Guijarro Ana, Laviano Alessandro, Meguid Michael M
Surgical Metabolism and Nutrition Laboratory, Neuroscience Program, University Hospital, SUNY Upstate Medical University, 750 Adams St., Syracuse, NY 13210, USA.
Prog Brain Res. 2006;153:367-405. doi: 10.1016/S0079-6123(06)53022-5.
The immune and neuroendocrine systems are closely involved in the regulation of metabolism at peripheral and central hypothalamic levels. In both physiological (meals) and pathological (infections, traumas and tumors) conditions immune cells are activated responding with the release of cytokines and other immune mediators (afferent signals). In the hypothalamus (central integration), cytokines influence metabolism by acting on nucleus involved in feeding and homeostasis regulation leading to the acute phase response (efferent signals) aimed to maintain the body integrity. Peripheral administration of cytokines, inoculation of tumor and induction of infection alter, by means of cytokine action, the normal pattern of food intake affecting meal size and meal number suggesting that cytokines acted differentially on specific hypothalamic neurons. The effect of cytokines-related cancer anorexia is also exerted peripherally. Increase plasma concentrations of insulin and free tryptophan and decrease gastric emptying and d-xylose absorption. In addition, in obesity an increase in interleukin (IL)-1 and IL-6 occurs in mesenteric fat tissue, which together with an increase in corticosterone, is associated with hyperglycemia, dyslipidemias and insulin resistance of obesity-related metabolic syndrome. These changes in circulating nutrients and hormones are sensed by hypothalamic neurons that influence food intake and metabolism. In anorectic tumor-bearing rats, we detected upregulation of IL-1beta and IL-1 receptor mRNA levels in the hypothalamus, a negative correlation between IL-1 concentration in cerebro-spinal fluid and food intake and high levels of hypothalamic serotonin, and these differences disappeared after tumor removal. Moreover, there is an interaction between serotonin and IL-1 in the development of cancer anorexia as well as an increase in hypothalamic dopamine and serotonin production. Immunohistochemical studies have shown a decrease in neuropeptide Y (NPY) and dopamine (DA) and an increase in serotonin concentration in tumor-bearing rats, in first- and second-order hypothalamic nuclei, while tumor resection reverted these changes and normalized food intake, suggesting negative regulation of NPY and DA systems by cytokines during anorexia, probably mediated by serotonin that appears to play a pivotal role in the regulation of food intake in cancer. Among the different forms of therapy, nutritional manipulation of diet in tumor-bearing state has been investigated. Supplementation of tumor bearing rats with omega-3 fatty acid vs. control diet delayed the appearance of tumor, reduced tumor-growth rate and volume, negated onset of anorexia, increased body weight, decreased cytokines production and increased expression of NPY and decreased alpha-melanocyte-stimulating hormone (alpha-MSH) in hypothalamic nuclei. These data suggest that omega-3 fatty acid suppressed pro-inflammatory cytokines production and improved food intake by normalizing hypothalamic food intake-related peptides and point to the possibility of a therapeutic use of these fatty acids. The sum of these data support the concept that immune cell-derived cytokines are closely related with the regulation of metabolism and have both central and peripheral actions, inducing anorexia via hypothalamic anorectic factors, including serotonin and dopamine, and inhibiting NPY leading to a reduction in food intake and body weight, emphasizing the interconnection of the immune and neuroendocrine systems in regulating metabolism during infectious process, cachexia and obesity.
免疫系统和神经内分泌系统在周围及下丘脑中枢水平的代谢调节中密切相关。在生理状态(进食)和病理状态(感染、创伤和肿瘤)下,免疫细胞均会被激活,释放细胞因子和其他免疫介质(传入信号)。在下丘脑(中枢整合),细胞因子通过作用于参与进食和稳态调节的核团影响代谢,引发旨在维持机体完整性的急性期反应(传出信号)。外周给予细胞因子、接种肿瘤和诱导感染,通过细胞因子的作用改变正常的食物摄入模式,影响餐量和进餐次数,这表明细胞因子对特定的下丘脑神经元有不同的作用。细胞因子相关的癌症厌食症的影响也作用于外周。胰岛素和游离色氨酸的血浆浓度升高,胃排空和d -木糖吸收降低。此外,肥胖时肠系膜脂肪组织中白细胞介素(IL)-1和IL-6增加,这与皮质酮增加一起,与肥胖相关代谢综合征的高血糖、血脂异常和胰岛素抵抗有关。下丘脑神经元能感知循环中营养物质和激素的这些变化,进而影响食物摄入和代谢。在患厌食症的荷瘤大鼠中,我们检测到下丘脑IL-1β和IL-1受体mRNA水平上调,脑脊液中IL-1浓度与食物摄入量呈负相关,且下丘脑5-羟色胺水平升高,肿瘤切除后这些差异消失。此外,5-羟色胺与IL-1在癌症厌食症的发生过程中存在相互作用,同时下丘脑多巴胺和5-羟色胺的产生增加。免疫组织化学研究表明,荷瘤大鼠下丘脑一级和二级核团中神经肽Y(NPY)和多巴胺(DA)减少,5-羟色胺浓度增加,而肿瘤切除可逆转这些变化并使食物摄入恢复正常,这表明厌食期间细胞因子对NPY和DA系统有负调节作用,可能由5-羟色胺介导,5-羟色胺似乎在癌症患者的食物摄入调节中起关键作用。在不同的治疗形式中,已对荷瘤状态下饮食的营养调控进行了研究。给荷瘤大鼠补充ω-3脂肪酸与对照饮食相比,延迟了肿瘤的出现,降低了肿瘤生长速率和体积,消除了厌食症的发作,增加了体重,减少了细胞因子的产生,增加了NPY的表达,并降低了下丘脑核团中α-黑素细胞刺激素(α-MSH)的水平。这些数据表明,ω-3脂肪酸通过使下丘脑与食物摄入相关的肽正常化,抑制促炎细胞因子的产生并改善食物摄入,并指出了这些脂肪酸治疗应用的可能性。这些数据总和支持这样一种概念,即免疫细胞衍生的细胞因子与代谢调节密切相关,具有中枢和外周作用,通过下丘脑厌食因子(包括5-羟色胺和多巴胺)诱导厌食,并抑制NPY导致食物摄入和体重减少,强调了免疫和神经内分泌系统在感染过程、恶病质和肥胖期间调节代谢中的相互联系。