AbstractAstrocytes are multi-functional glial cells in the central nervous system that play critical roles in modulation of metabolism, extracellular ion and neurotransmitter levels, and synaptic plasticity. Astrocyte-derived signaling molecules mediate many of these modulatory functions of astrocytes, including vesicular release of ATP.

摘要星形胶质细胞是中枢神经系统中的多功能神经胶质细胞，在调节代谢，细胞外离子和神经递质水平以及突触可塑性中起关键作用。。

In the present study, we used a unique genetic mouse model to investigate the functional significance of astrocytic exocytosis of ATP. Using primary cultured astrocytes, we show that loss of vesicular nucleotide transporter (Vnut), a primary transporter responsible for loading cytosolic ATP into the secretory vesicles, dramatically reduces ATP loading into secretory lysosomes and ATP release, without any change in the molecular machinery of exocytosis or total intracellular ATP content.

在本研究中，我们使用了一种独特的遗传小鼠模型来研究ATP星形细胞胞吐的功能意义。使用原代培养的星形胶质细胞，我们显示囊泡核苷酸转运蛋白（Vnut）的丢失，这是一种负责将胞质ATP加载到分泌囊泡中的主要转运蛋白，可显着降低ATP加载到分泌溶酶体和ATP释放中，而胞吐的分子机制或细胞内总ATP含量没有任何变化。

Deletion of astrocytic Vnut in adult mice leads to increased anxiety, depressive-like behaviors, and decreased motivation for reward, especially in females, without significant impact on food intake, systemic glucose metabolism, cognition, or sociability. These behavioral alterations are associated with significant decreases in the basal extracellular dopamine levels in the nucleus accumbens.

成年小鼠星形胶质细胞Vnut的缺失导致焦虑增加，抑郁样行为增加，奖励动机降低，尤其是女性，对食物摄入，全身葡萄糖代谢，认知或社交能力没有显着影响。这些行为改变与伏隔核中基础细胞外多巴胺水平的显着降低有关。

Likewise, ex vivo brain slices from these mice show a strong trend toward a reduction in evoked dopamine release in the nucleus accumbens. Mechanistically, the reduced dopamine signaling we observed is likely due to an increased expression of monoamine oxidases. Together, these data demonstrate a key modulatory role of astrocytic exocytosis of ATP in anxiety, depressive-like behavior, and motivation for reward, by regulating the mesolimbic dopamine circuitry..

同样，来自这些小鼠的离体脑切片显示出伏隔核中诱发的多巴胺释放减少的强烈趋势。从机制上讲，我们观察到的多巴胺信号传导减少可能是由于单胺氧化酶的表达增加。总之，这些数据通过调节中脑边缘多巴胺回路，证明了ATP星形细胞胞吐在焦虑，抑郁样行为和奖励动机中的关键调节作用。。

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Fig. 1: Vnut deletion in primary astrocytes does not cause major changes in the expression of signature astrocyte marker genes.Fig. 2: Loss of Vnut impairs ATP loading into secretory lysosomes and ATP release in primary astrocytes.Fig. 3: Loss of Vnut in astrocytes in adult mice shows minor effects on the expression of astrocyte marker genes, as well as genes involved in exocytosis and lysosomes.Fig.

图1：原代星形胶质细胞中的Vnut缺失不会引起特征性星形胶质细胞标记基因表达的重大变化。图2:Vnut的丢失会损害ATP加载到分泌溶酶体中以及原代星形胶质细胞中的ATP释放。。图。

4: Loss of Vnut in astrocytes in adult mice does not affect systemic glucose metabolism and insulin sensitivity.Fig. 5: Astrocyte-specific Vnut KO female mice display increased anxiety and depressive-like behavior.Fig. 6: Astrocytic Vnut in the nucleus accumbens is a critical mediator for depressive-like behavior in female mice in response to inescapable stress.Fig.

4： 成年小鼠星形胶质细胞中Vnut的丢失不影响全身葡萄糖代谢和胰岛素敏感性。图5：星形胶质细胞特异性Vnut KO雌性小鼠表现出增加的焦虑和抑郁样行为。图6：伏隔核中的星形胶质细胞Vnut是雌性小鼠应对不可避免的压力时抑郁样行为的关键介质。图。

7: The effects of astrocytic Vnut loss in adult female mice on evoked dopamine release in the nucleus accumbens.Fig. 8: Loss of Vnut in Aldh1l1+ astrocytes increases depressive-like behavior and reduces motivation for reward in adult female mice..

7： 。图8:Aldh1l1+星形胶质细胞中Vnut的丧失增加了成年雌性小鼠的抑郁样行为并降低了奖励动机。。

Data availability

数据可用性

The present study does not include any omics data to be deposited to the public repository. All the raw images and raw data will be provided upon request for research purpose only.

