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Tain, Y. Early-Life Origins of Metabolic Syndrome. Encyclopedia. Available online: https://encyclopedia.pub/entry/15796 (accessed on 22 December 2024).
Tain Y. Early-Life Origins of Metabolic Syndrome. Encyclopedia. Available at: https://encyclopedia.pub/entry/15796. Accessed December 22, 2024.
Tain, You-Lin. "Early-Life Origins of Metabolic Syndrome" Encyclopedia, https://encyclopedia.pub/entry/15796 (accessed December 22, 2024).
Tain, Y. (2021, November 08). Early-Life Origins of Metabolic Syndrome. In Encyclopedia. https://encyclopedia.pub/entry/15796
Tain, You-Lin. "Early-Life Origins of Metabolic Syndrome." Encyclopedia. Web. 08 November, 2021.
Early-Life Origins of Metabolic Syndrome
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This entry is adapted from the peer-reviewed paper 10.3390/ijms222111872

Metabolic syndrome (MetS) is not a single disease but a collection of medical conditions that occur together and increase the risk of cardiovascular disease (CVD). Although MetS had been defined slightly differently by various organizations, the main components of MetS include obesity, hypertension, dyslipidemia and insulin resistance. The prevalence estimates vary, based on the criteria used for the diagnosis of MetS. 

metabolic syndrome

1. Introduction

Metabolic syndrome (MetS) is not a single disease but a collection of medical conditions that occur together and increase the risk of cardiovascular disease (CVD). Although MetS had been defined slightly differently by various organizations [1], the main components of MetS include obesity, hypertension, dyslipidemia and insulin resistance. The prevalence estimates vary, based on the criteria used for the diagnosis of MetS. Thus far, global MetS prevalence is estimated to affect approximately one quarter of the world population [2]. More importantly, MetS-related disorders account for two thirds of the non-communicable disease (NCDs) deaths [3]. Also important is that it displays multiple and diverse phenotypes with indications for differing treatment strategies. In the absence of specific therapeutic regimens, the prevalence of MetS remains on the increase globally [2]. Therefore, a superior strategy to stop the spread of the MetS epidemic is required to for prevention, in addition to treatment.
Most NCDs may start in early life [4]. The establishment of various adverse environmental conditions, which takes place during pregnancy and lactation, could be involved in the early-life programming of health. This concept is now known as the developmental origin of health and disease (DOHaD) [5], which is supported by evidence coming from a large number of epidemiological and experimental observations.
Various early-life risk factors often linked to nutritional imbalance may lead to vulnerability to later MetS [6][7][8][9][10]. Remarkably, there is evidence for the programming of some similar features of MetS from different early-life insults, possibly suggesting a commonality of mechanism and highlighting that identifying underlying mechanistic pathways is vital to develop ideal prevention interventions [6]. By intervening before disease ever occurs, we have the potential to stop undesirable programming processes resulting in MetS, which is referred to as reprogramming [11].

2. Epidemiological Evidence Linked Early-Life Insults with Offspring MetS

Extensive epidemiological studies have linked adverse early-life conditions with the risk of MetS in the offspring in later life. First, there is evidence from severe famines [12][13][14][15][16]. The Dutch Famine Birth Cohort Study demonstrated that the children of pregnant women exposed to famine displayed various characteristics of MetS, like obesity, dyslipidemia, hypertension, insulin resistance and CVDs [12][13]. Findings similar to those of the Dutch famine were also established in other famine studies [14][15][16]. Of particular interest, maternal undernutrition during early gestation had greater effects in increasing cardiometabolic risk in adult offspring, compared to maternal undernutrition during middle- or late-gestation [12]. Another line of evidence comes from research in twin pregnancy. These studies reported there were associations between low birth weight (LBW) and different characteristics of MetS, including hypertension, type 2 diabetes and insulin resistance [17][18]. Third, a prior systematic review of 39 studies revealed that rapid postnatal catch-up growth of LBW neonate had an approximately 80% increased risk for CVDs, a major complication of MetS [19]. The risk factors for MetS of developmental origins have been assessed in a number of observational studies. Risk factors reported in these cohorts relating to adverse cardiometabolic outcomes in adult offspring include maternal obesity [20][21], gestational diabetes [21][22], excessive postnatal weight gain, [23] and environmental chemicals exposure [16]. To date, literature on paternal risk factors is scare. There is emerging evidence that paternal risk factors, such as obesity, diabetes mellitus, advanced age, and cigarette smoke are associated with adverse metabolic and cardiovascular outcomes in their offspring [24][25]. All of these observations provide links between the suboptimal early-life environment and the risks for developing MetS in adulthood.
However, these epidemiological studies do not propose molecular mechanisms underlying programming processes for the development of potential reprogramming interventions. Therefore, animal models have been established to demonstrate the biological plausibility of the associations observed in epidemiological studies, providing proof of causality.

