peptide are inversely related to pancreatic beta-cell function in patients with GDM.\u00a0<\/span>On the other hand, it is believed that\u00a0the\u00a0<\/span>chemokine (C-X-C motif) ligand 10<\/span>\u00a0(<\/span>CXCL10), an inflammatory marker, is capable of inhibiting the proliferation of pancreatic beta cells through binding to\u00a0<\/span>C-X-C motif ligand 3\u00a0<\/span>(CXCL3)<\/span>, or through interaction with the toll-like receptor 4 as part of the\u00a0NF-\u03baB<\/span>\u00a0activation pathways mediating IR in GDM.30<\/sup><\/span>\u00a0Although an in-depth review of the immunological alterations in GDM is not within the scope of this work, these findings highlight the immune-related features mediating GDM pathogenesis.<\/p>\n In pregnant women, several factors increase the risk of a disturbance in physiological IR. These include family and personal history of diabetes mellitus, obesity, race (primarily indigenous people worldwide, African American and Hispanic),23,24<\/sup><\/span>\u00a0and advanced maternal age (\u226535) (Table 1<\/em><\/span>).24,31<\/sup><\/span>\u00a0As a result, IR becomes more severe and cannot be compensated by maternal hyperinsulinemia, resulting in the characteristic hyperglycaemia of GDM.32<\/sup><\/span>\u00a0The mechanism by which these alterations occur requires further study. However, it is believed that obesity causes a decrease in hPL levels via the downregulation of CCAAT-enhancer binding protein transcription factors, which are co-expressed with hPL in the syncytiotrophoblast (SCTB). C\/EBP binds to an enhancer region downstream of the\u00a0hPL<\/em>\u00a0gene, modifying its expression. Therefore, its downregulation results in deficiencies in compensatory metabolic effects.33<\/sup><\/span><\/p>\n Low risk<\/b><\/p>\n<\/td>\n High risk<\/b><\/p>\n<\/td>\n<\/tr>\n<\/thead>\n\n Ethnic group with a low incidence of GDM<\/sup><\/p>\n<\/td>\n Being part of an ethnic group with a high incidence of GDM<\/sup><\/p>\n<\/td>\n<\/tr>\n No family history of DM<\/sup><\/p>\n<\/td>\n First-degree family history of DM<\/sup><\/p>\n<\/td>\n<\/tr>\n Younger than 25 years old<\/p>\n<\/td>\n Previous detection of glucose intolerance<\/p>\n<\/td>\n<\/tr>\n Normal weight<\/p>\n<\/td>\n Obesity<\/p>\n<\/td>\n<\/tr>\n Normal weight at birth<\/p>\n<\/td>\n Glycosuria accentuated during pregnancy<\/p>\n<\/td>\n<\/tr>\n<\/tbody>\n<\/table>\n<\/div>\n Adapted from\u00a0Santamaria et al., 2011.<\/span>31<\/sup><\/span><\/span><\/span><\/span><\/em><\/p>\n<\/div>\n DM<\/span>\u00a0=\u00a0diabetes mellitus<\/span>; <\/span>GDM<\/span>\u00a0=\u00a0gestational diabetes mellitus<\/span>.<\/span><\/em><\/p>\n<\/div>\n<\/div>\n<\/div>\n The incidence of GDM is higher among women with a higher body mass index (BMI) and weight before pregnancy compared with those with a normal BMI. A significant weight gain during the first trimester was positively associated with GDM in women with high BMI before pregnancy.26<\/sup><\/span>\u00a0These alterations are primarily seen in the last trimester. Hence, the diagnosis of GDM is made after week 24 using specific diagnostic criteria (Figure 2<\/span>).31,35,36<\/sup><\/span><\/p>\n Algorithm formulated from diagnostic measures outlined in international guidelines from Harris, 1995;34<\/sup><\/span>\u00a0Carpenter and Coustan, 1982;35<\/sup><\/span>\u00a0International Association of Diabetes and Pregnancy Study Groups Consensus Panel, 2010.36<\/sup><\/span><\/em><\/p>\n ACOG =\u00a0American College of Obstetricians and Gynecologists<\/span>;\u00a0<\/span>ADA =\u00a0American Diabetes Association<\/span>;\u00a0<\/span>h = hour;\u00a0<\/span>IADPSG =\u00a0International Association of Diabetes and Pregnancy Study Groups<\/span>;\u00a0<\/span>NGGD =\u00a0National Diabetes Data Group<\/span>;\u00a0<\/span>NIH =\u00a0National Institutes of Health<\/span>;\u00a0<\/span>OGTT =\u00a0oral glucose tolerance test<\/span>;\u00a0<\/span>WHO = World Health Organization.