微生物组成、功能和应激复原力或易感性:揭示性别特异性模式。

IF 4.9 2区 医学 Q1 ENDOCRINOLOGY & METABOLISM Biology of Sex Differences Pub Date : 2024-02-26 DOI:10.1186/s13293-024-00590-7
Arax Tanelian, Bistra Nankova, Mariam Miari, Esther L Sabban
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引用次数: 0

摘要

背景:遭受创伤性压力后,女性患情绪障碍的几率是男性的两倍。然而,个体对这种压力的反应各不相同,有些人会出现由压力引起的精神病态,而有些人则表现出抗压能力。影响情感障碍中与性别有关的差异以及复原力差异的因素仍不清楚;不过,新出现的证据表明,肠道微生物群的差异在其中发挥了作用。在这项研究中,我们利用创伤后应激障碍的单次长期应激(SPS)模型,研究了影响男女应激易感性或复原力的微生物组成、功能和代谢物的前后差异:雄性和雌性 Sprague-Dawley 大鼠被随机分配到对照组或 SPS 组。SPS两周后,对动物进行一系列行为测试,一天后将其斩首。根据大鼠的焦虑指数,将它们进一步分为 SPS 抗性组(SPS-R)和 SPS 易感组(SPS-S)。解剖当天,分离盲肠和部分脑组织。在接触 SPS 之前和之后采集粪便样本,在接触 SPS 之前和 30 分钟后采集尿液样本:结果:在接触 SPS 之前,交感肾上腺轴仅在男性亚组中出现了变化。SPS-S男性大脑中紧密连接蛋白claudin-5的表达量较低,而SPS-R女性大脑中紧密连接蛋白claudin-5的表达量较高。在整个研究过程中,与女性相比,男性的α多样性一直较低。Beta 多样性显示,在 SPS 之前,男性和女性易感群体之间存在明显的分离,而在 SPS 之后,这种分离在抗病群体中变得更加明显。在属一级,乳酸杆菌、Lachnospiraceae_Incertae_Sedis 和 Barnesiella 表现出性别特异性变化,在每种性别中的丰度相反。此外,在 SPS 前后,微生物的预测功能和目标功能模块都发生了性别特异性变化。还观察到微生物短链脂肪酸(SCFAs)的变化,易受 SPS 影响的雄性微生物的主要和次要 SCFAs 较低,而易受 SPS 影响的雌性微生物的支链 SCFAs 较高:本研究强调了与雌雄大鼠应激复原力相关的微生物组成、功能和代谢物在创伤前后的明显差异。这些发现强调了开发针对不同性别的治疗策略以有效解决应激相关疾病的重要性。亮点 SPS 模型诱导雄性和雌性啮齿动物对创伤性应激做出不同的焦虑和社会行为反应。与具有 SPS 抵抗能力的雄性啮齿动物相比,具有 SPS 抵抗能力的雌性啮齿动物表现出的焦虑行为更少,与幼鼠的互动也更多。在易感大鼠和抗应激大鼠中,观察到了肠道微生物组成和预测功能的性别差异。对 SPS 有抵抗力的雄性大鼠的盲肠乙酸盐含量升高,而对 SPS 易感的雌性大鼠的支链 SCFAs 含量升高。
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Microbial composition, functionality, and stress resilience or susceptibility: unraveling sex-specific patterns.

Background: Following exposure to traumatic stress, women are twice as likely as men to develop mood disorders. Yet, individual responses to such stress vary, with some people developing stress-induced psychopathologies while others exhibit resilience. The factors influencing sex-related disparities in affective disorders as well as variations in resilience remain unclear; however, emerging evidence suggests differences in the gut microbiota play a role. In this study, using the single prolonged stress (SPS) model of post-traumatic stress disorder, we investigated pre- and post-existing differences in microbial composition, functionality, and metabolites that affect stress susceptibility or resilience in each sex.

Methods: Male and female Sprague-Dawley rats were randomly assigned to control or SPS groups. Two weeks following SPS, the animals were exposed to a battery of behavioral tests and decapitated a day later. Based on their anxiety index, they were further categorized as SPS-resilient (SPS-R) or SPS-susceptible (SPS-S). On the day of dissection, cecum, and selected brain tissues were isolated. Stool samples were collected before and after SPS, whereas urine samples were taken before and 30 min into the SPS.

Results: Before SPS exposure, the sympathoadrenal axis exhibited alterations within male subgroups only. Expression of tight junction protein claudin-5 was lower in brain of SPS-S males, but higher in SPS-R females following SPS. Across the study, alpha diversity remained consistently lower in males compared to females. Beta diversity revealed distinct separations between male and female susceptible groups before SPS, with this separation becoming evident in the resilient groups following SPS. At the genus level, Lactobacillus, Lachnospiraceae_Incertae_Sedis, and Barnesiella exhibited sex-specific alterations, displaying opposing abundances in each sex. Additionally, sex-specific changes were observed in microbial predictive functionality and targeted functional modules both before and after SPS. Alterations in the microbial short-chain fatty acids (SCFAs), were also observed, with major and minor SCFAs being lower in SPS-susceptible males whereas branched-chain SCFAs being higher in SPS-susceptible females.

Conclusion: This study highlights distinct pre- and post-trauma differences in microbial composition, functionality, and metabolites, associated with stress resilience in male and female rats. The findings underscore the importance of developing sex-specific therapeutic strategies to effectively address stress-related disorders. Highlights SPS model induces divergent anxiety and social behavioral responses to traumatic stress in both male and female rodents. SPS-resilient females displayed less anxiety-like behavior and initiated more interactions towards a juvenile rat than SPS-resilient males. Sex-specific pre-existing and SPS-induced differences in the gut microbial composition and predictive functionality were observed in susceptible and resilient rats. SPS-resilient males displayed elevated cecal acetate levels, whereas SPS-susceptible females exhibited heightened branched-chain SCFAs.

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来源期刊
Biology of Sex Differences
Biology of Sex Differences ENDOCRINOLOGY & METABOLISM-GENETICS & HEREDITY
CiteScore
12.10
自引率
1.30%
发文量
69
审稿时长
14 weeks
期刊介绍: Biology of Sex Differences is a unique scientific journal focusing on sex differences in physiology, behavior, and disease from molecular to phenotypic levels, incorporating both basic and clinical research. The journal aims to enhance understanding of basic principles and facilitate the development of therapeutic and diagnostic tools specific to sex differences. As an open-access journal, it is the official publication of the Organization for the Study of Sex Differences and co-published by the Society for Women's Health Research. Topical areas include, but are not limited to sex differences in: genomics; the microbiome; epigenetics; molecular and cell biology; tissue biology; physiology; interaction of tissue systems, in any system including adipose, behavioral, cardiovascular, immune, muscular, neural, renal, and skeletal; clinical studies bearing on sex differences in disease or response to therapy.
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