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Oxidative Stress-Induced Hypertension of Developmental Origins: History
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Subjects: Biochemistry & Molecular Biology
Contributor: You-Lin Tain

Hypertension remains the leading cause of disease burden worldwide. Hypertension can originate in the early stages of life. A growing body of evidence suggests that oxidative stress, which is characterized as a reactive oxygen species (ROS)/nitric oxide (NO) disequilibrium, has a pivotal role in the hypertension of developmental origins. Results from animal studies support the idea that early-life oxidative stress causes developmental programming in prime blood pressure (BP)-controlled organs such as the brain, kidneys, heart, and blood vessels, leading to hypertension in adult offspring. Conversely, perinatal use of antioxidants can counteract oxidative stress and therefore lower BP. 

  • antioxidant
  • hypertension
  • nitric oxide
  • asymmetric dimethylarginine
  • oxidative stress
  • developmental origins of health and disease (DOHaD)
  • reactive oxygen species
  • renin-angiotensin system

1. Introduction

Hypertension is the number one risk factor for global deaths, affecting one in three adults across the world [1][2]. Significant interest has recently focused on the fact that the origins of hypertension can begin in early life [3][4][5]. Now this concept, based on observing that the developing fetus being exposed to adverse conditions in utero increases the risk for chronic diseases happening later in life, has been termed as the “developmental origins of health and disease (DOHaD)” [6]. The hypertension of developmental origins can be programmed by a number of modifiable environmental risk factors [7][8][9][10], especially those linked to maternal nutrition. Notably, the DOHaD concept, besides determining the early-life risk for the developmental programming of hypertension, offers a novel way to prevent hypertension by reprogramming therapy [11]. By switching therapy from adulthood to early life prior to illness onset, we have the potential to reverse adverse programming processes that would lead to hypertension. Accordingly, one may assume that early reprogramming therapy serves as an innovative strategy to reduce the burden of hypertension globally.
A growing body of evidence shows that oxidative stress plays a pivotal role in the pathogenesis of hypertension [12][13][14][15]. The overproduction of deleterious reactive oxygen and nitrogen species (ROS and RNS) that overwhelm the cellular antioxidant capacity results in pathogenic oxidative stress [16]. Experimental evidence supports that a ROS/nitric oxide (NO) disequilibrium under oxidative stress favors oxidation reactions involved in major blood pressure (BP)-controlled organs such as the brain, kidneys, heart, and blood vessels, underpinning the development of hypertension [12][13][14][15]. Conversely, treatment with antioxidants has been suggested to lower oxidative stress and therefore BP [16][17].
Although cumulative evidence has shown the impact of oxidative stress and antioxidant therapy in established hypertension [12][13][14][15][16][17][18], less attention has been paid to their implications in the hypertension of developmental origins. Therefore, the purpose of the current research is to highlight the best available evidence on the interaction between oxidative stress and the developmental programming of hypertension. In this research, attempts will be made to discuss the role of oxidative stress in the hypertension of developmental origins, its associations with the core mechanisms of developmental programming behind hypertension, and the potential of antioxidant therapy as a novel preventive strategy for the hypertension of developmental origins.

2. Oxidative-Stress-Related Hypertension of Developmental Origins

2.1. Oxidative Stress during Pregnancy

Fetal oxygen requirements vary at various stages of pregnancy [19]. During the first trimester, fetal oxygen levels are low. However, increasing oxygen need happens, during the second and third trimesters, for the formation of fetal-placental circulation and the rapid gain of fetal weight [20]. Oxidative damage occurs in a compromised pregnancy owing to the failure of defensive antioxidant mechanisms in responding to excessive ROS and RNS [21]. Many adverse conditions in pregnancy result in increased oxidative stress, including obesity, diabetes, preeclampsia, maternal smoking, and intrauterine growth retardation (IUGR) [22]. Accordingly, oxidative stress adversely affects the developing fetus, resulting in adult disease in later life [10][23].

2.2. Evidence from Human Studies

The association between the hypertension of developmental origins and low birth weight (LBW) was first highlighted by David Barker and colleagues in the late 1980s [24]. Another important observation from the Dutch Hunger Winter Study was that maternal undernutrition has lasting, negative effects on offspring health, including hypertension [25]. Additionally, several mother-child cohorts provide important support for the developmental programming of hypertension. A variety of early-life risks associated with offspring hypertension have been acknowledged, including maternal smoking [26], maternal obesity [27], low vitamin D consumption [28], gestational hypertension [29], IUGR [30], and short-term breastfeeding [31].
Although human observational studies provide relevant evidence correlating early-life factors with the developmental programming of hypertension, the direct cause-and-effect relationships between oxidative stress and offspring hypertension that drive programming processes cannot be established and therefore it is difficult to identify a potential reprogramming strategy.

