模拟失重对大鼠小动脉结构和功能的重塑作用以及-Gx重力的对抗效果
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摘要
航天观察与地面卧床研究均发现,航天员返回地面后,常表现出心血管功能失调的现象,其主要标志为立位耐力不良和运动能力下降。航天后心血管功能失调可导致航天人员工作能力下降,甚至危及航天飞行安全。大量研究工作表明,航天失重环境下血容量的减少是造成飞行后心血管功能失调的重要原因之一,此外,还涉及其他多重机制。在航天失重环境下,机体流体静压消失,从而使全身动脉血管系统的跨壁压发生改变:脑及上半身血压处于较地面1G直立体位时相对升高的“高血压”状态;下半身血管则处于较1G直立时相对较低的“低血压”状态,这些改变可进一步导致心血管系统的变化。本实验室在地面动物模拟失重实验中发现:模拟失重可引起大鼠脑动脉血管的肌源性紧张度(Myogenic Tone)增强,收缩反应性升高,血管中膜肥厚和平滑肌细胞层数增多,以及血管周围神经支配增强等适应性变化。而对于后身中、小动脉,则可引起肌源性紧张度减弱,收缩反应性降低,血管中膜萎缩,以及血管周围神经支配减弱等变化。据此我们曾提出“外周效应器机制假说”,认为失重所引起的心肌与动脉血管平滑肌结构和功能改变很可能是除血容量减少因素之外,导致飞行后心血管失调的另一个重要原因。我实验室前期工作已经发现:血管平滑肌离子通道机制与血管组织局部肾素-血管紧张素系统(local renin-angiotensin system)可能是介导失重所致血管区域特异性适应变化的重要调节环节。目前,近地轨道飞行采用的以运动为主的对抗措施,并不能完全防止长时间航天飞行导致的心血管失调,而“间断性人工重力”(intermittent artificial gravity)可能是未来航天中较为理想的一种对抗措施方案,相关研究亦日益受到关注与重视。在地面动物实验,可以采用+45°头高位倾斜(HUT)、离心机旋转及恢复动物正常站立体位来模拟IAG的对抗效果。我们前期工作已表明:每日1 h恢复站立(所受重力矢量为-Gx)具有对抗模拟失重大鼠基底动脉收缩反应性增强、股动脉和心肌收缩性降低的效果。在形态方面,1 h/d的-Gx也可防止模拟失重大鼠基底动脉肥厚和胫前动脉萎缩;在清醒大鼠则可以防止整体心血管失调反应。但我们最近的工作还表明:3天模拟失重可分别引起脑动脉和肠系膜动脉平滑肌细胞L型钙离子通道(CaL)电流密度增加和减少;1 h/d的-Gx可以防止肠系膜动脉血管平滑肌细胞CaL电流密度减少,但不能防止脑动脉血管平滑肌细胞CaL电流密度增加。由此我们推测:在脑血管,1 h/d的-Gx干预虽然可以防止模拟失重所致的脑血管肥厚性结构重塑,但并不能防止其肌源性紧张度升高和收缩反应性增强;而在肠系膜小动脉,1 h/d的-Gx则可以全面防止其功能与结构的适应性变化。
为证实我们提出的假说,本工作由以下两部分组成:
(1)观察短期(3天)及中期(28天)模拟失重大鼠大脑中动脉血管肌源性紧张度的变化,血管收缩反应性的变化,血管管壁超微结构的变化以及在此基础上,每日站立1小时-Gx重力影响对短期及中期模拟失重所引起的大脑中动脉功能和结构的适应变化有无防止作用。我们分离大鼠大脑中动脉,利用Pressure Myograph System观察血管管径-压力变化关系与血管管径-血管收缩剂浓度变化关系,以了解血管肌源性紧张度以及动脉收缩反应性的变化;同时通过电子显微镜技术观察血管管壁超微结构的变化。
(2)观察短期(3天)及中期(28天)模拟失重大鼠肠系膜小动脉血管肌源性紧张度的变化,血管收缩反应性的变化,血管管壁超微结构的变化以及在此基础上,每日站立1小时-Gx重力影响对短期及中期模拟失重所引起的肠系膜小动脉功能和结构的适应变化有无防止作用。我们分离大鼠肠系膜小动脉,利用Pressure Myograph System观察血管管径-压力变化关系与血管管径-血管收缩剂浓度变化关系,以了解血管肌源性紧张度以及收缩反应性的变化;通过电子显微镜技术观察血管管壁超微结构的变化。
本工作的主要发现如下:
(1)模拟失重可以引起大鼠大脑中动脉血管肌源性紧张度升高,血管对收缩物质反应性增强,引起血管管壁厚度增大,引起血管管壁横截面积增加,血管平滑肌中膜厚度增加以及平滑肌细胞层数的增多。每日站立1小时-Gx重力能够防止血管管壁结构的肥厚性变化,但不能防止血管肌源性紧张度、血管对收缩物质反应性升高的变化。根据大脑中动脉管径-压力、管径-收缩剂变化关系观察到,同对照组大鼠相比,短期模拟失重(3天)大鼠大脑中动脉血管肌源性紧张度以及血管对5-HT的收缩反应分别增强了11.7%、12.3%,每日站立1小时-Gx重力不能防止此种变化;模拟失重28天大鼠大脑中动脉血管肌源性紧张度、血管对5-HT收缩反应分别增强了18.8%、13.7%,血管管壁厚度、血管中膜厚度分别增加了56.4% (P<0.01)和63.0% (P<0.01),血管平滑肌细胞层数亦较对照组显著增加,每日站立1小时-Gx重力不能防止血管肌源性紧张度、血管收缩反应性增强,但能够防止血管管壁结构的变化。
(2)模拟失重可以引起大鼠肠系膜小动脉血管肌源性紧张度降低,血管收缩反应性减弱,引起血管管壁厚度减小,引起血管管壁横截面积减少,血管管壁中膜厚度减小以及平滑肌细胞层数的减少。每日站立1小时-Gx重力能够防止血管管壁结构的变化,亦能防止血管肌源性紧张度降低、血管收缩反应性减弱的变化。根据肠系膜小动脉管径-压力、管径-收缩剂浓度变化关系观察到,同对照组大鼠相比,短期模拟失重(3天)大鼠肠系膜小动脉血管肌源性紧张度、血管对PE反应性分别降低了11.5%、12.1%,每日站立1小时-Gx重力能够防止此种变化;模拟失重28天大鼠肠系膜小动脉血管肌源性紧张度、血管对PE反应性分别降低了22.5%、21.6%,血管管壁厚度、血管中膜厚度分别减小了20.0% (P<0.01)和28.6% (P<0.01),血管平滑肌细胞层数亦较对照组显著减少,每日站立1小时-Gx重力能防止血管肌源性紧张度降低、血管收缩反应性减弱的变化,亦能够防止血管管壁结构的变化。
以上结果表明,短期(3天)及中期(28天)模拟失重大鼠大脑中动脉和肠系膜小动脉血管的肌源性紧张度、收缩反应性分别发生了增强和减弱的变化,其血管超微结构亦分别发生了肥厚和萎缩的改变。每天站立一小时-Gx重力作用只能防止大脑中动脉结构的适应性变化而不能完全防止其血管功能的适应性变化;但在肠系膜小动脉,每天站立一小时-Gx重力作用对血管功能和结构的适应性变化均有良好的防止作用。