本研究不包括任何要保存到公共存储库的组学数据。所有原始图像和原始数据将根据要求提供，仅供研究之用。

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Download referencesAcknowledgementsThis work was supported by NIH grants R01 MH125903 and R03 AG083363 (to W.C.) and the Programs in Pharmacology and Experimental Therapeutics and Pharmacology and Drug Development of the Tufts University Graduate School of Biomedical Sciences (E.N.P.).

。

We thank Dr. Bradford Lowell’s laboratory at BIDMC, Harvard Medical School for the development and sharing of the Vnutf/f mice (P30 DK057521, P30 DK046200, R01 DK075632, R01 DK096010, R01 DK089044, and R01 DK071051, to B.B.L). A.E. is funded by an NIH grant R01 DK122167. The Imaging Center at the New York Institute of Technology provided important support.Author informationAuthors and AffiliationsDepartment of Molecular and Cellular Biochemistry, the Barnstable Brown Diabetes and Obesity Center, University of Kentucky College of Medicine, Lexington, KY, USAQian Huang & Weikang CaiDepartment of Biomedical Sciences, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, NY, USAQian Huang, Hiu Ham Lee, Bryan Volpe, Allen Li, Alyssa Lee, Sharon Tang, Chun Wa Wong, Yuan Huang, Raddy L.

我们感谢哈佛医学院BIDMC的Bradford Lowell博士实验室开发和共享Vnutf/f小鼠（P30 DK057521，P30 DK046200，R01 DK075632，R01 DK096010，R01 DK089044和R01 DK071051，B.B.L）。A、 E.由NIH拨款R01 DK122167资助。纽约理工学院成像中心提供了重要支持。作者信息作者和附属机构肯塔基大学医学院Barnstable Brown糖尿病与肥胖中心分子与细胞生物化学系，肯塔基州列克星敦，USAQian Huang＆Weikang Cai纽约理工大学骨科医学院生物医学系，纽约州老韦斯特伯里，USAQian Huang，Hiu Ham Lee，Bryan Volpe，Allen Li，Alyssa Lee，Sharon Tang，Chun Wa Wong，Yuan Huang，Raddy L。

Ramos, Randy F. Stout & Weikang CaiProgram in Pharmacology and Experimental Therapeutics and Pharmacology and Drug Development, Graduate School of Biomedical Sciences and Department of Immunology, Tufts University School of Medicine, Boston, MA, USAQingchen Zhang, Chang Xue, Yahia R. Abuhasan, Lingyun Li, Jeremy S.

Ramos，Randy F.Stout＆Weikang Cai药理学和实验疗法以及药理学和药物开发项目，塔夫茨大学医学院生物医学研究生院和免疫学系，马萨诸塞州波士顿，USAQingchen Zhang，Chang Xue，Yahia R.Abuhasan，Lingyun Li，Jeremy S。

Yang, Julie Egholm & Emmanuel N. PothosSection of Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA, USABrian C. Liu & C. Ronald KahnAnn Romney Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USACristina Gutierrez-Vazquez & Francisco J.

Yang，Julie Egholm＆Emmanuel N.波托什综合生理学和代谢科，乔斯林糖尿病中心，哈佛医学院，波士顿，马萨诸塞州，USABrian C.Liu＆C。哈佛医学院布莱根妇女医院罗纳德·卡南·罗姆尼神经系统疾病中心，马萨诸塞州波士顿，USACristina Gutierrez-Vazquez＆Francisco J。

QuintanaKey Laboratory of Ge.

通用电气金塔纳基实验室。

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PubMed Google ScholarContributionsHQ designed the study, performed experiments, and analyzed data. HHL, BV, QZ, CX, BCL, YRA, LL, JSY, JE, CGV, AL, AL, ST, CWW, TL, YH, RLR, RFS, AEO, FJQ, and BBL helped design and performed experiments. CRK and ENP helped design the experiments and provided edits for the manuscript.

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WC designed the study, supervised all work, and wrote the manuscript.Corresponding authorCorrespondence to.

WC设计了这项研究，监督了所有工作，并撰写了手稿。对应作者对应。

Weikang Cai.Ethics declarations

蔡维康。道德宣言

Competing interests

相互竞争的利益

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et al. Deletion of murine astrocytic vesicular nucleotide transporter increases anxiety and depressive-like behavior and attenuates motivation for reward..

小鼠星形胶质细胞囊泡核苷酸转运蛋白的缺失会增加焦虑和抑郁样行为，并减弱奖励的动机。。

Mol Psychiatry (2024). https://doi.org/10.1038/s41380-024-02692-5Download citationReceived: 06 February 2024Revised: 17 July 2024Accepted: 02 August 2024Published: 09 August 2024DOI: https://doi.org/10.1038/s41380-024-02692-5Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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