2.3. Evidence from Animal Studies

In recent years, our understanding of the molecular mechanisms behind the hypertension of developmental origins has grown by using animal models [32][33]. These mechanisms contain oxidative stress, reduced nephron number, aberrant activation of the RAS, dysregulated nutrient-sensing signals, gut microbiota dysbiosis, and so on [9][10][11][32]. Among them, oxidative stress has a crucial role and is closely interconnected to other core mechanisms behind the hypertension of developmental origins.
The present entry is limited to adverse early-life insults beginning in pregnancy and lactation, with a focus on the oxidative-stress-related hypertension of developmental origins.
Maternal nutritional insults are the leading causes of the oxidative-stress-related hypertension of developmental origins in animal models. Under- and over-nutrition can both induce nutritional programming [34]. These nutritional risk factors include calorie restriction [35][36][37][38], protein restriction [39], and a diet high in fructose [40][41][42][43], fat [44][45], salt [46][47], or methyl-donors [48]. Another factor interfering with oxidative stress programming is maternal illness. Maternal diabetes [49][50][51], preeclampsia [52], CKD [53][54], and hypertension [55][56] have been reported to induce oxidative stress and the hypertension of developmental origins concurrently. Additionally, pregnancy complications such as reduced uterine perfusion [57], inflammation [58], and hypoxia [59][60][61] are also relevant to oxidative-stress-related programmed hypertension. Offspring hypertension can also be programmed by dams exposed to environmental chemicals, such as 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) [62], bisphenol A [63], and di-n-butyl phthalate [64]. Moreover, medication use such as glucocorticoid can program the hypertension of developmental origins [49][50][51][65][66].

2.4. Mechanisms Underpinning Oxidative Stress in Hypertension of Developmental Origins

There are several oxidative-stress-mediated mechanisms involved in the pathogenesis of programmed hypertension, including increased ROS [51][42][56][64][66], increased ROS-producing enzyme expression [38][41][67][57][55][47], decreased antioxidant capabilities [51][44][67][47], an impaired ADMA–NO pathway [35][36][37][68][49][51][52][40][53][54][69][70][71][62][63][66][60][61], increased peroxynitrite [37][50][55][46], and increased oxidative damage [72][35][36][39][50][40][41][43][48][53][54][44][70][71][62][63][57][45][55][47][65][59].
3-nitrotyrosine (3-NT) is a marker of oxidative stress formed due to the nitration of protein-bound and free tyrosine residues by reactive peroxynitrite molecules [73].
Prior work indicates that ADMA-related NO–ROS imbalance in early life induces adulthood hypertension [74]. Several studies support the notion that ADMA is a key risk factor related to oxidative stress programming in various programming models, such as caloric restriction [35][36], diabetes [49], preeclampsia [52], maternal CKD [53][54], combined dexamethasone and TCDD exposure [62], prenatal bisphenol A exposure and high-fat diet [63], and high-salt diet [46]. NO deficiency in the vessels [37] and kidneys [69] is also relevant to the hypertension of developmental origins.
Several frequently used markers of lipid peroxidation have been used to detect oxidative damage in models of programmed hypertension, including F2-isoprostanes [72][39], thiobarbituric acid reactive substances (TBARS) [50], malondialdehyde (MDA) [41][44][47], and 4-hydroxynonenal (4-NHE) [65]. In addition, 8-hydroxydeoxyguanosine (8-OHdG) is the most frequently detected and studied oxidized nucleoside of DNA [75]. Maternal caloric restriction [35][36], a high-fructose diet [40], a maternal methyl-deficient or donor-rich diet [48], CKD [53][54], prenatal dexamethasone exposure [70][71][62], combined dexamethasone and TCDD exposure [62], prenatal bisphenol A exposure and high-fat diet [63], and high-fat diet [45] have been shown to give rise to programmed hypertension in the presence of increased 8-OHdG expression.
It is noteworthy that most studies have mainly focused on the renal and cardiovascular systems; rather less attention has been paid to oxidative stress programming on other organ systems, including the brain [41][55][65], spleen [42], and adrenal glands [67].

2.5. Oxidative-Stress-Induced Renal Programming

During development, the fetal kidney is susceptible to adverse early-life events, leading to changes in structure and function, namely renal programming [76]. Renal programming is the most commonly studied mechanism behind the hypertension of developmental origins [4][5][11]. A reduced nephron number can develop during pregnancy through childhood to later life in different animal models of renal programming [77]. Maternal insults need only last for 1–2 days to impair nephrogenesis, resulting in a permanent reduction in the nephron number [78]. Accordingly, the main phenotype of renal programming associated with a reduced nephron number is hypertension [77].
An impaired ADMA–NO pathway is tightly linked to oxidative stress in determining renal programming [74]. NO deficiency in pregnancy induced by NOS inhibitor NG-nitro-l-arginine methyl ester (L-NAME) caused renal programming, coinciding with increased oxidative stress in adult offspring [72]. Additionally, maternal NO deficiency was able to modify more than 2000 renal transcripts in a 1-day-old offspring kidney. It has been found that several genes belonging to the RAS and arachidonic acid metabolism pathway contribute to the pathogenesis of programmed hypertension [72]. In a prenatal dexamethasone exposure model [69][78], offspring rats developed hypertension coinciding with a reduced nephron number, increased plasma ADMA levels, and reduced renal NO production. Likewise, the links between oxidative stress and a reduced nephron number have been reported in a caloric restriction model [35] and a streptozotocin-induced diabetes model [49]. Moreover, the researchers' prior work has demonstrated that ADMA can impair nephrogenesis [49]. Metanephroi grown in 2 or 10 µM ADMA displayed reduced nephron numbers in a dose-dependent manner [49]. When we treated cultured metanephroi with 10 µM ADMA, the next-generation sequencing (NGS) analysis identified 1221 differential expressed genes [79]. Among them, Ephx2, Avpr1a, Npy1r, Hba2, and Hba-a2, have been linked to programmed hypertension in other models [80][81]. Together, these observations support the notion that oxidative-stress-induced renal programming contributes to the hypertension of developmental origins.