Humans exposed to microgravity often exhibit signs of cardiovascular deconditioning marked by orthostatic intolerance and reduced exercise capacity on reexposure to gravity. The impaired cardiovascular response to standing after return from space might be among the highest risks to the safety, well-being, and performance of astronauts. In addition to hypovolemia, postflight cardiovascular deconditioning has also been associated with diminished cardiac and vascular function. All gravitational blood pressure gradients will disappear during microgravity exposure. Thus, a redistribution of transmural pressures and flows across and within the arterial vasculature is induced by the removal of gravity. Therefore, in humans, blood vessels in dependent body regions are chronically exposed to lower than normal upright 1-G blood pressure, whereas vessels in upper body regions are exposed to higher than normal 1-G blood pressure. Our previous ground-based animal studies have shown for the first time that simulated microgravity may induce upward and downward regulations in function, structure, and innervation state of the medium- and small-sized muscular arteries from fore (cerebral) and hind body parts of the same animal subjected to tail-suspended head-down tilt (SUS). On the basis of these findings and the relevant ground-based and spaceflight studies reported recently, we have raised the“peripheral effector mechanism hypothesis”. We suggested that, in addition to hypovolemia, the microgravity-induced adaptation changes in function and structure of cardiac muscle and vascular smooth muscle might be another important factor responsible for postflight cardiovascular dysfunction. Our previous studies have also shown that the ion channel remodeling mechanism of vascular smooth muscle cells (VSMCs) and vascular local renin-angiotensin system (L-RAS) might be involved in vascular region-specific adaptational changes to microgravity. Furthermore, currently used, exercise-based countermeasures seem insufficient to prevent the occurrence of cardiovascular dysfunction in future long-duration, exploration class mission. In the past two decades, intermittent artificial gravity (IAG) by incorporating a short-arm centrifuge into the spacecraft has been suggested as a gravity-based countermeasure for future spaceflight. Our previous studies have shown that daily short-duration exposure to -Gx (dorsoventral) gravitation by standing (STD) to restore the rat’s orthostatic posture , or -Gx with +Gz component by +45°head-up tilt, which mimics the IAG countermeasure, is surprisingly effective in preventing myocardial contractility depression and vascular changes. For example, it has been demonstrated that daily 1-h -Gx by STD is sufficient to prevent the differential changes in two kinds of medium-sized conduit arteries that might occur due to a 28-d simulated microgravity alone. Our work has further shown that simulated microgravity increases and decreases current densities and protein expression of CaL in cerebral and mesenteric arterial VSMCs,the countermeasure of 1 h/d -Gx can prevents the