3. Animal Models for Developmental Origins of MetS

In view of the difficulties in establishing animal models that manifest all the characteristics of MetS, most investigations into MetS of developmental origin are done using models that display certain hallmarks of MetS [6][7][8]. To date, a broad range of adverse early-life environmental factors are associated with certain features of MetS in adult offspring, including nutrition imbalance, maternal conditions or disease, chemical exposure, medication use, etc. [6][7][8][9][10][26][27][28][29]. However, excessive information is available based on only one characteristic of MetS, and in the interest of brevity, we have limited this review to at least two of the listed components that are present [30][31][32][33][34][35][36][37][38][39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72] (See Table 1). Diverse small- and large-animal models have been developed for DOHaD research [29][73], each with its own natural advantages and disadvantages. This review was restricted to rodent models for appropriate comparisons of major characteristics of MetS appear through a lifetime. Table 1 reveals the outcomes relating to MetS determined in rats ranging from eight weeks to one year of age. Considering one human year is almost equivalent to two rat weeks in adulthood [74], most outcomes are determined from childhood to middle adulthood in terms of human age. Each category is discussed in turn.
Table 1. Rodent models of MetS of developmental origins, categorized according to environmental factors.
Animal Models Timing Experimental
Animal		 Offspring Outcomes Relating to MetS
Nutritional imbalance
Caloric restriction Pregnancy and lactation SD rats [30]/Wistar rats [31][32] ↑BP 12-16 wk [30][31], ↓insulin levels and exhibit insulin resistance 14 wk [32]
Protein restriction Pregnancy Wistar rats ↑BP 12 wk [33], exhibit insulin resistance 12 wk [34]
High-fat diet Pregnancy and lactation SD rats ↑BP 16 wk [35], ↑adiposity 16 wk [36], dyslipidemia 16 wk [37], ↑BW, exhibit dyslipidemia and hyperinsulinemia 100 day [38]
High-fructose diet Pregnancy and lactation SD rats/C57BL6J mice ↑BP [39], exhibit insulin resistance and dyslipidemia 12 wk [40], ↑BP, exhibit insulin resistance and obesity 1 year [41]
High-fructose diet plus high-fat diet Pregnancy and lactation SD rats [42]/Wistar rats [43] ↑BP 16 wk [42], ↑BW and adiposity 150 days [43]
Calcium-deficient diet Pregnancy WKY rats [44]/SD rats [45] ↑BP 1 year [44], ↑adiposity, exhibit insulin resistance and dyslipidemia [45]
Zinc-deficient diet Pregnancy and lactation Wistar rats [46]/SD rats [47] ↑BP 12 wk [46], ↑BW, exhibit insulin resistance 15 wk [47]
Vitamin D restricted diet Pregnancy and lactation SD rats ↑BP 8 wk [48], exhibit insulin resistance 16 wk [49]
Maternal illness/condition
Uteroplacental insufficiency Pregnancy WKY rats [50]/Wistar rats [51] ↑BP 22 wk [50], exhibit dyslipidemia and insulin resistance 30 wk [51]
Polycystic ovary syndrome Pregnancy Wistar rat [52], SD rats [53] ↑BP 120 days [52], exhibit dyslipidemia 16 wk [53]
Maternal hypoxia Pregnancy Wistar rats [52]/SD rats [54] ↑BP 4 mo [52], ↑BW and adiposity, exhibit insulin resistance 12 wk [54]
Maternal inflammation Pregnancy SD rats [55]/Wistar rats [56] ↑BP 12 wk [55], insulin resistance 75 days [56]
Diabetes Pregnancy SD rats [57]/Wistar rats [58][59] ↑BP 12 wk [57], ↑BW and adiposity 12 wk [58], exhibit insulin resistance and dyslipidemia 16 wk [59]
Chronodisruption Pregnancy and lactation SD rats [60]/Wistar rats [61] ↑BP 12 wk [60], exhibit insulin resistance 18 wk [61]
Chemical/medication exposure
DEHP Pregnancy Wistar rats ↑BP 21 wk [62], exhibit insulin resistance 80 day [63]
BPA Pregnancy and lactation SD rats ↑BP 16 wk [64], exhibit insulin resistance 6 mo [65]
Alcohol Pregnancy SD rats ↑BP 6 mo [66], exhibit insulin resistance 6 mo [67]
Nicotine Pregnancy Wistar rats ↑BP 8 mo [68], ↑BW and adiposity, exhibit insulin resistance [69]
Glucocorticoid Pregnancy and postnatal days1-3 SD rats [70][71]/Wistar rats [72] ↑BP 12 mo [70][71], exhibit insulin resistance 6 mo [72]
SD = Sprague-Dawley rat; WKY = Wistar-Kyoto rat; BP = blood pressure; BW = body weight; wk = week; mo = month; di-DEHP = (2-ethylhexyl) phthalate; BPA = bisphenol A; ↑ = increased; ↓ = decreased.

