Holmstrand Ericka C, Lund David, Cherian Ajeesh Koshy, Wright Jane, Martin Rolicia F, Ennis Elizabeth A, Stanwood Gregg D, Sarter Martin, Blakely Randy D
Department of Pharmacology, Vanderbilt University School of Medicine, Nashville, TN, USA.
Department of Psychology, University of Michigan, Ann Arbor, MI, USA; Department of Neuroscience, University of Michigan, Ann Arbor, MI, USA.
Neurochem Int. 2014 Jul;73:217-28. doi: 10.1016/j.neuint.2013.11.008. Epub 2013 Nov 22.
The hemicholinium-3 (HC-3) sensitive, high-affinity choline transporter (CHT) sustains cholinergic signaling via the presynaptic uptake of choline derived from dietary sources or from acetylcholinesterase (AChE)-mediated hydrolysis of acetylcholine (ACh). Loss of cholinergic signaling capacity is associated with cognitive and motor deficits in humans and in animal models. Whereas genetic elimination of CHT has revealed the critical nature of CHT in maintaining ACh stores and sustaining cholinergic signaling, the consequences of elevating CHT expression have yet to be studied. Using bacterial artificial chromosome (BAC)-mediated transgenic methods, we generated mice with integrated additional copies of the mouse Slc5a7 gene. BAC-CHT mice are viable, appear to develop normally, and breed at wild-type (WT) rates. Biochemical studies revealed a 2 to 3-fold elevation in CHT protein levels in the CNS and periphery, paralleled by significant increases in [(3)H]HC-3 binding and synaptosomal choline transport activity. Elevations of ACh in the BAC-CHT mice occurred without compensatory changes in the activity of either choline acetyltransferase (ChAT) or AChE. Immunohistochemistry for CHT in BAC-CHT brain sections revealed markedly elevated CHT expression in the cell bodies of cholinergic neurons and in axons projecting to regions known to receive cholinergic innervation. Behaviorally, BAC-CHT mice exhibited diminished fatigue and increased speeds on the treadmill test without evidence of increased strength. Finally, BAC-CHT mice displayed elevated horizontal activity in the open field test, diminished spontaneous alteration in the Y-maze, and reduced time in the open arms of the elevated plus maze. Together, these studies provide biochemical, pharmacological and behavioral evidence that CHT protein expression and activity can be elevated beyond that seen in wild-type animals. BAC-CHT mice thus represent a novel tool to examine both the positive and negative impact of constitutively elevated cholinergic signaling capacity.
半胱氨酸-3(HC-3)敏感的高亲和力胆碱转运体(CHT)通过对源自饮食或乙酰胆碱酯酶(AChE)介导的乙酰胆碱(ACh)水解产生的胆碱进行突触前摄取,来维持胆碱能信号传导。胆碱能信号传导能力的丧失与人类和动物模型中的认知及运动缺陷相关。虽然CHT的基因敲除已揭示了CHT在维持ACh储存和胆碱能信号传导中的关键性质,但CHT表达升高的后果尚未得到研究。我们使用细菌人工染色体(BAC)介导的转基因方法,培育出整合了额外小鼠Slc5a7基因拷贝的小鼠。BAC-CHT小鼠可存活,似乎发育正常,且以野生型(WT)的繁殖率繁殖。生化研究显示,中枢神经系统和外周的CHT蛋白水平升高了2至3倍,同时[(3)H]HC-3结合及突触体胆碱转运活性也显著增加。BAC-CHT小鼠中ACh的升高并未伴随胆碱乙酰转移酶(ChAT)或AChE活性的代偿性变化。对BAC-CHT脑切片进行的CHT免疫组织化学显示,胆碱能神经元细胞体以及投射到已知接受胆碱能神经支配区域的轴突中,CHT表达明显升高。行为学上,BAC-CHT小鼠在跑步机测试中表现出疲劳减轻和速度增加,但未显示力量增强。最后,BAC-CHT小鼠在旷场试验中表现出水平活动增加,在Y迷宫中自发交替减少,在高架十字迷宫开放臂中的停留时间减少。这些研究共同提供了生化、药理学和行为学证据,表明CHT蛋白表达和活性可以升高到超过野生型动物的水平。因此,BAC-CHT小鼠代表了一种新工具,可用于研究胆碱能信号传导能力持续升高的正负影响。