change of mesenteric artery but cannot prevent the change in cerebral artery. This study is on the basis of such hypothesis that in middle cerebral artery, 1h/d -Gx can prevent the thickening of structure induced by microgravity, but can not prevent the increase of myogenic tone and the enhancement of vasoconstriction. In mesenteric small artery, not only the 1h/d -Gx can prevent the attentuation of vasoconstriction and thinningz of structure induced by microgravity, but also can prevent the increase of myogenic tone.
To confirm our hypothesis mentioned above, we use tail-suspension rat model to simulate the cardiovascular dysfunction after flight and daily 1-h standing to simulate the countermeasure effect of IAG. The changes of vessel function and structure in rats were examined. The main work was divided into two parts:
(1) The first part of work was aim to examine the change of myogenic tone, the vasoconstriction of middle cerebral artery and mesenteric small artery after a short-term (3-day) simulated microgravity with and without 1-h/d -Gx countermeasure. After simulated microgravity, the middle cerebral artery and mesenteric small artery were isolated and cannulated, the responses to increases of pressure and concentrations of vaso-constrictor were detected.
(2) The second part of work was aim to examine the change of myogenic tone, the vasoconstriction and the vessel structure under electron microscope of middle cerebral artery and mesenteric small artery after a medium-term (28-day) simulated microgravity with and without 1-h/d -Gx countermeasure. After simulated microgravity, the middle cerebral artery and mesenteric small artery were isolated and cannulated, the responses to increases of pressure and concentrations of vaso-constrictor were detected, then fixed the vessel at in-situ length, the structure was examined with electronmicroscope.
The main findings of the present work are as follows:
(1) Simulated microgravity alone induced an enhancement of the myogenic tone and vasoconstrictor responsiveness in the isolated middle cerebral artery, increases the wall thiskness, the media thickness and the number of smooth muscle cell layers. Daily STD for 1 h prevented the changes of vessel structure, but did not prevent the functional enhancement in the middle cerebral artery. Compared with the simultaneous CON group, the myogenic tone and vasoconstriction to 5-HT of middle cerebral artery in SUS group (3-day) were increased 11.7%, 12.3%, respectively. In 28-day group, the myogenic tone and vasoconstriction to 5-HT of middle cerebral artery were increased 18.8 %, 13.7%, respectively. The wall thickness, the media thickness of middle cerebral artery in SUS group were increased by 56.4%(P<0.01), 63%(P<0.01), respectively, compared with that of in CON group. With 1h/d standing, the change of vessel structure can be prevented, but the increase of myogenic tone and vasoconstriction cannot be prevented.
