PMC:4195273 / 10017-31273 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/4195273","sourcedb":"PMC","sourceid":"4195273","source_url":"https://www.ncbi.nlm.nih.gov/pmc/4195273","text":"Central CART in the regulation of appetite and energy homeostasis\nA considerable amount of information has been accumulated for the role of CART in modulating metabolism via actions within the CNS. Together with several other critical neuropeptides, CART is integrated into the circuits that control the overall regulation of energy balance. The major site of action is the hypothalamic arcuate nucleus located at the base of the hypothalamus in an area where the blood-brain barrier is semi-permeable, hence uniquely assessable to circulating humoral and metabolic mediators (Barsh and Schwartz, 2002; Berthoud, 2002; Faouzi et al., 2007). As a consequence, the arcuate nucleus circuit serves as sensor of whole-body energy status represented by adiposity levels and promptly directs downstream responses accordingly through neuronal signaling to maintain a constant level of fuel stores (Schwartz et al., 2000; Barsh and Schwartz, 2002).\nTwo sets of neurons with reciprocal metabolic effects reside in the Arc, namely the orexigenic neuropeptide Y (NPY)/AgRP neurons which promote food intake and reduce energy expenditure, and the adjacent anorexigenic POMC/CART neurons that inhibit food intake and increase energy expenditure (Chronwall, 1985; Elmquist et al., 1998; Barsh and Schwartz, 2002). In response to circulating hormones, such as leptin and insulin that are secreted from adipose tissues and the pancreas, respectively, with a plasma level proportionate to body adipose stores (Zhang et al., 1994; McGregor et al., 1996; Ostlund et al., 1996), hypothalamic expression of the two sets of neurons is differentially regulated (Schwartz et al., 2000). For instance, leptin and insulin levels are reduced following food deprivation that lowers body fat stores, which inhibits POMC/CART neurons and stimulates NPY/AgRP neurons (Schwartz et al., 2000). In addition, the NPY/AgRP neurons are also subject to activation by the circulating orexigenic peptide ghrelin released from the stomach with peak levels before meal initiation (Nakazato et al., 2001).\nNPY/AGRP and POMC/CART neurons are not merely two independent sensors mediating opposing effects and projecting parallel extensions to second-order hypothalamic neuropeptide neurons, activity of the two pairs of neurons is subject to regulation by a multitude of mechanisms involved in the control of energy homeostasis. For instance, neuroanatomical studies have shown that there are intra-arcuate connections between the two neuronal subgroups, which are autoregulated by melanocortin peptides as well as local γ-aminobutyric acid (GABA)-mediated effects (Bagnol et al., 1999; Cowley et al., 2001). POMC/CART neurons express the melanocortin 3-receptor (MC3-R) which is specific for melanocortin peptides derived from the post-translational cleavage of POMC (Bagnol et al., 1999), such as the anorectic α-MSH (Fan et al., 1997; Huszar, 1997; Kim et al., 2000; Zheng et al., 2005). The activation of a subset of Arc POMC/CART neurons following exposure to leptin via leptin receptors has been reported to impose an autoinhibitory effect exerted through MC3-R activation in response to elevated release of POMC-derived peptides (Elias et al., 1998; Ahima et al., 1999; Cowley et al., 2001). However, inconsistency exists with the proposed negative autoreceptor manner of MC3-R in diminishing POMC/CART neuronal activity due to the mild increase in adiposity and body weight observed in MC3-R-deficient mice (Butler et al., 2000; Chen et al., 2000). In addition to the potential feedback mechanism described above, the inhibitory neurotransmitter GABA constitutes a principal modulator in the complex intra-arcuate circuit (Cowley et al., 2001). Subpopulations of Arc neurons harbor colocalized expression of NPY and GABA (Horvath et al., 1997), where GABA released from the orexigenic NPY/GABA terminals induces inhibitory post-synaptic currents (IPSCs) that consequently hyperpolarizing hence decreasing firing rate of the post-synaptic POMC/CART neurons (Cowley et al., 2001). Besides such direct neuronal innervations synapsing into Arc POMC/CART