<\/span><\/em><\/p>\n<\/div>\n Since the mid 20th century, the main placental hormones, hPL and placental growth hormone (PGH), have been considered vital elements in the aetiopathogenesis of GDM, given their known diabetogenic effects in pregnant women.36<\/sup><\/span>\u00a0Nevertheless, even though the current evidence is not conclusive, it suggests a possible secondary role within the pathogenesis of this metabolic disease, with a greater emphasis on PGH dysregulation.37<\/sup><\/span><\/p>\n PGH is a polypeptide drug synthesized in placental SCTB from gestational weeks 13 to 20, replacing the pituitary growth hormone from that moment onwards.32<\/sup><\/span>\u00a0Its release is independent of the growth hormone-releasing hormone and induced by maternal hypoglycaemia.33<\/sup><\/span>\u00a0The direct and indirect effects of PGH as a primary regulator of insulin growth factor 1 (IGF-1) are limited to maternal and placental tissues, regulating placental growth and blood flow and generating a state of physiological IR to reduce the maternal use of glucose so that it can reach the foetus and allow adequate growth and development.31<\/sup><\/span>\u00a0Nonetheless, insulin is not the only hormone able to activate these signalling pathways since cytokines, as well as other hormones and growth factors, play a very important role in their activation. These molecules are also involved in cellular metabolism and may affect the transport of nutrients.38<\/sup><\/span><\/p>\n Among the mechanisms by which PGH generates a state of IR is a reduction in adiponectin synthesis. It is an important insulin-sensitizing and anti-inflammatory hormone, possibly via the activation of STAT5 proteins and their posterior binding to adiponectin promoter sites, decreasing its expression and release.36<\/sup><\/span>\u00a0Furthermore, it inhibits the insulin intracellular signalling pathway, with subsequent inhibition of glucose transporter 4 (GLUT4) translocation via the induction of expression of the gene-encoding\u00a0p85<\/em>\u00a0subunits;\u00a0this competitively inhibits insulin receptor substrate 1 (IRS-1), which activates PI3K by preventing its heterodimerization with a p110 subunit in insulin-dependent tissues<\/span>.39,40<\/sup><\/span>\u00a0Thus, along with other diabetogenic hormones, this mechanism creates a diabetogenic environment that favours maternal catabolic processes that generate energetic substrates for the foetus. Although these processes occur physiologically, their role in GDM has been associated with an overproduction of PGH,41 <\/sup><\/span>demonstrating a possible dose\u2013dependent relationship. However, the mechanisms causing these findings have not been completely elucidated.<\/p>\n Moreover, hPL is a polypeptide hormone synthesized by SCTB, whose levels increase significantly at the start of the second trimester. Its effects are mediated by PRLRs, activation of which mainly regulates the function and proliferation of pancreatic beta cells to maintain insulin release that compensates for the state of IR generated during gestation. Lepercq\u00a0<\/span>et al. proposed that polymorphisms of a single nucleotide (rs10068521 and rs9292578) in the gene encoding for PRLRs are related to a 2.3-fold increased risk of developing GDM.42<\/sup><\/span><\/p>\n It was proposed that these effects are related to the downregulation of molecules that inhibit the cell cycle, such as the B-cell lymphoma 6 (BCL6<\/span>) protein and cyclin-dependent kinase inhibitor 1 (p21), as well as the induction of anti-apoptotic molecules, such as B-cell lymphoma-extra-large (BCL-xL) and securin (PTTG1), and the protooncogene\u00a0FoxM1<\/em>.43,44<\/sup><\/span>\u00a0Thus, any alterations of these molecules in pancreatic beta cells or PRLRs may be involved in the reduction of proliferation and expansion of pancreatic beta-cell mass, leading to a deficient insulin release incapable of overcoming maternal IR and GDM development.42,45,46<\/sup><\/span><\/p>\n Leptin has also been associated with the development of IR and GDM.47<\/sup><\/span>\u00a0This polypeptide hormone is mainly synthesized in white adipose tissues. However, during gestation, the SCTB constitutes the primary synthesizing tissue. Hence, leptin levels are higher than they are in non-pregnant women48<\/sup><\/span>\u00a0. These levels progressively increase after implantation, reaching