(2) Simulated microgravity alone induced an attenuation of the myogenic tone and vasoconstrictor responsiveness in the isolated mesenteric small artery, decreases the wall thiskness, the media thickness and the number of smooth muscle cell layers. Daily STD for 1 h can prevent the changes of vessel structure, and can also prevent the functional decrement in the mesenteric small artery. Compared with the simultaneous CON group, the myogenic tone and vasoconstriction to PE of mesenteric small artery in SUS group (3-day) were decreased 11.5%, 12.1%, respectively. In 28-day group, the myogenic tone and vasoconstriction to PE of mesenteric small artery were decreased 22.5%, 21.6%, respectively. The wall thickness, the media thickness of mesenteric small artery in SUS group were decreased by 20.0%(P<0.01), 28.6%(P<0.01), respectively, compared with that of in CON group. With 1h/d standing, not only the change of vessel structure can be prevented, but the decrease of myogenic tone and vasoconstriction can also be prevented.
In conclusion, our working hypothesis has been supported by these above findings. Firstly, SUS alone induced an enhancement of the myogenic tone and vasoconstrictor responsiveness in the isolated middle cerebral artery but a depression of those in the mesenteric small artery. Secondly, the structure of middle cerebral artery and mesenteric small artery were changed by different effects. Daily standing for 1 h prevented the depression of myogenic tone and vasoconstrictor responsiveness in the mesenteric small artery, but did not prevent the functional enhancement in the middle cerebral artery. These data suggest that a short-term simulated microgravity may result in differential alterations in the function and structure of the cerebral artery and the resistance vessel in the hind-body. Both of the alteration of middle cerebral artery and mesenteric small artery can be prevented by 1h/d standing. However, only the functional changes in the mesenteric small arteries, not in the cerebral arteries, can be prevented by such a countermeasure of daily 1 h standing.
为证实我们提出的假说,本工作由以下两部分组成:
(1)观察短期(3天)及中期(28天)模拟失重大鼠大脑中动脉血管肌源性紧张度的变化,血管收缩反应性的变化,血管管壁超微结构的变化以及在此基础上,每日站立1小时-Gx重力影响对短期及中期模拟失重所引起的大脑中动脉功能和结构的适应变化有无防止作用。我们分离大鼠大脑中动脉,利用Pressure Myograph System观察血管管径-压力变化关系与血管管径-血管收缩剂浓度变化关系,以了解血管肌源性紧张度以及动脉收缩反应性的变化;同时通过电子显微镜技术观察血管管壁超微结构的变化。
(2)观察短期(3天)及中期(28天)模拟失重大鼠肠系膜小动脉血管肌源性紧张度的变化,血管收缩反应性的变化,血管管壁超微结构的变化以及在此基础上,每日站立1小时-Gx重力影响对短期及中期模拟失重所引起的肠系膜小动脉功能和结构的适应变化有无防止作用。我们分离大鼠肠系膜小动脉,利用Pressure Myograph System观察血管管径-压力变化关系与血管管径-血管收缩剂浓度变化关系,以了解血管肌源性紧张度以及收缩反应性的变化;通过电子显微镜技术观察血管管壁超微结构的变化。
本工作的主要发现如下:
(1)模拟失重可以引起大鼠大脑中动脉血管肌源性紧张度升高,血管对收缩物质反应性增强,引起血管管壁厚度增大,引起血管管壁横截面积增加,血管平滑肌中膜厚度增加以及平滑肌细胞层数的增多。每日站立1小时-Gx重力能够防止血管管壁结构的肥厚性变化,但不能防止血管肌源性紧张度、血管对收缩物质反应性升高的变化。根据大脑中动脉管径-压力、管径-收缩剂变化关系观察到,同对照组大鼠相比,短期模拟失重(3天)大鼠大脑中动脉血管肌源性紧张度以及血管对5-HT的收缩反应分别增强了11.7%、12.3%,每日站立1小时-Gx重力不能防止此种变化;模拟失重28天大鼠大脑中动脉血管肌源性紧张度、血管对5-HT收缩反应分别增强了18.8%、13.7%,血管管壁厚度、血管中膜厚度分别增加了56.4% (P<0.01)和63.0% (P<0.01),血管平滑肌细胞层数亦较对照组显著增加,每日站立1小时-Gx重力不能防止血管肌源性紧张度、血管收缩反应性增强,但能够防止血管管壁结构的变化。
(2)模拟失重可以引起大鼠肠系膜小动脉血管肌源性紧张度降低,血管收缩反应性减弱,引起血管管壁厚度减小,引起血管管壁横截面积减少,血管管壁中膜厚度减小以及平滑肌细胞层数的减少。每日站立1小时-Gx重力能够防止血管管壁结构的变化,亦能防止血管肌源性紧张度降低、血管收缩反应性减弱的变化。根据肠系膜小动脉管径-压力、管径-收缩剂浓度变化关系观察到,同对照组大鼠相比,短期模拟失重(3天)大鼠肠系膜小动脉血管肌源性紧张度、血管对PE反应性分别降低了11.5%、12.1%,每日站立1小时-Gx重力能够防止此种变化;模拟失重28天大鼠肠系膜小动脉血管肌源性紧张度、血管对PE反应性分别降低了22.5%、21.6%,血管管壁厚度、血管中膜厚度分别减小了20.0% (P<0.01)和28.6% (P<0.01),血管平滑肌细胞层数亦较对照组显著减少,每日站立1小时-Gx重力能防止血管肌源性紧张度降低、血管收缩反应性减弱的变化,亦能够防止血管管壁结构的变化。
以上结果表明,短期(3天)及中期(28天)模拟失重大鼠大脑中动脉和肠系膜小动脉血管的肌源性紧张度、收缩反应性分别发生了增强和减弱的变化,其血管超微结构亦分别发生了肥厚和萎缩的改变。每天站立一小时-Gx重力作用只能防止大脑中动脉结构的适应性变化而不能完全防止其血管功能的适应性变化;但在肠系膜小动脉,每天站立一小时-Gx重力作用对血管功能和结构的适应性变化均有良好的防止作用。