neurons by GABA-secreting NPY neurons (Cowley et al., 2001), a recent investigation has demonstrated the direct action of leptin on hyperpolarizing presynaptic GABAergic neurons in reducing GABA-mediated inhibitory tone to POMC/CART cells (Vong et al., 2011), whilst ghrelin was shown to trigger the opposite events on the same neurons (Cowley et al., 2003). Collectively, the electrophysiological regulation of arcuate POMC/CART neurons constitutes two primary mechanisms, including the direct effects of potent neuropeptide modulators on membrane potential through influencing ion channel activity, as well as the indirect impacts on IPSC frequency marking GABA inhibition from local NPY/GABA neurons (Cowley et al., 2001). The resultant resting action potential is purported to concurrently involve the autoregulatory effects of melanocortin peptides (Cowley et al., 2001), ultimately providing an integrated circuit at the Arc for the regulation of food intake and energy homeostasis.\nPresent in both classic neuroendocrine neurons and hypothalamic projection neurons, Arc CART displays an almost 100% colocalization with POMC and complete segregation from the more medially located orexigenic NPY in rodents (Elias et al., 1998; Vrang et al., 1999a; Fekete et al., 2000, 2004). The co-existence of CART with POMC and derivatives such as α-MSH were found to persist throughout the rostrocaudal extent of the Arc (Vrang et al., 1999a), wherein CART immunoreactivity (IR) was depicted in a separate study to pervade all α-MSH-IR perikarya and axons (Menyhért et al., 2007), which accords with the anorectic role widely adopted for POMC/CART neurons. In accordance with established neuronal projections from Arc (Schwartz et al., 2000), all α-MSH-IR axons in the PVN have also been shown to contain CART immunoreactivity (Menyhért et al., 2007).\nIn addition to co-storage with the POMC and associated cleavage products which promote negative energy balance (Fan et al., 1997; Huszar, 1997; Kim et al., 2000; Zheng et al., 2005), CART exhibits \u003e95% colocalization with the orexigenic melanin-concentrating hormone (MCH) (Qu et al., 1996; Rossi et al., 1997; Ludwig et al., 1998) at the LHA and zona incerta (ZI) (Vrang et al., 1999a; Elias et al., 2001; Menyhért et al., 2007). All MCH-positive cells showed immunoreactivity for CART in the rostral ZI and the most medial region of LHA, whilst an increasing number of non-CART MCH cells were detected in the caudal and lateral parts of the LHA apart from the CART-containing MCH neurons (Vrang et al., 1999a). In regard to the extensive hypothalamic colocalization of CART-IR with both anorexigenic and orexigenic neurotransmitters, namely POMC at the Arc and MCH at the LHA and ZI respectively, it has been hypothesized that CART co-stored within POMC-IR neurons, functions to counteract the effects of MCH in feeding stimulation, on the assumption that CART and MCH may be co-released (Shimada et al., 1998; Vrang et al., 1999a). This is supported by the observation of an elevated CART tone in the MCH-IR LHA neurons in MCH knockout mice, which exhibited anorexic tendencies marked by hypophagia and a leaner phenotype (Shimada et al., 1998; Vrang et al., 1999a). Interestingly, no colocalization was found between CART and another orexigenic peptide confined to neurons in the LHA, orexin B (de Lecea et al., 1998; Peyron et al., 1998; Sakurai et al., 1998; Vrang et al., 1999a), which increases in transcription activity during fasting to elicit stimulatory effects on feeding (Sakurai et al., 1998).\nColocalization experiments exploring the resemblance of CART distribution in feeding-related neuronal groups of the human hypothalamus revealed that, while overlap is seen in certain areas, some striking differences in colocalization pattern also exist (Charnay et al., 1999; Elias et al., 2001; Menyhért et al., 2007). For example, the close overlap of CART and POMC expression in rodents is not so obvious in the human brain (Mihaly et al., 2000; Menyhért et al., 2007). In particular, CART expression could not be detected in the perikarya and axons of α-MSH-IR neurons but interestingly was found in approximately 30% of NPY/agouti-related protein (AgRP) neurons (Mihaly et al., 2000) in the human infundibular nucleus analogous