2.6. Oxidative-Stress-Induced Cardiovascular Programming

The fetal cardiovascular system is similar to the developing kidneys with great vulnerability to adverse in utero conditions [82]. Oxidative stress may mediate developmental plasticity in the CV system with structural and functional changes during the organogenesis of the heart–vascular system, leading to endothelial dysfunction, a stiffer vascular tree, fewer cardiomyocytes, and small coronary arteries, through cardiovascular programming [82][83][84]. 
In the maternal caloric restriction model, offspring displayed high BP accompanied with a decrease in NOS activity in the microvessels and increased cardiac xanthine-oxidase expression [37][38]. Another study showed that adult offspring born to diabetic dams developed hypertension related to an increased ROS level and decreased SOD expression and NO bioavailability in mesenteric arteries [51]. Moreover, developmental hypoxia has been reported to impair the NO pathway and endothelial function, consequently programming hypertension in the adult offspring of chickens and sheep [60][61]. In rats and mice, cardiovascular maturation continues past birth, becoming completed by the second week postnatally. Unlike rodents, chickens and sheep share similar temporal windows of precocial cardiovascular development and maturation with humans [85]. Therefore, cardiovascular data derived from these two models provide a useful translation to the human situation.
In addition, endothelium-dependent hyperpolarization (EDH), a dominant vasodilator in resistance arteries, is also involved in the regulation of BP. Considering that oxidative stress impairs EDH during hypertension in some vessels [86], reduced EDH might contribute to the oxidative-stress-induced hypertension of developmental origins. Indeed, a previous study has shown that offspring exposed to a high-fat diet display reduced EDH and BP elevation concurrently, despite the mechanisms of oxidative stress remaining undetermined [87].

2.7. Other Mechanisms Related to Oxidative Stress Programming

Considering a wide spectrum of early-life insults create similar outcomes (i.e., hypertension) in adult offspring, it is logical to think that common mechanisms contribute to the hypertension of developmental origins. In addition to oxidative stress, several mechanisms have been proposed, including glucocorticoid effect, aberrant RAS, dysregulated nutrient-sensing signals, gut microbiota dysbiosis, etc. [4][5][10][11][88][32]. Among them, oxidative stress plays a decisive role and is tightly interconnected to other core molecular pathways involved in the hypertension of developmental origins (Figure 1).
/media/item_content/202203/62313df15dd5dantioxidants-11-00511-g002.png
Figure 1. Oxidative stress and possible molecular pathways linked to the hypertension of developmental origins.
First, several studies have linked increased fetal glucocorticoid exposure to the developmental programming of hypertension in adult offspring [67][69][70][71][62][65][66]. One previous study reported that programmed male offspring exhibited reduced antioxidant glutathione peroxidase 1 (Gpx1) expression and increased NADPH-oxidase expression in the adrenal glands [67]. Second, the aberrant activation of the RAS is a well-known mechanism underlying the hypertension of developmental origins [88]. In a maternal hypertension model, offspring hypertension was found to be related to increased expression of angiotensin II type 1 receptor (AT1R) and oxidative-stress-related protein in the brain [55]. Conversely, an early blockade of the RAS by renin inhibitor aliskiren mitigates increases in ADMA and restores NO bioavailability, contributing to the decrease in BP in young spontaneously hypertensive rats (SHRs) [89].
Dysregulated nutrient-sensing signals are also involved in the development of hypertension [83]. In a maternal high-fructose model, the dysfunction of AMP-activated protein kinase (AMPK)-regulated AT1R expression and sirtuin 1 (SIRT1)-mediated mitochondrial biogenesis coincided with increased oxidative stress in RVLM, which in turn increased sympathetic activity and BP in offspring [41]. Besides, a maternal high-fructose diet was found to decrease expression of AMPK, SIRT4, and peroxisome proliferator-activated receptors (PPARs) in offspring kidneys [43].
Furthermore, recent evidence indicates that early development of the gut microbiota influences the development of hypertension [90][91]. Data from several animal models indicate that the interactions between gut microbiota dysbiosis and oxidative stress may contribute to the pathogenesis of programmed hypertension, such as maternal CKD [53], high-fructose diet [43], and high-fat diet [92] models.

This entry is adapted from the peer-reviewed paper 10.3390/antiox11030511

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