Humans exposed to microgravity often exhibit signs of cardiovascular deconditioning marked by orthostatic intolerance and reduced exercise capacity on reexposure to gravity. The impaired cardiovascular response to standing after return from space might be among the highest risks to the safety, well-being, and performance of astronauts. In addition to hypovolemia, postflight cardiovascular deconditioning has also been associated with diminished cardiac and vascular function. All gravitational blood pressure gradients will disappear during microgravity exposure. Thus, a redistribution of transmural pressures and flows across and within the arterial vasculature is induced by the removal of gravity. Therefore, in humans, blood vessels in dependent body regions are chronically exposed to lower than normal upright 1-G blood pressure, whereas vessels in upper body regions are exposed to higher than normal 1-G blood pressure. Our previous ground-based animal studies have shown for the first time that simulated microgravity may induce upward and downward regulations in function, structure, and innervation state of the medium- and small-sized muscular arteries from fore (cerebral) and hind body parts of the same animal subjected to tail-suspended head-down tilt (SUS). On the basis of these findings and the relevant ground-based and spaceflight studies reported recently, we have raised the“peripheral effector mechanism hypothesis”. We suggested that, in addition to hypovolemia, the microgravity-induced adaptation changes in function and structure of cardiac muscle and vascular smooth muscle might be another important factor responsible for postflight cardiovascular dysfunction. Our previous studies have also shown that the ion channel remodeling mechanism of vascular smooth muscle cells (VSMCs) and vascular local renin-angiotensin system (L-RAS) might be involved in vascular region-specific adaptational changes to microgravity. Furthermore, currently used, exercise-based countermeasures seem insufficient to prevent the occurrence of cardiovascular dysfunction in future long-duration, exploration class mission. In the past two decades, intermittent artificial gravity (IAG) by incorporating a short-arm centrifuge into the spacecraft has been suggested as a gravity-based countermeasure for future spaceflight. Our previous studies have shown that daily short-duration exposure to -Gx (dorsoventral) gravitation by standing (STD) to restore the rat’s orthostatic posture , or -Gx with +Gz component by +45°head-up tilt, which mimics the IAG countermeasure, is surprisingly effective in preventing myocardial contractility depression and vascular changes. For example, it has been demonstrated that daily 1-h -Gx by STD is sufficient to prevent the differential changes in two kinds of medium-sized conduit arteries that might occur due to a 28-d simulated microgravity alone. Our work has further shown that simulated microgravity increases and decreases current densities and protein expression of CaL in cerebral and mesenteric arterial VSMCs,the countermeasure of 1 h/d -Gx can prevents the change of mesenteric artery but cannot prevent the change in cerebral artery. This study is on the basis of such hypothesis that in middle cerebral artery, 1h/d -Gx can prevent the thickening of structure induced by microgravity, but can not prevent the increase of myogenic tone and the enhancement of vasoconstriction. In mesenteric small artery, not only the 1h/d -Gx can prevent the attentuation of vasoconstriction and thinningz of structure induced by microgravity, but also can prevent the increase of myogenic tone.
