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研究生:吳偉立
研究生(外文):Wu, Wei-Li
論文名稱:探討第三型酸敏感性離子通道基因剔除對小鼠社交行為及焦慮程度的影響
論文名稱(外文):The Effect of ASIC3 Knockout on Social and Anxiety Behavior in Mice
指導教授:陳志成陳志成引用關係
指導教授(外文):Chen, Chih-Cheng
口試委員:李小媛陳志成黃翊恭王智弘廖瑞銘鄭雅薇賴文崧
口試委員(外文):Lee, Eminy Hsiao-YuanChen, Chih-ChengHuang, Eagle Yi-KungWang, Chih-HungLiao, Ruey-MingCheng, Ya-WeiLai, Wen-Sung
學位類別:博士
校院名稱:國防醫學院
系所名稱:生命科學研究所
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:2010
畢業學年度:99
語文別:英文
論文頁數:200
中文關鍵詞:第三型酸敏感性離子通道基因剔除小鼠聽覺聽性腦幹誘發反應母性行為超音波叫聲社交行為刻板行為血清張力素三叉神經中腦核焦慮高腳十字迷宮
外文關鍵詞:Acid sensing ion channel 3 (ASIC3)Knockout miceHearingAuditory brainstem response (ABR)Maternal behaviorUltrasonic vocalizationSocial behaviorStereotypic behaviorSerotonin (5-HT)Mesencephalic trigeminal nucleus (Me5)AnxietyElevated plus mazeAPETx2
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感覺系統對於情緒的恆定是相當重要的,感覺的剝奪會造成情緒的表達異常。第三型酸敏感性離子通道主要表現於哺乳類動物的感覺神經系統中。過去的研究顯示抑制第三型酸敏感性離子通道會對感覺功能及疼痛功能造成相當大的影響,然而第三型酸敏感性離子通道對於情緒的調控上卻從未被探討。在此我們提出假說認為第三型酸敏感性離子通道會透過感覺系統來影響到情緒的表現,本論文中我們利用基因剔除小鼠的模式來探討第三型酸敏感性離子通道在情緒調控的角色。在第一部份,以聽覺驚嚇反射及聽性腦幹誘發反應實驗證實了第三型酸敏感性離子通道基因剔除小鼠聽力隨著年齡而逐漸衰退,然而在視覺及嗅覺的試驗中表現正常。同時也發現聽力的退化影響到小鼠的母性行為而造成第三型酸敏感性離子通道基因剔除小鼠在繁養後代較為困難。第三型酸敏感性離子通道基因剔除小鼠在母性行為的測試中表現出較慢將幼兒叼回至巢中、提供幼兒較少的照顧、經常性的造成幼兒的傷害及築巢功能的缺損。聽力的退化與母性行為缺損的關連性更進一步的在母性行為過程中以超音波聲音記錄實驗中證實,第三型酸敏感性離子通道基因剔除小鼠對於幼兒的超音波聲音較無回應,而野生型小鼠及第三型酸敏感性離子通道異型雜合子小鼠對於幼兒所發出的特定超音波音聲數目比率、頻率、長短有所回應。第三型酸敏感性離子通道基因剔除小鼠的母性行為缺損也阻礙了後代的社交行為發展,由第三型酸敏感性離子通道基因剔除小鼠所哺育的後代表現出較低程度的社交行為、較少發出超音波聲音溝通以及增加固定重複性的行為,此外第三型酸敏感性離子通道基因剔除小鼠所哺育的後代腦部血清張力素活性也呈現較低的現象。由此部份的結果顯示剔除第三型酸敏感性離子通道後後透過聽力退化及母性行為缺損而對小鼠社交行為造成基因後生遺傳的影響。第二部份中,由於我們在上一個部份仍舊觀察到許多第三型酸敏感性離子通道基因剔除後基因直接造成的影響,因此本部份在探討腦中第三型酸敏感性離子通道可能扮演的角色。在反轉錄聚合酵素鏈鎖反應及免疫螢光組織染色中顯示大腦中的第三型酸敏感性離子通道主要分布於小鼠中腦及腦幹。腦部磁振頻譜也顯示第三型酸敏感性離子通道基因剔除小鼠中腦及腦幹的細胞活性較低。相反的第三型酸敏感性離子通道基因剔除小鼠的海馬迴神經可塑性則沒有明顯的改變。在行為檢測中發現第三型酸敏感性離子通道基因剔除小鼠僅在高腳十字迷宮顯示較低的焦慮程度,而在認知功能測試、恐懼反應測試、類憂鬱行為測試、前脈衝抑制測試及運動功能測試上則顯示正常。而在野生型小鼠中樞直接給予第三型酸敏感性離子通道專一性抑製劑APETx2會造成類似於第三型酸敏感性離子通道基因剔除小鼠的抗焦慮行為。本部份的結果顯示抑制腦部的第三型酸敏感性離子通道對於小鼠的情緒上仍會有基因遺傳的直接影響。在第三部份中,由於第三型酸敏感性離子通道位於人類染色體7q的位置,此位置的遺傳變異也與自閉症相關。因此我們比較了與自閉症相關位於染色體7q的位置之基因剔除鼠模式以及目前認定為自閉症動物模式的小鼠模式與第三型酸敏感性離子通道基因剔除小鼠的行為表徵的差異。本部份在探討第三型酸敏感性離子通道基因剔除小鼠作為自閉症模式動物的可能性。整體而言,抑制第三型酸敏感性離子通道對小鼠情緒的調控上造成基因遺傳與基因後生遺傳的影響,第三型酸敏感性離子通道所調控的感覺功能參與了小鼠社交行為的表現,然而第三型酸敏感性離子通道對在小鼠腦中於情緒的調控也不能排除,腦中第三型酸敏感性離子通道可能也參與了焦慮行為的調控。研究第三型酸敏感性離子通道提供了社交缺損與焦慮症上一個治療新契機。
Sensory inputs are essential for emotion homeostasis. Sensory deprivation may lead to emotion abnormality. Acid sensing ion channel 3 (ASIC3) is predominately distributed in most sensory nervous systems in mammals. Inhibition of ASIC3 produced profound effect on sensory and nociception function. However, the effect of ASIC3 inhibition on emotion control had never been investigated. We hypothesized that ASIC3 inhibition may affect emotion expression through specific sensory deficit. In this thesis, we aimed to unravel the role of ASIC3 in emotion control by using genetically deletion of Asic3 in mice. In the first part, age-dependent hearing impairment in Asic3-/- mice was demonstrated by acoustic startle reflex and auditory brainstem response (ABR). Asic3-/- mice displayed normal in visual and olfactory tasks. Age-dependent hearing impairment in Asic3-/- mice leaded to maternal deficiency. Asic3-/- mice showed maternal deficiency in pup retrieval, caring pups, and nest-building behavior. The linkage between hearing impairment and maternal deficiency was further evidenced by ultrasonic vocalization (USV) recoding during pup retrieval test. Asic3-/- mice did not respond to pups’ USV, while wild type and Asic3+/- mice responded to certain calling rate, frequency and duration of USV. The maternal deficiency then hindered the offspring social development. Mice raised by Asic3-/- dam showed decreased social behaviors, low USV emission and increased stereotypic behaviors. The brain 5-HT turnover rate was also altered in Asic3-/- mice raised by Asic3-/- dam. Asic3 deletion exerted an epigenetic effect on mice social behavior resulting from hearing and maternal deficit. In the second part, we investigated the genetically driven phenotypes in Asic3-/- mice. At first, we examined we aimed to know whether the brain Asic3 playa a role for emotional control in mice. In the brain, Asic3 was found expressed in mice midbrain and brainstem by RT-PCR and immunohistochemistry. Brain magnetic resonance spectroscopy (MRS) showed reduction of cell activity at midbrain and brainstem of Asic3-/- mice. On the contrary, the hippocampal synaptic plasticity was normal in Asic3-/- mice. In behavior phenotyping, Asic3-/- mice only showed lower anxiety level on elevated plus maze (EPM) than wild type mice. The other cognitive functions including fear response, depression-like behavior, prepulse inhibition and motor function were intact in Asic3-/- mice. By centrally administrated high dose ASIC3 specific blocker- APETx2, wild type mice showed similar anxiolytic behavior with Asic3-/- mice on EPM. We conclude that inhibition of ASIC3 in the brain was effective on emotion control. In the third part, the possibility of Asic3-/- mice as ASD mice model was proposed and discussed. ASIC3 gene locates at human chromosome 7q35, which is considered as an autism spectrum disorder (ASD) association chromosome locus. We compared the behavioral phenotypes of Asic3-/- mice with ASD association genes on chromosome 7q and other known ASD mice models. In conclusion, inhibition of ASIC3 produced both genetic and epigenetic effects on mice emotion. The ASIC3-dependent sensory function is involved in mice social behavior display. However, the effect of brain ASIC3 on mice emotion control cannot be excluded. Brain ASIC3 may play a role in control anxiety behavior. Therefore, ASIC3 might be a new therapeutic target on social deficit and anxiety disorder.
Chapter 1. General Background 1
1.1 Introduction 1
1.2 Acid sensing ion channel (ASIC) 1
1.2.1 Structure of ASICs 2
1.2.2 Subtypes and general distributions of ASICs 2
1.2.3 Electrophysiological properties of ASICs 3
1.2.4 General functions of ASICs 4
1.3 Acid sensing ion channel 3 (ASIC3) 5
1.3.1 Electrophysiological properties of ASIC3 5
1.3.2 Distributions of ASIC3 6
1.3.3 Functions of ASIC3 6
1.3.4 Specific antagonist of ASIC3 7
1.4 Linkage of ASIC3 to emotion process 8
1.4.1 ASICs, hearing sensation, maternal caring and social development 8
1.4.2 ASICs, fear and anxiety 10
1.5 Emotional behavior related in this thesis 11
1.5.1 Social behavior 11
A. Definition of social behavior 11
B. Social behavior and sensory function 11
C. Neural circuits underlying social behavior 12
D. Disorders with abnormal social behavior 12
1.5.2 Anxiety behavior 13
A. Definition of anxiety behavior 13
B. Classification of anxiety disorder 13
C. Neural circuits underlying anxiety disorder 13
1.6 Objectives 14