a peak between weeks 24 and 26, and persist until the immediate postpartum period.49,50<\/sup><\/span>\u00a0During gestation, leptin regulates vital processes, such as implantation, mitogenesis and placental growth, as well as the placental transport of amino acids, the release of human chorionic gonadotropin, immune response and maternal appetite.51,52<\/sup><\/span><\/p>\n Although a state of hyperleptinaemia is considered physiological, multiple studies reported significantly higher leptin levels in women with GDM.53\u201355<\/sup><\/span>\u00a0This could be the result of a combination of factors, including polymorphisms in the LEP rs2617270 allele of the gene that codes for this hormone, obesity prior to conception and excessive weight increase during pregnancy.52,55\u201357<\/sup><\/span>\u00a0These conditions are associated with IR and states of compensatory hyperinsulinaemia. Since insulin is a critical inductor of leptin secretion by white adipose tissues, it further stimulates its release, causing a vicious cycle. Moreover, despite the fact that leptin released by trophoblastic cells has a wide range of biological functions and plays a role in the successful establishment of pregnancy, it results in a higher hyperleptinaemia under these conditions, contributing to glucose resistance.58<\/sup><\/span><\/p>\n In this sense, it was proposed that hyperleptinaemia during the first trimester could significantly increase the risk of developing GDM by further accentuating the state of physiological IR via the release of tumour necrosis factor-alpha and interleukin 6 (IL-6) in the placenta.59<\/sup><\/span>\u00a0These inhibit the insulin intracellular signalling pathway and decrease its peripheral effects.60<\/sup><\/span>\u00a0Furthermore, the hyperleptinaemia would increase lipid mobilization, accentuating the lipotoxicity states of peripheral tissues.61<\/sup><\/span><\/p>\n Resistin is another adipokine that has generated interest over the last decades due to its association with IR, participating in entities such as T2DM, metabolic syndrome and obesity.62,63<\/sup><\/span>\u00a0This adipokine is a polypeptide hormone composed of 108 amino acids secreted by adipose cells during adipogenesis. Based on recent studies, resistin is also secreted by the pancreatic islets, skeletal muscle, mononuclear cells and liver, as well as the placenta, which is the primary source of resistin during gestation.62,63<\/sup><\/span><\/p>\n Like the previously described hormones, resistin secretion is progressive, reaching its peak in the third trimester and returning to normality after childbirth.64<\/sup><\/span>\u00a0It was reported that women with GDM have higher serum resistin levels.65 <\/sup><\/span>These levels increase even further if there is obesity since, just as with leptin, supraphysiological insulin levels stimulate resistin release even further in the placenta and adipose tissues.61<\/sup><\/span>\u00a0On the other hand, case-control studies have not shown an association between resistin levels and GDM, suggesting that resistin does not predict risk for this disease.44<\/sup><\/span><\/p>\n The implication of resistin in GDM development can be explained by its actions on the pancreatic islet, where it induces the expression of the suppressor of cytokine signalling 3 (SOCS3<\/em>) and inhibits the phosphorylation of the AKT pathway, leading to a decrease in insulin release.From\u00a0physiological\u00a0<\/span>insulin resistance<\/span>\u00a0to\u00a0<\/span>gestational diabetes<\/span>: When equilibrium is lost<\/span><\/h1>\n
Figure 1: <\/span>Physiological changes in macromolecule metabolism during pregnancy16<\/sup><\/span><\/h2>\n
<\/p>\n<\/div>\n
Table 1: <\/span>Risk factors for gestational diabetes mellitus31<\/sup><\/span><\/h2>\n
\n\n
\n \n \n \n \n \n \n \n \n \n \n \n \n \n \n \n \n \n Figure 2: <\/span>Different diagnostic criteria for gestational diabetes mellitus and recommending associations<\/h2>\n
<\/p>\n
Placental\u00a0hormones:\u00a0W<\/span>hen the good goes bad<\/span><\/h1>\n
Placental\u00a0lactogen and\u00a0<\/span>placental growth hormone<\/span><\/h2>\n
Leptin<\/h2>\n
Resistin<\/h2>\n