3.1. Nutritional Imbalance

Studies of nutritional programming linking DOHaD-related disorders using animal models have been ongoing since the early 1990s [73]. Dietary manipulation has been the focus of a large body of work relating to MetS of developmental origins. Table 1 shows insufficient or excessive consumption of a certain nutrient has been used to induce different features of MetS. Following the studies of the Dutch famine [12][13], a number of maternal nutrient restriction models have been established to mimic the undernutrition experienced by pregnant women at that time.
Caloric restriction is defined as an overall reduction in energy and nutrient intake without incurring specific nutrient. In rats, a 50% caloric restriction during gestation and lactation can result in hypertension and insulin resistance in adult offspring [28][29][30]. Restriction of calories by a range of 30% to 70% in pregnant rats has been reported to induce increases of BP in their adult progeny, as reviewed elsewhere [74]. From a general perspective, offspring exposed to a greater degree of caloric restriction are prone to develop hypertension earlier [75]. However, the extent to which the severity of caloric restriction affects other characteristics of MetS in adult offspring remains to be elucidated further.
Similar to caloric restriction, the protein restriction model may mimic the challenge faced in developing nations. Adult rat offspring born to dams exposed to protein restriction during pregnancy develop hypertension [31] and insulin resistance [32]. Although a more severe protein restriction causes an earlier development of hypertension in offspring [75], a previous study reported that two low-protein diet manipulations with the same protein concentration (9%) but different components in pregnant rat provoked different programming effects on BP in adult offspring [76]. It is therefore possible that the balance of specific amino acids and other nutrients may be a critical determinant in programming of MetS-related phenotypes but not protein restriction per se.
Table 1 indicates maternal high-fat diet programs almost all feature of MetS in adult rat offspring at 14–16 weeks of age, such as hypertension [33], obesity [34][36], dyslipidemia [35][36], and insulin resistance [36]. A high-fat diet has been widely used to explore the mechanisms of metabolic disease of both established and developmental origins [77][78]. Nevertheless, the programming effects of maternal high-fat diet on offspring BP are diverse according to age, sex, strains, and different fatty acids compositions [78]. Notably, abnormal regulation of insulin signaling and lipid metabolism programmed by a maternal high-fat diet can be promoted by a post-weaning high-fat diet, leading to development of MetS-related phenotypes in adult offspring [37][79][80]. A maternal high-fructose diet has also been reported as a commonly used animal model for studying MetS of developmental origins [81]. We and others have shown that adult rat offspring of mothers exposed to 60% high-fructose diet during gestation and lactation displayed MetS-related comorbidities [39][40][41][81]. Furthermore, mother rats receiving a high-fructose diet plus a high-fat diet saw an elevation in BP and BW in their offspring [42][43]. These findings suggest that maternal diets containing key components based on the human Western diet may have synergistic effects between fat and sugar on the development of features of MetS in adult offspring. Moreover, deficiencies in micronutrients, including calcium [44][45], zinc [46][47], and vitamin D [48][49] in pregnant mother rats are associated with offspring MetS.

3.2. Maternal Illnesses and Conditions

Complications during pregnancy and maternal diseases can affect fetal programming, resulting in intrauterine growth retardation (IUGR) in offspring [82]. As IUGR reflects an abnormal adaptive fetal growth in an adverse intrauterine environment, IUGR animal models are applied to decipher the underlying mechanisms behind MetS of developmental origins [82]. In the model of uteroplacental insufficiency developed by uterine artery ligation in the pregnant rat, IUGR offspring developed hypertension, dyslipidemia and insulin resistance in adulthood [50][51]. Additionally, several animal models resembling maternal conditions and diseases have been evaluated, such as polycystic ovary syndrome (PCOS) [52][53], maternal hypoxia [52][54], maternal inflammation [55][56], diabetes [57][58][59], and chronodisruption [60][61].
Epidemiological observations have established that inflammatory disorders, PCOS, and hypoxia increase the risk of pregnancy complications [83][84]. In the PCOS model, maternal hyperandrogenemia was induced by injection of testosterone cypionate in late gestation for studying cardiometabolic outcomes in adult offspring. Accordingly, adult offspring exhibited hypertension and dyslipidemia at 16–17 weeks of age [52][53]. Likewise, several features of MetS can be programmed by maternal hypoxia and inflammation, including hypertension [52][55], obesity [54], and insulin resistance [54][56].
It is clear from a range of human observational studies that maternal diabetes gives rise to different phenotypes of MetS in offspring, including obesity, insulin resistance, hypertension, dyslipidemia, and CVDs [85]. The majority of rodent studies of maternal diabetes have employed streptozotocin (STZ)-induced diabetes [57][58][59]. When injected into neonates [57][58] or adult rats [57][59], STZ can cause type 1 or type 2 diabetes, respectively. Almost all major characteristics of MetS are present in adult offspring born to diabetic mothers at 12–16 weeks of age [57][58][59], which are largely in line with the findings in humans.
There is now increasing evidence connecting disturbances in the circadian rhythm with the key components of MetS [86]. A meta-analysis including 22 studies showed that overall sleep quality as well as sleep complaints have significant positive associations with MetS [87]. The circadian system is the major regulator of human metabolism [88]. The circadian clock system consists of central and peripheral clocks, which are coordinated to produce daily rhythms [89]. This central clock located in the suprachiasmatic nucleus regulates the body’s metabolism through synchronizing peripheral clocks in our body’s key organs such as the heart, kidney, liver, muscle and adipose tissue [90]. Accordingly, it is not surprising that circadian rhythm sleep disorders have been linked to several components of the MetS [86].
In pregnant women, circadian disruption can lead to a wide range of adverse consequences for their children [91]. Maternal circadian disruption affects not only central and peripheral circadian clocks but also a range of endogenous circadian signals including melatonin and glucocorticoid secretion [92][93]. Although data on maternal sleep disorder programs MetS in offspring remain limited, two animal studies have reported that adult rat offspring born to dams received constant light exposure or pinealectomy developed hypertension [60] and insulin resistance [61].

3.3. Chemical and Medication Exposures

Relatively few studies have investigated early-life chemical and medication exposures on developmental programming of MetS. A broad range of early-life environmental chemical exposures have been related to increased risk for developing hypertension of developmental origins, as we reviewed elsewhere [94]. These chemicals, di-(2-ethylhexyl) phthalate (DEHP) and bisphenol A, have been studied for their impact on insulin resistance in adult progeny [63][65]. These findings are in agreement with epidemiological research data showing that endocrine-disrupting chemical exposure is linked to CVDs later in life [95].
As with chemical effects during development, substance abuse is another risk factor. A high proportion (6–16%) of pregnant women in the United States are cigarette smokers, alcohol abusers, or illicit drug users [96]. In rodent models, maternal nicotine or alcohol exposure causes hypertension [66][68], insulin resistance [67][69], and obesity [69] in adult offspring.
Despite a number of medications (such as cyclosporine [97] and minocycline [98]) administered in pregnancy that have been related to developmentally programmed hypertension in adult offspring [29], only glucocorticoid has been studied for other features of MetS [70][71][72]. During development, the fetus is at risk of glucocorticoid exposure through excess maternal corticosteroids (e.g., stressed pregnancies) or through exogenous administration (e.g., preterm birth). Antenatal or neonatal administration of dexamethasone lead to hypertension [70][71] and insulin resistance [72] in adult rat offspring.
Comparable to maternal programming, reported animal models relating to paternal factors-induced MetS in offspring are rather limited [25]. So far, only adult offspring of paternal low protein intake [99], paternal high-fat diet [100], and paternal hyperglycemia [101] have been evaluated, and these have developed at least two components of MetS.
Considering animal models are in good agreement with the epidemiological observations showing various maternal insults induce similar features of MetS in offspring, it is possible that various insults may mediate common mechanisms culminating in MetS of developmental origins.