Chapter 2. Materials and Methods 16
2.1 Animals 16
2.2 Molecular biology 16
2.2.1 Genotyping 16
2.2.2 RT-PCR 18
2.3 Immunohistochemistry 19
2.4 Auditory brainstem response (ABR) 19
2.5 Neurochemical measurement 20
2.6 Electrophysiology 21
2.7 Neuroimaging 22
2.8 Behavioral test 22
2.8.1 Behavioral temporal sequence 22
2.8.2 Sensory function tests 24
A. Visual cliff 24
B. Olfactory habituation 25
C. Acoustic startle reflex and prepulse inhibition 25
2.8.3 Maternal behavior 27
A. Maternal behavior of dams 27
B. Pup retrieval tests 27
C. Cross-fostering 29
2.8.4 USV recording 29
A. USV recording during pup retrieval 29
B. Isolation-induced USV recording 30
C. USV recording during social interaction 31
2.8.5 Social behavior 31
A. Juvenile social behaviors 31
B. Resident–intruder test 32
2.8.6 Anxiety-like behavioral test 34
A. Open-field test 34
B. Open-field test at high light intensity 34
C. Light-dark box 34
D. Light-dark box test at high light intensity 35
E. Elevated plus maze 35
2.8.7 Cognitive function tests 36
A. Morris water maze 36
B. Context fear conditioning 38
C. Cued fear conditioning test 39
D. Pain sensitivity to electric foot shock 40
2.8.8 Motor function tests 40
A. Novel cage exploratory behavior 40
B. Locomotion activity in open field 41
C. Rotarod 41
2.8.9 Depression-like behavior 42
A. Tail suspension test 42
B. Forced swim test 42
2.9 Intracerebroventricular (I.C.V.) injection of APETx2 43
2.10 Statistical analysis 44