to the Arc in rodents (Menyhért et al., 2007). However, similar co-expression patterns of CART and other neurotransmitters between human and rodents were seen in the PVN region (Menyhért et al., 2007). Intriguingly, the co-expression of CART in NPY/AgRP instead of POMC neurons of the Arc was also observed in other primates such as monkeys (Grayson et al., 2006). Comparable with the observation in rodents, CART was demonstrated to colocalize with MCH in the lateral hypothalamus of humans, particularly in the perifornical region where up to 50% overlap in immunoreactivities of the two peptides was detected (Menyhért et al., 2007). In the infundibular nucleus, fibers comprising MCH-IR were also observed in a portion of CART-IR axons, suggestive of lateral hypothalamic origin (Menyhért et al., 2007).\nIt is of particular interest that CART in humans has been shown to exhibit the contrasting colocalization with the orexigenic NPY/AgRP neurons and complete segregation from POMC-containing cells in the infundibular nucleus analogous to the rodent arcuate nucleus, whilst co-storage with MCH remained in the lateral hypothalamus. Speculations entailing an orexigenic role of CART as well as the involvement in other functions have therefore arisen, which is supported by the elevated food intake following CART administration to the PVN even in rodents (Stanley et al., 2001). Such paradoxical potentials of CART in feeding behaviors as evident in multiple pharmacological and physiological studies will be discussed subsequently in the present review. With regard to the resembling colocalization with the orexigenic MCH in the LHA consistent across species investigated (Ludwig et al., 1998; Vrang et al., 1999a; Elias et al., 2001; Menyhért et al., 2007), although CART expression appeared unaffected by alterations in energy homeostasis in the MCH neurons in rodents, MCH administration effectively blocked intracerebroventricular CART-induced stimulation of central dopaminergic neurons (Yang and Shieh, 2005). Indeed, lateral hypothalamic CART synthesis has been linked to the regulation of dopaminergic reward pathways (Philpot and Smith, 2006), where psychostimulant-like effects were modulated by CART through moderating the activities of dopaminergic neurons (Jaworski et al., 2003; Dominguez et al., 2004b; Kuhar et al., 2005). Thus, while possibility exists that CART and MCH may participate in regulating different physiological functions effectuated by the same neuronal groups, anatomical and functional interplay of the two peptides has been indicated to prevail in the interactions between food intake and reward neurocircuitries (Saper et al., 2002; Yang and Shieh, 2005; Pang and Han, 2012). Knowledge regarding the underlying cellular mechanisms awaits further extension through neuronal mapping and biochemical studies.\nWhile the role of CART in controlling appetite and energy homeostasis in the human system might be somewhat different, in rodents, the neuronal network in which CART is involved to modulate energy homeostasis has been well-described. The expression of endogenous CART at brain regions involved in feeding regulation has been shown to be sensitive to the energy balance status and the genetic background of mice. In brief, fasting has been documented in various mammals to reduce CART mRNA levels at the hypothalamic PVN, Arc, perifornical region, as well as the nucleus accumbens shell (AcbSh) of the striatum, whilst refeeding restored the expression (Kristensen et al., 1998; Lambert et al., 1998; Adams et al., 1999; Vrang et al., 1999a, 2000; Henry et al., 2001; Li et al., 2002; Yang and Shieh, 2005; Van Vugt et al., 2006; Germano et al., 2007). As a leptin-regulated neurotransmitter, the expression of CART mRNA and peptide levels at the Arc is described to be positively correlated with circulating leptin levels (Kristensen et al., 1998; Ahima et al., 1999; Ahima and Hileman, 2000; Rohner-Jeanrenaud et al., 2002; Wortley et al., 2004). This relationship between leptin and CART levels was less consistently demonstrated at the PVN and LHA (Wortley et al., 2004), despite evidence supporting a pivotal role of CART-containing neurons projecting from the Arc to the second order neurons located in the PVN and LHA in producing anorexia (Elias