References

  1. Alberti, K.G.; Eckel, R.H.; Grundy, S.M.; Zimmet, P.Z.; Cleeman, J.I.; Donato, K.A.; Fruchart, J.C.; James, W.P.; Loria, C.M.; Smith, S.C., Jr.; et al. Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009, 120, 1640–1645.
  2. Saklayen, M.G. The Global Epidemic of the Metabolic Syndrome. Curr. Hypertens. Rep. 2018, 20, 12.
  3. Zarocostas, J. Need to increase focus on non-communicable diseases in global health, says WHO. Br. Med. J. 2010, 341, c7065.
  4. Hanson, M. The birth and future health of DOHaD. J. Dev. Orig. Health Dis. 2015, 6, 434–437.
  5. Hanson, M.; Gluckman, P. Developmental origins of noncommunicable disease: Population and public health implications. Am. J. Clin. Nutr. 2011, 94, 1754S–1758S.
  6. McMillen, I.C.; Robinson, J.S. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol. Rev. 2005, 85, 571–633.
  7. Gluckman, P.D.; Hanson, M.A. The developmental origins of the metabolic syndrome. Trends Endocrinol. Metab. 2004, 15, 183–187.
  8. Armitage, J.A.; Khan, I.Y.; Taylor, P.D.; Nathanielsz, P.W.; Poston, L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: How strong is the evidence from experimental models in mammals? J. Physiol. 2004, 561, 355–377.
  9. de Gusmão Correia, M.L.; Volpato, A.M.; Águila, M.B.; Mandarim-de-Lacerda, C.A. Developmental origins of health and disease: Experimental and human evidence of fetal programming for metabolic syndrome. J. Hum. Hypertens. 2012, 26, 405–419.
  10. Ma, N.; Hardy, D.B. The Fetal Origins of the Metabolic Syndrome: Can We Intervene? J. Pregnancy 2012, 2012, 482690.
  11. Tain, Y.L.; Joles, J.A. Reprogramming: A preventive strategy in hypertension focusing on the kidney. Int. J. Mol. Sci. 2015, 17, 23.
  12. Lumey, L.H. Reproductive outcomes in women prenatally exposed to undernutrition: A review of findings from the Dutch famine birth cohort. Proc. Nutr. Soc. 1998, 57, 129–135.
  13. Schulz, L.C. The Dutch Hunger Winter and the Developmental Origins of Health and Disease. Proc. Natl. Acad. Sci. USA 2010, 107, 16757–16758.
  14. Stanner, S.A.; Yudkin, J.S. Fetal programming and the Leningrad Siege study. Twin Res. 2001, 4, 287–292.
  15. Hult, M.; Tornhammar, P.; Ueda, P.; Chima, C.; Bonamy, A.K.; Ozumba, B.; Norman, M. Hypertension, diabetes and overweight: Looming legacies of the Biafran famine. PLoS ONE 2010, 5, e13582.
  16. Wang, G.; Chen, Z.; Bartell, T.; Wang, X. Early Life Origins of Metabolic Syndrome: The Role of Environmental Toxicants. Curr. Environ. Health Rep. 2014, 1, 78–89.
  17. Bo, S.; Cavallo-Perin, P.; Ciccone, G.; Scaglione, L.; Pagano, G. The metabolic syndrome in twins: A consequence of low birth weight or of being a twin? Exp. Clin. Endocrinol. Diabetes 2001, 109, 135–140.
  18. Vaag, A.; Poulsen, P. Twins in metabolic and diabetes research: What do they tell us? Curr. Opin. Clin. Nutr. Metab. Care 2007, 10, 591–596.
  19. Kelishadi, R.; Haghdoost, A.A.; Jamshidi, F.; Aliramezany, M.; Moosazadeh, M. Low birthweight or rapid catch-up growth: Which is more associated with cardiovascular disease and its risk factors in later life? A systematic review and cryptanalysis. Paediatr. Int. Child Health 2015, 35, 110–123.
  20. Hrudey, E.J.; Reynolds, R.M.; Oostvogels, A.J.; Brouwer, I.A.; Vrijkotte, T.G. The association between maternal 25-hydroxyvitamin D concentration during gestation and early childhood cardio-metabolic outcomes: Is there interaction with pre-pregnancy BMI? PLoS ONE 2015, 10, e0133313.
  21. Boney, C.M.; Verma, A.; Tucker, R.; Vohr, B.R. Metabolic syndrome in childhood: Association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005, 115, e290–e296.
  22. Tam, W.H.; Ma, R.C.W.; Ozaki, R.; Li, A.M.; Chan, M.H.M.; Yuen, L.Y.; Lao, T.T.H.; Yang, X.; Ho, C.S.; Tutino, G.E.; et al. In utero exposure to maternal hyperglycemia increases childhood cardiometabolic risk in offspring. Diabetes Care 2017, 40, 679–686.
  23. Fraser, A.; Tilling, K.; Macdonald-Wallis, C.; Sattar, N.; Brion, M.J.; Benfield, L.; Ness, A.; Deanfield, J.; Hingorani, A.; Nelson, S.M.; et al. Association of maternal weight gain in pregnancy with offspring obesity and metabolic and vascular traits in childhood. Circulation 2010, 121, 2557–2564.
