Leptin system is not affected by different diets in the abomasum of the sheep reared in semi-natural pastures of the Central Apennines

The adipose tissue stores energy in the body in addition to a mechanical protective function. Adipocytes also perform a wide range of metabolic functions through the production of adipokines, making the adipose tissue a real endocrine organ (Wozniak et al., 2009). The adipokines are generally defined as biologically active molecules with hormonal action, which are secreted by adipose tissue, above all by the white adipose tissue (Trayhurn et al., 2006). A molecule belonging to the adipokine group is leptin (Lep) discovered in 1994 by Zhang et al. (Zhang, et al., 1994; Trayhurn et al., 2006). Lep is a 167 amino acid protein encoded by the gene obese (Ob), and it acts by its receptor LepR, which together constitute the Lep system. Etymologically, the name leptin is derived from Greek leptos and means lean, thin, indeed, the most important factor regulating the secretion of Lep is body weight (Goumenou et al., 2002). Serving as a lipostatic factor, as lipid reserves increase, the white fat cells stimulate Lep synthesis, which signals to the hypothalamus that food intake must be reduced and stimulates energy consumption, by enhancing the release of anorexigenic factors like cocaine- and amphetamine-regulated transcript (CART) and pro-opiomelanocortin (POMC) and at the same time inhibiting the orexigenic ones, neuropeptide-Y (NPY), agouti-related protein (AgRP), and orexin (Cammisotto and Bendayan, 2012). Therefore, this molecule regulates energy metabolism and food intake by systemic action (Radin et al., 2009; Cammisotto and Bendayan, 2012), specifically by an anorexigenic action. The binding between the Lep and the LepR, in the hypothalamic satiety centers triggers the anorexigenic pathway by the activation of the JAK-STAT Pathway (Radin et al., 2009): NPY-secreting neurons in the arcuate nucleus are inhibited and the release of α-melanocyte stimulating hormone is promoted thus suppressing the appetite. LepR comprises six different isoforms (LepRa-f) sharing an identical extracellular ligand binding domain (Gorska et al., 2010). The long isoform, LepRb, allows cell signal transduction mediating most of the physiologic Lep function (Kim and Kim, 2021). LepRe is a soluble isoform representing a carrier of leptin protein capable of modulating its bioavailability (Schaab and Kratzsch, 2015). The short isoforms are mainly involved in the transport and degradation of leptin in tissues (Gorska et al., 2010).

Over time, it has been discovered that adipose tissue is not the only producer of Lep, as it has been detected in other organs like the mammary glands, placenta, ovary, pancreas, skin and stomach (Bado et al., 1998, Chilliard et al., 2005, Dall'Aglio et al., 2013, Mercati et al., 2019a, Cappai et al., 2022). The stomach represents the major source of Lep in the gastrointestinal tract (Yarandi et al., 2011) and it has been demonstrated the active role of Lep in the gastric functionality of humans and laboratory animals (Bado et al., 1998, Cinti et al., 2000). It seems to stimulate gastroprotection since it enhances mucosal integrity by increasing mucosal blood flow. The Lep in this case exerts its action after the injection of CCK-8, thus like a final factor. At the systemic level, likewise in synergy with CCK-8, the gastric Lep can take place in the short-term control of satiety, via vagal afferent fibres in the rat (Sobhani et al., 2000). Leptin may have further roles in nutrient absorption since it has effects on gastric acid (Mix et al., 2000) and gastric hormones secretion (Cammisotto et al., 2005). In addition, it has been shown that Lep regulates gastric motility since a Lep deficiency increases the rate of stomach emptying in mice (Yarandi et al., 2011). The abomasum represents the glandular stomach of ruminants and performs digestive functions like the single-chambered stomach of monogastric animals: the production of gastric juices allows the abomasum to digest dietary proteins as well as the microorganisms deriving from prestomacal compartments such as rumen. For grazing ruminants, or "grass and roughage eaters", to which the ovine species belongs, abomasum is also of fundamental importance for the denaturation of hemicelluloses by hydrochloric acid. Their diet is based mainly on pabular species that are moderately rich in hemicellulose and the denaturation of hemicelluloses allows their following digestion in the distal fermentation chamber, represented by the caecum and the proximal loop of the colon (Aguggini et al., 1998). Therefore, the full functionality of the abomasum is very important for the digestive efficiency of ruminants.

Over the last past years, much knowledge on gastric leptin has been acquired thanks to numerous studies carried out in humans and rats, leading to the definition of a regulatory role of this molecule in the control of the digestive tract and modulation of food intake. Sheep studies were not performed considering the transfer of information between species as valid. However, ruminants have quite peculiar anatomical and physiological characteristics due to the presence of a complex gastric system characterized by forestomaches and ruminal activity for which it is of particular importance to directly analyse them and acquire original data.

Given the importance of Lep in regulating the functions of the gastrointestinal tract, we propose a study carried out in the abomasum of sheep grazing on semi-natural pasture in the Central Italian Apennines. These pastures are affected by the growing summer drought that is reducing their nutritional value, by altering the distribution and quantity of the pabular species present in the grasslands. In particular, summer aridity is anticipating the moment of maximum flowering of the pasture, in which the nutritional value of the pasture is high and shortening the period between the moment of maximum flowering and maximum dryness of the pasture (Catorci et al., 2012, Scocco et al., 2016). The shortening of the period of trophic resources’ availability and the consequent reduction of their nutritional value led to a worsening of the animal health status which may not be adequate to support its production capacities. Since Lep is involved in the local regulation of the gastrointestinal tract, we studied this molecule in sheep subjected to different diets to highlight any variations that could affect animal welfare as well as to deepen the knowledge of the gastroenteric tract functions in ruminants. These insights can contribute to improve sheep management and optimize the sustainability of livestock production.

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