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研究生:薛斐丹
研究生(外文):Pei-Tan Hsueh
論文名稱:小鼠自閉症行為發展之腸道菌相,神經傳導物質與免疫偏離的特性
論文名稱(外文):Characteristics of gut microbiota, neurotransmitters and aberrant immunity on development of murine autistic behaviors
指導教授:劉仲康劉仲康引用關係
指導教授(外文):Liu, Jong-Kang
學位類別:博士
校院名稱:國立中山大學
系所名稱:生物科學系研究所
學門:生命科學學門
學類:生物學類
論文種類:學術論文
論文出版年:2017
畢業學年度:105
語文別:中文
論文頁數:206
中文關鍵詞:母體免疫活化脂多醣體腸道菌相自閉症血清素
外文關鍵詞:serotoninintestinal microbiotaautismMIALPS
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以脂多醣體(Lipopolysaccharide; LPS)為過敏原誘發小鼠母體免疫活化(Maternal immune activation; MIA)而導致焦慮與自閉樣行為,可以成為觀察人類自閉症光譜的動物模型。本研究假設母體暴露低劑量環境脂多醣體會直接造成子代腦組織細胞傷害、腸道菌群改變,而間接影響細胞黏附因子免疫偏離與神經傳導物質的失衡,進而導致腦神經細胞發育障礙與自閉行為的發展。因此,本研究首先評估低劑量之Burkholderia spp與Escherchia coli LPS誘發之內毒血症的生理特性,結果顯示Burkholderia LPS (特別是B. multivorans LPS)具有較高的免疫刺激性,以及促進脾臟細胞活化、骨髓單核球增生、血清細胞激素增加的能力,但E. coli LPS則誘發較多的CD16/32+CD45lo腦浸潤白血球。因此,本研究暴露E. coli LPS (total, 100 μg/Kg)後,在曠野實驗、光暗盒與十字實高架迷宮以及家籠行為實驗與3倉社交行為實驗證實MIA小鼠出現焦慮與自閉行為。這些焦慮自閉行為表現之小鼠出現(1)大腦血清素(Serotonin,5-HT),以及5-HT合成酵素- tph2基因、5-HT transpoter -slc6a4基因下降,並且伴隨5-HT神經元於裂縫核的數目與分布密度的減少,以及5-HT神經元之axon hillock變細等;(2) 腸道菌相發生改變,特別是Clostridium cocleatum成為MIA子代腸道之優勢菌種。(3)大腦組織干擾素誘發之gbp3、irgm1、ifi44基因;IL-2誘發之Jak3基因;細胞凋亡相關之tnfrsf1、nlrp3、nr4a1基因;以及細胞黏附因子sell、selp等免疫相關基因發生明顯變化。(4) MIA子代腦組織之IL-6增加(青春期與成鼠),MCP-1降低 (成鼠),以及L-selectin的降低(青春期與成鼠)等,並且經過LPS再度刺激,相較於再度刺激之生理食鹽水子代,被刺激之MIA子代於24 h後會出現高表現的TNF-、IL-6、IFN-、MCP-1、L-selectin與P-selectin。因此,本研究結論LPS誘發之MIA子代,短期效應造成腦組織細胞與神經傳導物質的失衡,長期效應造成腸道菌群改變,而直接或間接影響IL-6、MCP-1與L-selectin等免疫偏離與神經傳導物質5-HT的長期失衡,進而導致5-HT神經元發展障礙與焦慮自閉行為的發展。
The offspring of maternal immune activation (MIA) mice induced by environmental allergen lipopolysaccharides (LPS) is an animal model to reflect the observation of anxiety- and autism-like behaviors in human. In this project, we hypothesized that, during pregnancy, mouse exposure to low doses of LPS directly lead to the offspring occuring the neuronal damages, the changes of intenstinal microflora, aberrance of immune response and neurotransmistters, and ultimately result in developing anxiety- and autism-like bahaviors. The abilities in activation of splenocytes, proliferation of bone marrow cells as well as raised serum cytokines and chemokines were firstly evaluated for endotoxemic mice that respectively induced by Burkholderia spp. and Escherichia coli LPS at low doses. Although B. multivorans LPS potentially had the strongest immune stimulation, E. coli LPS can induce an increase of CD16/32+CD45lo brain infiltrating leukocytes. Thus, MIA were induced by E. coli LPS at 100 g/Kg, totally. The appearance of anxiety-like behaviors in MIA offspring were evaluated using open-field test, dark/light boxes test and elevated plus maze test as well as of autism-like behaviors by home cage test and 3-chamber behavior test. Those mice with anxiety- and autism-like behaviors exhibited (1) a down-regulation of cerebral serotonin (5-HT), 5-HT synthetic enzyme gene (tph2) and 5-HT transporter gene (slc6a) in combination with decrease of the number and distributed density of 5-HT neurons, (2) alteration of intestinal microbiota, pariticularly is predominately Clostridium cocleatum, (3) the changes of interferon-induced genes (gbp3, irgm1 and ifi44), IL-2-induced gene (jak3), apoptotic genes (tnfrsf1, nlrp3 and nr4a1) and cell adhesion molecule genes (sell and selp) in the brains, and (4) up-regulation of cerebral IL-6 at adolescent and adulthood but decrease of MCP-1 at adulthood as well as down-regulation of L-selectin at adolescent and adulthood. Moreover, TNF-, IL-6, IFN-, MCP-1, L-selectin and P-selectin in the brain were increased for MIA offspring re-stimulated by LPS as compared to PBS offspring re-stimulated. Our results indicated that the MIA offspring appeared an imbalance of neurotransmitters and brain development on shor-term effect as well as the changes of intestinal microbiota that directly and indirectly effected on aberrant expression of IL-6, MCP-1 and L-selectin and development of 5-HT neuron and neurotransmitters at long-term effect. Ultimately, anxiety- and autism-like behaviors were generated in MIA offspring.