  24. Soubry, A. Epigenetics as a Driver of Developmental Origins of Health and Disease: Did We Forget the Fathers? Bioessays 2018, 40, 1700113.
  25. Eberle, C.; Kirchner, M.F.; Herden, R.; Stichling, S. Paternal metabolic and cardiovascular programming of their offspring: A systematic scoping review. PLoS ONE 2020, 15, e0244826.
  26. Tain, Y.L.; Hsu, C.N. Interplay between Oxidative Stress and Nutrient Sensing Signaling in the Developmental Origins of Cardiovascular Disease. Int. J. Mol. Sci. 2017, 18, 841.
  27. Chong, E.; Yosypiv, I.V. Developmental programming of hypertension and kidney disease. Int. J. Nephrol. 2012, 2012, 760580.
  28. Hsu, C.N.; Tain, Y.L. Early Origins of Hypertension: Should Prevention Start Before Birth Using Natural Antioxidants? Antioxidants 2020, 9, 1034.
  29. Hsu, C.N.; Tain, Y.L. Animal Models for DOHaD Research: Focus on Hypertension of Developmental Origins. Biomedicines 2021, 9, 623.
  30. Tain, Y.L.; Hsieh, C.S.; Lin, I.C.; Chen, C.C.; Sheen, J.M.; Huang, L.T. Effects of maternal L-citrulline supplementation on renal function and blood pressure in offspring exposed to maternal caloric restriction: The impact of nitric oxide pathway. Nitric Oxide 2010, 23, 34–41.
  31. Franco Mdo, C.; Ponzio, B.F.; Gomes, G.N.; Gil, F.Z.; Tostes, R.; Carvalho, M.H.; Fortes, Z.B. Micronutrient prenatal supplementation prevents the development of hypertension and vascular endothelial damage induced by intrauterine malnutrition. Life Sci. 2009, 85, 327–333.
  32. Holemans, K.; Verhaeghe, J.; Dequeker, J.; Van Assche, F.A. Insulin sensitivity in adult female rats subjected to malnutrition during the perinatal period. J. Soc. Gynecol. Investig. 1996, 3, 71–77.
  33. Cambonie, G.; Comte, B.; Yzydorczyk, C.; Ntimbane, T.; Germain, N.; Lê, N.L.; Pladys, P.; Gauthier, C.; Lahaie, I.; Abran, D.; et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292, R1236–R1245.
  34. Ozanne, S.E.; Smith, G.D.; Tikerpae, J.; Hales, C.N. Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am. J. Physiol. 1996, 270, E559–E564.
  35. Hsu, C.N.; Hou, C.Y.; Chang-Chien, G.P.; Lin, S.; Tain, Y.L. Maternal Garlic Oil Supplementation Prevents High-Fat Diet-Induced Hypertension in Adult Rat Offspring: Implications of H2S-Generating Pathway in the Gut and Kidneys. Mol. Nutr. Food Res. 2021, 65, e2001116.
  36. Tsai, T.A.; Tsai, C.K.; Huang, L.T.; Sheen, J.M.; Tiao, M.M.; Tain, Y.L.; Chen, C.C.; Lin, I.C.; Lai, Y.J.; Tsai, C.C.; et al. Maternal Resveratrol Treatment Re-Programs and Maternal High-Fat Diet-Induced Retroperitoneal Adiposity in Male Offspring. Int. J. Environ. Res. Public Health 2020, 17, 2780.
  37. Sheen, J.M.; Yu, H.R.; Tain, Y.L.; Tsai, W.L.; Tiao, M.M.; Lin, I.C.; Tsai, C.C.; Lin, Y.J.; Huang, L.T. Combined maternal and postnatal high-fat diet leads to metabolic syndrome and is effectively reversed by resveratrol: A multiple-organ study. Sci. Rep. 2018, 8, 5607.
  38. Wu, Z.; Zhao, J.; Xu, H.; Lyv, Y.; Feng, X.; Fang, Y.; Xu, Y. Maternal quercetin administration during gestation and lactation decrease endoplasmic reticulum stress and related inflammation in the adult offspring of obese female rats. Eur. J. Nutr. 2014, 53, 1669–1683.
  39. Hsu, C.N.; Lin, Y.J.; Hou, C.Y.; Tain, Y.L. Maternal Administration of Probiotic or Prebiotic Prevents Male Adult Rat Offspring against Developmental Programming of Hypertension Induced by High Fructose Consumption in Pregnancy and Lactation. Nutrients 2018, 10, 1229.
  40. Chao, Y.M.; Tain, Y.L.; Leu, S.; Wu, K.L.; Lee, W.C.; Chan, J.Y. Developmental programming of the metabolic syndrome: Next-generation sequencing analysis of transcriptome expression in a rat model of maternal high fructose intake. Sheng Li Xue Bao 2016, 68, 557–567.
  41. Saad, A.F.; Dickerson, J.; Kechichian, T.B.; Yin, H.; Gamble, P.; Salazar, A.; Patrikeev, I.; Motamedi, M.; Saade, G.R.; Costantine, M.M. High-fructose diet in pregnancy leads to fetal programming of hypertension, insulin resistance, and obesity in adult offspring. Am. J. Obstet. Gynecol. 2016, 215, 378.e1–378.e6.
  42. Yamada-Obara, N.; Yamagishi, S.I.; Taguchi, K.; Kaida, Y.; Yokoro, M.; Nakayama, Y.; Ando, R.; Asanuma, K.; Matsui, T.; Ueda, S.; et al. Maternal exposure to high-fat and high-fructose diet evokes hypoadiponectinemia and kidney injury in rat offspring. Clin. Exp. Nephrol. 2016, 20, 853–886.