To confirm our hypothesis mentioned above, we use tail-suspension rat model to simulate the cardiovascular dysfunction after flight and daily 1-h standing to simulate the countermeasure effect of IAG. The changes of vessel function and structure in rats were examined. The main work was divided into two parts:
(1) The first part of work was aim to examine the change of myogenic tone, the vasoconstriction of middle cerebral artery and mesenteric small artery after a short-term (3-day) simulated microgravity with and without 1-h/d -Gx countermeasure. After simulated microgravity, the middle cerebral artery and mesenteric small artery were isolated and cannulated, the responses to increases of pressure and concentrations of vaso-constrictor were detected.
(2) The second part of work was aim to examine the change of myogenic tone, the vasoconstriction and the vessel structure under electron microscope of middle cerebral artery and mesenteric small artery after a medium-term (28-day) simulated microgravity with and without 1-h/d -Gx countermeasure. After simulated microgravity, the middle cerebral artery and mesenteric small artery were isolated and cannulated, the responses to increases of pressure and concentrations of vaso-constrictor were detected, then fixed the vessel at in-situ length, the structure was examined with electronmicroscope.
The main findings of the present work are as follows:
(1) Simulated microgravity alone induced an enhancement of the myogenic tone and vasoconstrictor responsiveness in the isolated middle cerebral artery, increases the wall thiskness, the media thickness and the number of smooth muscle cell layers. Daily STD for 1 h prevented the changes of vessel structure, but did not prevent the functional enhancement in the middle cerebral artery. Compared with the simultaneous CON group, the myogenic tone and vasoconstriction to 5-HT of middle cerebral artery in SUS group (3-day) were increased 11.7%, 12.3%, respectively. In 28-day group, the myogenic tone and vasoconstriction to 5-HT of middle cerebral artery were increased 18.8 %, 13.7%, respectively. The wall thickness, the media thickness of middle cerebral artery in SUS group were increased by 56.4%(P<0.01), 63%(P<0.01), respectively, compared with that of in CON group. With 1h/d standing, the change of vessel structure can be prevented, but the increase of myogenic tone and vasoconstriction cannot be prevented.
(2) Simulated microgravity alone induced an attenuation of the myogenic tone and vasoconstrictor responsiveness in the isolated mesenteric small artery, decreases the wall thiskness, the media thickness and the number of smooth muscle cell layers. Daily STD for 1 h can prevent the changes of vessel structure, and can also prevent the functional decrement in the mesenteric small artery. Compared with the simultaneous CON group, the myogenic tone and vasoconstriction to PE of mesenteric small artery in SUS group (3-day) were decreased 11.5%, 12.1%, respectively. In 28-day group, the myogenic tone and vasoconstriction to PE of mesenteric small artery were decreased 22.5%, 21.6%, respectively. The wall thickness, the media thickness of mesenteric small artery in SUS group were decreased by 20.0%(P<0.01), 28.6%(P<0.01), respectively, compared with that of in CON group. With 1h/d standing, not only the change of vessel structure can be prevented, but the decrease of myogenic tone and vasoconstriction can also be prevented.