et al., 1999; Wang et al., 2000; Fekete et al., 2004). Intravenous leptin administration was shown to induce Fos expression in hypothalamic CART neurons in the PVN, DMH, Arc, and the ventral premammillary nucleus (Elias et al., 1998, 2001). Whilst Arc CART mRNA and peptide levels were strongly downregulated in food-deprived animals, the transcripts were nearly absent in genetically obese fa/fa rats and ob/ob mice with disrupted leptin signaling, wherein daily intraperitoneal leptin treatment led to CART restoration in the Arc and DMH (Friedman and Halaas, 1998; Kristensen et al., 1998; Ahima et al., 1999; Ahima and Hileman, 2000; Rohner-Jeanrenaud et al., 2002), suggesting that leptin-induced anorexigenic actions may be mediated via CART neurons at the Arc. In comparison, in the anx/anx anorexia mouse model characterized by marked reduction in feeding and premature death, CART expression was significantly lower in the Arc, and less prominently in the DMH and LHA regions (Johansen et al., 2000). The reduced Arc CART expression, together with downregulated serum leptin levels, was attributed to a compensatory response to the energy-deprived state, as well as a probable molecular defect in the Arc deregulating the cellular source of CART mRNA (Johansen et al., 2000). In contrast with genetically obese animal models, diet-induced obese (DIO) rodents subjected to a high fat diet (HFD) have been shown to display higher Arc CART mRNA levels compared with lean animals fed a low fat diet, due to hyperleptinaemia (Rohner-Jeanrenaud et al., 2002; Wortley et al., 2004; Hou et al., 2010). Elevated CART transcript levels were also found in normal-weight obesity-prone rats compared to obesity-resistant subjects, where the Arc leptin-CART pathway was proposed to respond to fat-rich dietary intervention through inhibiting excessive body fat accrual by substituting lipid storage with lipid mobilization (Rohner-Jeanrenaud et al., 2002; Wortley et al., 2004).\nDespite purported relevance of CART in the modulation of gastrointestinal (GI) function, it is at present unclear the definite roles of enteric CART in intestinal motility, satiety and feeding behavior (Okumura et al., 2000; Ekblad et al., 2003; Smedh and Moran, 2003; Tebbe et al., 2004). Convincing evidence supporting the GI effects of CART have been provided by independent investigations, where central injections of CART in rodents elicited an anorexigenic response accompanied by the inhibition of gastric emptying and gastric acid secretion (Okumura et al., 2000; Asakawa et al., 2001; Smedh and Moran, 2003), while colonic motility measured by colonic transit time was accelerated (Tebbe et al., 2004). Contrary to a local ENS effect, such alterations in GI functions were indicated to be conveyed through CART acting in the CNS (Okumura et al., 2000; Ekblad et al., 2003; Smedh and Moran, 2003, 2006; Tebbe et al., 2004), as intraperitoneal (i.p.) CART administration failed to reduce food consumption or reproduce similar gastric responses (Okumura et al., 2000; Tebbe et al., 2004; Skibicka et al., 2009). Furthermore, pretreatment with central injection of CRH receptor antagonist prior to central CART administration completely abolished the CART-induced gastric effects, suggesting a central CART-directed CNS modulation of the digestive tract behavioral motor functions via CRH-dependent mechanisms (Okumura et al., 2000; Smedh and Moran, 2003, 2006; Tebbe et al., 2004).\nConsistent with a potential CART pathway connecting gut-brain signals in the control of food intake, co-expression of CART and the satiety factor cholescystokinin (CCK)-1 receptors has been detected in the f afferent neurons in rodents (Crawley et al., 1991; Moran et al., 1992; Mercer and Beart, 1997; Koylu et al., 1998; Broberger et al., 1999; Dun et al., 2001; Lodge and Lawrence, 2001; Zheng et al., 2002; de Lartigue et al., 2007). Substantially, the synergistic effect of CART and the anorexigenic gut hormone CCK (Crawley and Corwin, 1994) on food intake regulation analogous to that documented for leptin and CCK (Barrachina et al., 1997; Broberger et al., 1999; Morton et al., 2005; Merino et al., 2008) has been demonstrated in animal studies, during which the responses to simultaneous as well as separate central administration