  43. Li, M.; Reynolds, C.M.; Gray, C.; Patel, R.; Sloboda, D.M.; Vickers, M.H. Long-term effects of a maternal high-fat: High-fructose diet on offspring growth and metabolism and impact of maternal taurine supplementation. J. Dev. Orig. Health Dis. 2020, 11, 419–426.
  44. Bergel, E.; Belizán, J.M. A deficient maternal calcium intake during pregnancy increases blood pressure of the offspring in adult rats. BJOG 2002, 109, 540–545.
  45. Park, S.; Kang, S.; Kim, D.S. Severe calcium deficiency increased visceral fat accumulation, down-regulating genes associated with fat oxidation, and increased insulin resistance while elevating serum parathyroid hormone in estrogen-deficient rats. Nutr. Res. 2020, 73, 48–57.
  46. Tomat, A.; Elesgaray, R.; Zago, V.; Fasoli, H.; Fellet, A.; Balaszczuk, A.M.; Schreier, L.; Costa, M.A.; Arranz, C. Exposure to zinc deficiency in fetal and postnatal life determines nitric oxide system activity and arterial blood pressure levels in adult rats. Br. J. Nutr. 2010, 104, 382–389.
  47. Jou, M.Y.; Philipps, A.F.; Lönnerdal, B. Maternal zinc deficiency in rats affects growth and glucose metabolism in the offspring by inducing insulin resistance postnatally. J. Nutr. 2010, 140, 1621–1627.
  48. Tare, M.; Emmett, S.J.; Coleman, H.A.; Skordilis, C.; Eyles, D.W.; Morley, R.; Parkington, H.C. Vitamin D insufficiency is associated with impaired vascular endothelial and smooth muscle function and hypertension in young rats. J. Physiol. 2011, 589, 4777–4786.
  49. Zhang, H.; Chu, X.; Huang, Y.; Li, G.; Wang, Y.; Li, Y.; Sun, C. Maternal vitamin D deficiency during pregnancy results in insulin resistance in rat offspring, which is associated with inflammation and Iκbα methylation. Diabetologia 2014, 57, 2165–2172.
  50. Wlodek, M.E.; Westcott, K.; Siebel, A.L.; Owens, J.A.; Moritz, K.M. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008, 74, 187–195.
  51. Nüsken, K.D.; Dötsch, J.; Rauh, M.; Rascher, W.; Schneider, H. Uteroplacental insufficiency after bilateral uterine artery ligation in the rat: Impact on postnatal glucose and lipid metabolism and evidence for metabolic programming of the offspring by sham operation. Endocrinology 2008, 149, 1056–1063.
  52. Sherman, S.B.; Sarsour, N.; Salehi, M.; Schroering, A.; Mell, B.; Joe, B.; Hill, J.W. Prenatal androgen exposure causes hypertension and gut microbiota dysbiosis. Gut Microbes 2018, 9, 400–421.
  53. Zuchowski, Y.; Dalmasso, C.; Shawky, N.M.; Reckelhoff, J.F. Cardiometabolic consequences of maternal hyperandrogenemia in male offspring. Physiol. Rep. 2021, 9, e14941.
  54. Iqbal, W.; Ciriello, J. Effect of maternal chronic intermittent hypoxia during gestation on offspring growth in the rat. Am. J. Obstet. Gynecol. 2013, 209, 564.e1–564.e9.
  55. Wang, J.; Yin, N.; Deng, Y.; Wei, Y.; Huang, Y.; Pu, X.; Li, L.; Zheng, Y.; Guo, J.; Yu, J.; et al. Ascorbic Acid Protects against Hypertension through Downregulation of ACE1 Gene Expression Mediated by Histone Deacetylation in Prenatal Inflammation-Induced Offspring. Sci. Rep. 2016, 6, 39469.
  56. Tsosura, T.V.S.; Chiba, F.Y.; Mattera, M.S.L.C.; Pereira, R.F.; Cintra, L.T.A.; Conti, L.C.; Santos, R.M.D.; Mateus, J.H.P.; Garbin, C.A.S.; Sumida, D.H. Maternal apical periodontitis is associated with insulin resistance in adult offspring. Int. Endod. J. 2019, 52, 1040–1050.
  57. Tain, Y.L.; Lee, W.C.; Hsu, C.N.; Lee, W.C.; Huang, L.T.; Lee, C.T.; Lin, C.Y. Asymmetric dimethylarginine is associated with developmental programming of adult kidney disease and hypertension in offspring of streptozotocin-treated mothers. PLoS ONE 2013, 8, e55420.
  58. Oliveira, A.C.; Andreotti, S.; Chimin, P.; Sertié, R.A.; Farias Tda, S.; Torres-Leal, F.L.; de Proença, A.R.; Campaña, A.B.; D’Avila, L.S.; Oliveira, K.A.; et al. Neonatal streptozotocin-induced diabetes in mothers promotes metabolic programming of adipose tissue in male rat offspring. Life Sci. 2015, 136, 151–156.
  59. Thaeomor, A.; Teangphuck, P.; Chaisakul, J.; Seanthaweesuk, S.; Somparn, N.; Roysommuti, S. Perinatal Taurine Supplementation Prevents Metabolic and Cardiovascular Effects of Maternal Diabetes in Adult Rat Offspring. Adv. Exp. Med. Biol. 2017, 975, 295–305.