In conclusion, our working hypothesis has been supported by these above findings. Firstly, SUS alone induced an enhancement of the myogenic tone and vasoconstrictor responsiveness in the isolated middle cerebral artery but a depression of those in the mesenteric small artery. Secondly, the structure of middle cerebral artery and mesenteric small artery were changed by different effects. Daily standing for 1 h prevented the depression of myogenic tone and vasoconstrictor responsiveness in the mesenteric small artery, but did not prevent the functional enhancement in the middle cerebral artery. These data suggest that a short-term simulated microgravity may result in differential alterations in the function and structure of the cerebral artery and the resistance vessel in the hind-body. Both of the alteration of middle cerebral artery and mesenteric small artery can be prevented by 1h/d standing. However, only the functional changes in the mesenteric small arteries, not in the cerebral arteries, can be prevented by such a countermeasure of daily 1 h standing.
引文
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126.Zhang LF, Sun B, Cao XS, Liu C, Yu ZB, Zhang LN, Cheng JH, Wu YH, and Wu XY. Effectiveness of intermittent -Gx gravitation in preventing deconditioning due to simulated microgravity. J Appl Physiol 95: 207-218, 2003.
127.Zhang LF, Yu ZB, Ma J, Mao QW. Peripheral effector mechanism hypothesis of postflight cardiovascular dysfunction. Aviat Space Environ Med 72: 567-575, 2001.
128.Zhang LF, Zhang LN, Meng QJ, Fu ZJ. Research in differential adaptations of vessels to microgravity. J Gravit Physiol 9: P55-P58, 2002.
129.Zhang LF. Invited review: Vascular adaptation to microgravity: what have we learned? J Appl Physiol 91: 2415-2430, 2001.
130.Zhang LF. Letter to the Editor: Vascular adaptation to microgravity. J Appl Physiol 97:1584-5; author reply 1584-1587, 2004.
131.Zhang LF. Microgravity induced cardiovascular deconditioning: peripheral effecter mechanism hypothesis and gravity-based countermeasure. J Gravit Physiol 7: 135-136, 2000.
132.Zhang LF. Reply“Letter to the editor”: Vascular adaptation to microgravity: extending the hypothesis. J Appl Physiol 93: 1181-1182, 2002.
133.Zhang LF. System specificity in responsiveness to intermittent -Gx gravitation during simulated microgravity in rats. J Gravit Physiol 12: P1- P4, 2005.
134.Zhang LF, Cheng JH, Liu X, Wang SY, Liu Y, Lu HB and Ma J. Cardiovascular changes of conscious rats after simulated microgravity with and without daily -Gx gravitation. J Appl Physiol 105:1134-45, 2008.
135.Zhang LN, Gao F, Ma J, and Zhang LF. Daily head-up tilt, standing or centrifugation can prevent vasoreactivity changes in arteries of simulated weightless rats. J Gravit Physiol 7: P143-P144, 2000.
136.Zhang LN, Zhang LF, Ma J. Simulated microgravity enhances vasoconstrictor responsiveness of rat basilar artery. J Appl Physiol 90: 2296-305, 2001.
137.陈杰,马进,丁兆平,张立藩一种模拟长期失重影响的大鼠尾部悬吊模型空间科学学报13: 159-162, 1993.
138.高放,张立藩,黄威权,孙岚.慢性阻断血管紧张素Ⅱ1型受体不能完全防止模拟失重大鼠血管的适应性结构变化生理学报59: 821-830, 2007
139.孟庆军,李剑,张文红,张乐宁,张立藩抗血管紧张素原多克隆抗血清的制备及鉴定生理学报55: 110-113, 2003.
140.张立藩,余志斌,马进航天飞行后心血管失调的外周效应器机制假说。生理科学进展32: 13-17, 2001.
141.张立藩人工重力生物医学问题:以往工作回顾与面临的挑战航天医学与医学工程14:70-74, 2001.
142.张立藩,孟庆军展望新世纪的重力生理学生理科学进展33:276-284,2002.