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Research Articles, Neurobiology of Disease

Ventrolateral Periaqueductal Gray Astrocytes Regulate Nociceptive Sensation and Emotional Motivation in Diabetic Neuropathic Pain

Lan Yang, Jingshan Lu, Jianpeng Guo, Jian Chen, Fangfang Xiong, Xinyao Wang, Li Chen and Changxi Yu
Journal of Neuroscience 26 October 2022, 42 (43) 8184-8199; DOI: https://doi.org/10.1523/JNEUROSCI.0920-22.2022
Lan Yang
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
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  • ORCID record for Lan Yang
Jingshan Lu
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
2Fujian Center for Safety Evaluation of New Drug, Fujian Medical University, Fuzhou, 350122, Fujian China
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Jianpeng Guo
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
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Jian Chen
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
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Fangfang Xiong
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
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Xinyao Wang
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
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Li Chen
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
3Fujian Key Laboratory of Drug Target Discovery and Structural and Functional Research, Fujian Medical University, Fuzhou, 350122, Fujian China
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Changxi Yu
1Department of Pharmacology, School of Pharmacy, Fujian Medical University, Fuzhou, 350122, Fujian China
3Fujian Key Laboratory of Drug Target Discovery and Structural and Functional Research, Fujian Medical University, Fuzhou, 350122, Fujian China
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Abstract

Diabetic neuropathic pain (DNP) is a diabetes complication experienced by many patients. Ventrolateral periaqueductal gray (vlPAG) neurons are essential mediators of the descending pain modulation system, yet the role of vlPAG astrocytes in DNP remains unclear. The present study applied a multidimensional approach to elucidate the role of these astrocytes in DNP. We verified the activation of astrocytes in different regions of the PAG in male DNP-model rats. We found that only astrocytes in the vlPAG exhibited increased growth. Furthermore, we described differences in vlPAG astrocyte activity at different time points during DNP progression. After the 14th day of modeling, vlPAG astrocytes exhibited obvious activation and morphologic changes. Furthermore, activation of Gq-designer receptors exclusively activated by a designer drug (Gq-DREADDs) in vlPAG astrocytes in naive male rats induced neuropathic pain-like symptoms and pain-related aversion, whereas activation of Gi-DREADDs in vlPAG astrocytes in male DNP-model rats alleviated sensations of pain and promoted pain-related preference behavior. Thus, bidirectional manipulation of vlPAG astrocytes revealed their potential to regulate pain. Surprisingly, activation of Gi-DREADDs in vlPAG astrocytes also mitigated anxiety-like behavior induced by DNP. Thus, our results provide direct support for the hypothesis that vlPAG astrocytes regulate diabetes-associated neuropathic pain and concomitant anxiety-like behavior.

SIGNIFICANCE STATEMENT Many studies examined the association between the ventrolateral periaqueductal gray (vlPAG) and neuropathic pain. However, few studies have focused on the role of vlPAG astrocytes in diabetic neuropathic pain (DNP) and DNP-related emotional changes. This work confirmed the role of vlPAG astrocytes in DNP by applying a more direct and robust approach. We used chemogenetics to bidirectionally manipulate the activity of vlPAG astrocytes and revealed that vlPAG astrocytes regulate DNP and pain-related behavior. In addition, we discovered that activation of Gi-designer receptors exclusively activated by a designer drug in vlPAG astrocytes alleviated anxiety-like behavior induced by DNP. Together, these findings provide new insights into DNP and concomitant anxiety-like behavior and supply new therapeutic targets for treating DNP.

  • astrocytes
  • chemogenetic
  • diabetic neuropathic pain
  • emotional motivation
  • ventrolateral periaqueductal gray

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The Journal of Neuroscience: 42 (43)
Journal of Neuroscience
Vol. 42, Issue 43
26 Oct 2022
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Ventrolateral Periaqueductal Gray Astrocytes Regulate Nociceptive Sensation and Emotional Motivation in Diabetic Neuropathic Pain
Lan Yang, Jingshan Lu, Jianpeng Guo, Jian Chen, Fangfang Xiong, Xinyao Wang, Li Chen, Changxi Yu
Journal of Neuroscience 26 October 2022, 42 (43) 8184-8199; DOI: 10.1523/JNEUROSCI.0920-22.2022

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Ventrolateral Periaqueductal Gray Astrocytes Regulate Nociceptive Sensation and Emotional Motivation in Diabetic Neuropathic Pain
Lan Yang, Jingshan Lu, Jianpeng Guo, Jian Chen, Fangfang Xiong, Xinyao Wang, Li Chen, Changxi Yu
Journal of Neuroscience 26 October 2022, 42 (43) 8184-8199; DOI: 10.1523/JNEUROSCI.0920-22.2022
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Keywords

  • astrocytes
  • chemogenetic
  • diabetic neuropathic pain
  • emotional motivation
  • ventrolateral periaqueductal gray

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