  60. Tain, Y.L.; Lin, Y.J.; Chan, J.Y.H.; Lee, C.T.; Hsu, C.N. Maternal melatonin or agomelatine therapy prevents programmed hypertension in male offspring of mother exposed to continuous light. Biol. Reprod. 2017, 97, 636–643.
  61. Ferreira, D.S.; Amaral, F.G.; Mesquita, C.C.; Barbosa, A.P.; Lellis-Santos, C.; Turati, A.O.; Santos, L.R.; Sollon, C.S.; Gomes, P.R.; Faria, J.A.; et al. Maternal melatonin programs the daily pattern of energy metabolism in adult offspring. PLoS ONE 2012, 7, e38795.
  62. Wei, Z.; Song, L.; Wei, J.; Chen, T.; Chen, J.; Lin, Y.; Xia, W.; Xu, B.; Li, X.; Chen, X.; et al. Maternal exposure to di-(2-ethylhexyl)phthalate alters kidney development through the renin-angiotensin system in offspring. Toxicol. Lett. 2012, 212, 212–221.
  63. Rajagopal, G.; Bhaskaran, R.S.; Karundevi, B. Maternal di-(2-ethylhexyl) phthalate exposure alters hepatic insulin signal transduction and glucoregulatory events in rat F1 male offspring. J. Appl. Toxicol. 2019, 39, 751–763.
  64. Hsu, C.N.; Lin, Y.J.; Tain, Y.L. Maternal exposure to bisphenol A combined with high-fat diet-induced programmed hypertension in adult male rat offspring: Effects of resveratrol. Int. J. Mol. Sci. 2019, 20, 4382.
  65. Galyon, K.D.; Farshidi, F.; Han, G.; Ross, M.G.; Desai, M.; Jellyman, J.K. Maternal bisphenol A exposure alters rat offspring hepatic and skeletal muscle insulin signaling protein abundance. Am. J. Obstet. Gynecol. 2017, 216, 290.e1–290.e9.
  66. Gray, S.P.; Denton, K.M.; Cullen-McEwen, L.; Bertram, J.F.; Moritz, K.M. Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J. Am. Soc. Nephrol. 2010, 21, 1891–1902.
  67. Nguyen, T.M.T.; Steane, S.E.; Moritz, K.M.; Akison, L.K. Prenatal alcohol exposure programmes offspring disease: Insulin resistance in adult males in a rat model of acute exposure. J. Physiol. 2019, 597, 5619–5637.
  68. Xiao, D.; Huang, X.; Li, Y.; Dasgupta, C.; Wang, L.; Zhang, L. Antenatal Antioxidant Prevents Nicotine-Mediated Hypertensive Response in Rat Adult Offspring. Biol. Reprod. 2015, 93, 66.
  69. Holloway, A.C.; Lim, G.E.; Petrik, J.J.; Foster, W.G.; Morrison, K.M.; Gerstein, H.C. Fetal and neonatal exposure to nicotine in Wistar rats results in increased beta cell apoptosis at birth and postnatal endocrine and metabolic changes associated with type 2 diabetes. Diabetologia 2005, 48, 2661–2666.
  70. Tain, Y.L.; Sheen, J.M.; Chen, C.C.; Yu, H.R.; Tiao, M.M.; Kuo, H.C.; Huang, L.T. Maternal citrulline supplementation prevents prenatal dexamethasone-induced programmed hypertension. Free Radic. Res. 2014, 48, 580–586.
  71. Chang, H.Y.; Tain, Y.L. Postnatal dexamethasone-induced programmed hypertension is related to the regulation of melatonin and its receptors. Steroids 2016, 108, 1–6.
  72. Nyirenda, M.J.; Lindsay, R.S.; Kenyon, C.J.; Burchell, A.; Seckl, J.R. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J. Clin. Investig. 1998, 101, 2174–2181.
  73. McMullen, S.; Mostyn, A. Animal models for the study of the developmental origins of health and disease. Proc. Nutr. Soc. 2009, 68, 306–320.
  74. Sengupta, P. The Laboratory Rat: Relating Its Age with Human’s. Int. J. Prev. Med. 2013, 4, 624–630.
  75. Hsu, C.N.; Tain, Y.L. The Double-Edged Sword Effects of Maternal Nutrition in the Developmental Programming of Hypertension. Nutrients 2018, 10, 1917.
  76. Langley-Evans, S.C. Critical differences between two low protein diet protocols in the programming of hypertension in the rat. Int. J. Food Sci. Nutr. 2000, 51, 11–17.
  77. Buettner, R.; Schölmerich, J.; Bollheimer, L.C. High-fat diets: Modeling the metabolic disorders of human obesity in rodents. Obesity 2007, 15, 798–808.
  78. Williams, L.; Seki, Y.; Vuguin, P.M.; Charron, M.J. Animal models of in utero exposure to a high fat diet: A review. Biochim. Biophys. Acta 2014, 1842, 507–519.
  79. Hsu, M.H.; Sheen, J.M.; Lin, I.C.; Yu, H.R.; Tiao, M.M.; Tain, Y.L.; Huang, L.T. Effects of Maternal Resveratrol on Maternal High-Fat Diet/Obesity with or without Postnatal High-Fat Diet. Int. J. Mol. Sci. 2020, 21, 3428.
  80. Tain, Y.L.; Lin, Y.J.; Sheen, J.M.; Yu, H.R.; Tiao, M.M.; Chen, C.C.; Tsai, C.C.; Huang, L.T.; Hsu, C.N. High Fat Diets Sex-Specifically Affect the Renal Transcriptome and Program Obesity, Kidney Injury, and Hypertension in the Offspring. Nutrients 2017, 9, 357.