Chapter 3. The Role of ASIC3 in Social Behavior 45
3.1 Asic3-/- mice displayed normal in visual, olfactory, and motor tasks, but less responded in acoustic startle reflex test 45
3.2 Age-dependent hearing deficiency in Asic3-/- mice 46
3.3 Maternal deficit in Asic3-/- mice 48
3.4 Less maternal response to pup calls in Asic3-/- mice 51
3.5 Offspring social deficit in Asic3-/- mice 53
3.6 Less vocalization during juvenile social interaction in Asic3-/- mice 55
3.7 Altered neuronal activity during juvenile social interaction in Asic3-/- mice 56
3.8 Cross-fostering reversed the social deficit phenotype in Asic3-/- mice 57
3.9 Low aggression level to intruders in Asic3-/- mice 59

Chapter 4. The Role of ASIC3 in Anxiety Behavior 61
4.1 Asic3 mRNA expression in brains of mice 61
4.2 Distribution of ASIC3 protein in the brain of mice 62
4.3 Low cell membrane turnover rate at midbrain and brainstem in Asic3-/- mice 62
4.4 Bi-directional plasticity was similar in young Asic3+/+ and Asic3-/- mice. 63
4.5 Asic3-/- mice performance was normal in cognitive function 64
4.6 Low anxiety level in Asic3-/- mice 65
4.7 Asic3-/- mice showed no depression-like and normal sensorimotor gating function 66
4.8 Motor function was unaffected in Asic3-/- mice 67
4.9 Central ASIC3 inhibition produced anxiolytic effect 68

Chapter 5. Proposing Asic3-/- mice As a Mice Model of Autism Spectrum Disorder 70
5.1 The symptoms of ASD 70
5.2 The genome mapping of ASD and related mice model 72
5.3 Comparing Asic3-/- mice with other mice model of ASD 75
5.4 ASD related phenotypes that never been tested in Asic3-/- mice 80

Chapter 6. Discussion 83

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