論文審定書……………………………………………………………………… i
誌謝……………………………………………………………………………… ii
中文摘要………………………………………………………………………… iii
英文摘要………………………………………………………………………… v
中英對照與縮寫………………………………………………………………… vii
第一章 研究目的……………………………………………………………… 1
第二章 研究背景……………………………………………………………… 3
2.1 環境因子、遺傳基因與免疫反應影響神經發育與ASD的行為發展………………………………………………………………………. 3
2.2 細菌表面的脂多醣體(LPS)是環境過敏原的重要成分……………... 5
2.3 動物行為模型與測量……………………………..………….……….. 7
2.4 MIA (Maternal Immune Activation)模型與神經傳導物質…………. 8
2.5 腸道菌群與腸腦軸 (Gut-to-Brain Axis)……………………………… 10
2.6 免疫偏離…………………………………...…………………………... 11
第三章 研究假設..…………………………………………………….………. 13
第四章 材料與方法………………………………………………..………….. 15
4.1 免疫源的準備…………………………………………………………. 15
4.2 動物模型準備…………………………………………………………. 15
4.3 GC-MS分析免疫原…………………………………………………. 16
4.4 免疫刺激細胞之單細胞懸浮液準備……………….………………… 17
4.5 內毒素活性與試管內TNF-分析…….……………………………… 18
4.6 流式細胞分析儀分析細胞群體、細胞激素與趨化激素……………. 19
4.7 腦部組織萃取…………………………………………………………. 19
4.8 高效液相色譜法(High performance liquid chromatography; HPLC) 與酶聯免疫法(Enzyme-linked immunoassay; ELISA )分析……….. 20
4.9 胎兒性別檢測…………………………………………………………. 21
4.10 組織學檢測…………………………………………………………... 21
4.11 大腦基因變化檢測………….……………………………………….. 22
4.12 菌相變化測量…………………………………….………………….. 23
4.13 小鼠行為分析……………………………………….....…………….. 24
4.14 統計分析……………………………………..………………………. 26
第五章 結果…………………….………………………………………….….. 27
5.1 LPS當免疫原對MIA母鼠的影響………….……………………… 27
5.1.1 免疫原的準備………………………………………………….. 27
5.1.2 Burkholderia LPS試管內免疫分析..………………………… 28
5.1.3 致死劑量與內毒血症……………………….…………………. 28
5.1.4 內毒血症之脾臟與骨髓細胞群變化的差異………………….. 29
5.1.5 內毒血症原誘發細胞激素與趨化激素的差..………………… 30
5.1.6 內毒血症之腦組織的變化…………………………………….. 30
5.2 MIA子代之Anxiety-like與ASD-like行為行為變化.…………….. 32
5.2.1 體重、活動力與肌肉強度……………..………………………. 32
5.2.2 Anxiety-like行為分析……………………….….…………….. 32
5.2.3 ASD-like 行為………………………………………………… 33
5.3 MIA子代神經元與神經傳導物質的變化……….………………….. 33
5.3.1 5-HT與DA相關基因表現……………………….………….. 33
5.3.2 神經元或膠質細胞的型態………………...…………………… 34
5.3.3 腦組織5-HT與DA的變化……….……….…………………... 35
5.4 MIA子代腸道菌群的變化………………..…..…….……………….. 36
5.4.1 菌種數量與多樣性………….……………….…..……………... 36
5.4.2 細菌菌相分布…………………………..….………….……….. 37
5.4.3 C. cocleatum與MIA子代變化的趨勢….……….………….. 40
5.5 MIA子代腦組織基因變化與免疫偏離………….…..……………... 40
5.5.1 Microarray篩選分析……………………....……..…………... 41
5.5.2 qRT-PCR鑑別基因的變化……………….…………………... 43
5.2.3 MIA子代的免疫偏離………………….…………….……….. 44
第六章 討論……………………………………………………….…………… 45
6.1 免疫原………………………………………………..……………….. 45
6.2 MIA子代行為、神經細胞與神經傳導物質……….……………… 49
6.3 MIA子代之菌相變化………………………………….…………… 53
6.4 MIA子代之基因改變與免疫偏離…………………………………. 55
第七章 結論…………………………………………………………………… 59
參考文獻………………………………………………………………………… 61
圖………........................………………………………………………………… 75
表………........................…………………………………………………………133
附錄圖表........................…………………………………………………………137
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