  81. Lee, W.C.; Wu, K.L.H.; Leu, S.; Tain, Y.L. Translational insights on developmental origins of metabolic syndrome: Focus on fructose consumption. Biomed. J. 2018, 41, 96–101.
  82. Armengaud, J.B.; Yzydorczyk, C.; Siddeek, B.; Peyter, A.C.; Simeoni, U. Intrauterine growth restriction: Clinical consequences on health and disease at adulthood. Reprod. Toxicol. 2021, 99, 168–176.
  83. Bahri Khomami, M.; Joham, A.E.; Boyle, J.A.; Piltonen, T.; Silagy, M.; Arora, C.; Misso, M.L.; Teede, H.J.; Moran, L.J. Increased maternal pregnancy complications in polycystic ovary syndrome appear to be independent of obesity-A systematic review, meta-analysis, and meta-regression. Obes. Rev. 2019, 20, 659–674.
  84. Kalagiri, R.R.; Carder, T.; Choudhury, S.; Vora, N.; Ballard, A.R.; Govande, V.; Drever, N.; Beeram, M.R.; Uddin, M.N. Inflammation in Complicated Pregnancy and Its Outcome. Am. J. Perinatol. 2016, 33, 1337–1356.
  85. Saravanan, P.; Diabetes in Pregnancy Working Group; Maternal Medicine Clinical Study Group; Royal College of Obstetricians and Gynaecologists, UK. Gestational diabetes: Opportunities for improving maternal and child health. Lancet Diabetes Endocrinol. 2020, 8, 793–800.
  86. Zimmet, P.; Alberti, K.G.M.M.; Stern, N.; Bilu, C.; El-Osta, A.; Einat, H.; Kronfeld-Schor, N. The Circadian Syndrome: Is the Metabolic Syndrome and much more! J. Intern. Med. 2019, 286, 181–191.
  87. Lian, Y.; Yuan, Q.; Wang, G.; Tang, F. Association between sleep quality and metabolic syndrome: A systematic review and meta-analysis. Psychiatry Res. 2019, 274, 66–74.
  88. Scheer, F.A.; Hilton, M.F.; Mantzoros, C.S.; Shea, S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. USA 2009, 106, 4453–4458.
  89. Takahashi, J.S. Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet. 2017, 18, 164–179.
  90. Sumová, A.; Bendová, Z.; Sládek, M.; El-Hennamy, R.; Laurinová, K.; Jindráková, Z.; Illnerová, H. Setting the biological time in central and peripheral clocks during ontogenesis. FEBS Lett. 2006, 580, 2836–2842.
  91. Reiter, R.J.; Tan, D.X.; Korkmaz, A.; Rosales-Corral, S.A. Melatonin and stable circadian rhythms optimize maternal, placental and fetal physiology. Hum. Reprod. Update 2014, 20, 293–307.
  92. Okatani, Y.; Okamoto, K.; Hayashi, K.; Wakatsuki, A.; Tamura, S.; Sagara, Y. Maternal-fetal transfer of melatonin in pregnant women near term. J. Pineal Res. 1998, 25, 129–134.
  93. Hsu, C.N.; Tain, Y.L. Light and Circadian Signaling Pathway in Pregnancy: Programming of Adult Health and Disease. Int. J. Mol. Sci. 2020, 21, 2232.
  94. Hsu, C.N.; Tain, Y.L. Adverse Impact of Environmental Chemicals on Developmental Origins of Kidney Disease and Hypertension. Front. Endocrinol. 2021, 12, 745716.
  95. Kirkley, A.G.; Sargis, R.M. Environmental endocrine disruption of energy metabolism and cardiovascular risk. Curr. Diabetes Rep. 2014, 14, 494.
  96. Slotkin, T.A. Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 2004, 198, 132–151.
  97. Slabiak-Blaz, N.; Adamczak, M.; Gut, N.; Grajoszek, A.; Nyengaard, J.R.; Ritz, E.; Wiecek, A. Administration of cyclosporine a in pregnant rats—The effect on blood pressure and on the glomerular number in their offspring. Kidney Blood Press. Res. 2015, 40, 413–423.
  98. Hsu, C.N.; Chan, J.Y.H.; Wu, K.L.H.; Yu, H.R.; Lee, W.C.; Hou, C.Y.; Tain, Y.L. Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure. Int. J. Mol. Sci. 2021, 22, 2674.
  99. Watkins, A.J.; Sinclair, K.D. Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am. J. Physiol. Heart Circ. Physiol. 2014, 306, H1444–H1452.
  100. Masuyama, H.; Mitsui, T.; Eguchi, T.; Tamada, S.; Hiramatsu, Y. The effects of paternal high-fat diet exposure on offspring metabolism with epigenetic changes in the mouse adiponectin and leptin gene promoters. Am. J. Physiol. Endocrinol. Metab. 2016, 311, E236–E245.
  101. Li, X.; Shi, X.; Hou, Y.; Cao, X.; Gong, L.; Wang, H.; Li, J.; Li, J.; Wu, C.; Xiao, D.; et al. Paternal hyperglycemia induces transgenerational inheritance of susceptibility to hepatic steatosis in rats involving altered methylation on Pparα promoter. Biochim. Biophys. Acta Mol. Basis Dis. 2019, 1865, 147–160.
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You-Lin Tain
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