of CART peptide and the CCK octapeptide (CCK-8) through cannula implantation (Maletinska et al., 2007) were compared (Volkoff, 2006; Maletinska et al., 2008). In fasted lean mice, the anorexigenic effect induced by CART delivery was significantly enhanced by parallel CCK-8 injection when compared with the administration of each particular peptide alone, while the additive reaction was also shown in an open field test where locomotor activity of the subjects was inhibited (Maletinska et al., 2008). On the contrary, application of the CCK-1 receptor antagonist devazepide blocked CART-induced alteration in food intake (Maletinska et al., 2008). Such long-lasting cooperative action on feeding was speculated to associate in turn with the synergistic effect of leptin on CCK-induced satiety, where CART release from the nodose ganglia was mediated by the interaction of low-affinity vagal CCK-1 receptors and leptin receptors to produce short-term satiety (Maletinska et al., 2008; Heldsinger et al., 2012). Furthermore, 17 and 41% of vagal afferent neurons projecting from the nodose ganglia to the stomach and duodenum respectively were identified to be CART-immunoreactive (Zheng et al., 2002). The vagus has been proposed a mediator of the dorsal hindbrain action of CART on gastric motor function, as indicated by the inhibitory gastric effects of hindbrain intracerebroventricular (i.c.v.) CART microinfusion, which was blocked by subdiaphragmatic vagotomy (Smedh and Moran, 2003, 2006). In particular, the dorsal vagal complex (DVC) was demonstrated to be a target site for both CART and CRH in the suppression of gastric emptying, where effective inhibition occurred in response to the intraparenchymal injection of either peptide into the DVC, at a lower dose compared to that required to elicit a noticeable inhibitory effect by hindbrain i.c.v. administration (Smedh and Moran, 2006).\nReciprocal of a central CART-directed modulation of gastric behavior in feeding regulation, the anorectic actions of central CART have also been proposed to result from stimulation by gut hormones (Hunter et al., 2004). Following food intake, CCK released in the GI tract has been delineated to direct CART release from central vagal afferents, where an abundance of CCK-1 receptor mRNA expression was detected in the nodose ganglion (Broberger et al., 1999; Hunter et al., 2004). CCK-borne information is then mediated by CART to the hindbrain sites where suppression of food intake is elicited (Broberger et al., 1999; Hunter et al., 2004). However, the role of CART released from vagal afferent terminals in the commissural part of the nucleus of the solitary tract (NTS) was suggested to be minor in mediating vagal satiety signals, as a diminished suppression of food intake was exerted by direct NTS subnuclei CART injections compared to hindbrain i.c.v. CART (Zheng et al., 2001, 2002; Skibicka et al., 2009). Thus, the potential function of CART on satiation may involve a distal site of action as well as interaction with other nutritional transmitters critical for vagally-mediated gastrointestinal satiety (Broberger et al., 1999; Zheng et al., 2002). For instance, induction of CART immunoreactivity was readily demonstrated upon CCK administration both in rats and cultured vagal afferent neurons in a state of energy restriction, while refeeding of starved animals markedly increased CART immunoreactivity via a CCK-1 receptor antagonist-sensitive mechanism (de Lartigue et al., 2007, 2010). In addition, introduction of the orexigenic peptide ghrelin inhibited CCK-mediated CART stimulation (de Lartigue et al., 2007), illustrating an interplay between gastrointestinal orexigenic and anorexic peptides in modulating CART expression. In particular, immunoreactive CART neurons have been shown to display differential quantities during developmental changes in the dorsal motor nucleus of the vagus (DMNV), wherein vagal preganglionic neurons are responsible for regulating various ingestive behaviors through innervations in the GI tract (Dun et al., 2001; Zheng et al., 2002). Such descending expression levels upon maturation indicate a potential signaling role of CART critical in the early post-natal development (Dun et al., 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