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      PRG-1 prevents neonatal stimuli-induced persistent hyperalgesia and memory dysfunction via NSF/Glu/GluR2 signaling

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          Summary

          Neonatal repetitive noxious stimuli (RNS) has been shown to cause long-term harmful effects on nociceptive processing, learning, and memory which persist until adulthood. Plasticity-related gene 1 (PRG-1) regulates synaptic plasticity and functional reorganization in the brain during neuronal development. In this study, neonatal RNS rats were established by repetitive needle pricks to neonatal rats on all four feet to model repetitive pain exposure in infants. Neonatal RNS caused thermal hyperalgesia, mechanical allodynia, learning, and memory impairments which manifested in young rats and persisted until adulthood. Hippocampal PRG-1/N-ethylmaleimide sensitive fusion protein (NSF) interaction was determined to be responsible for the RNS-induced impairment via enhanced extracellular glutamate release and AMPAR GluR2 trafficking deficiency in a cell-autonomous manner. These pathways likely act synergistically to cause changes in dendritic spine density. Our findings suggest that PRG-1 prevents the RNS-induced hyperalgesia, learning, and memory impairment by regulating synaptic plasticity via NSF/Glu/GluR2 signaling.

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          Highlights

          • •

            Neonatal RNS induced hyperalgesia, learning, and memory impairment until adulthood.

          • •

            PRG-1 attenuated RNS-induced impairments by dendritic spine regulation.

          • •

            PRG-1 prevents RNS-induced impairments via NSF/Glu/GluR2 signaling.

          Abstract

          Behavioral neuroscience; Molecular neuroscience; Developmental neuroscience; Cellular neuroscience

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          Most cited references68

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          Morris water maze: procedures for assessing spatial and related forms of learning and memory.

          Charles V. Vorhees, Michael Williams (2006)
          The Morris water maze (MWM) is a test of spatial learning for rodents that relies on distal cues to navigate from start locations around the perimeter of an open swimming arena to locate a submerged escape platform. Spatial learning is assessed across repeated trials and reference memory is determined by preference for the platform area when the platform is absent. Reversal and shift trials enhance the detection of spatial impairments. Trial-dependent, latent and discrimination learning can be assessed using modifications of the basic protocol. Search-to-platform area determines the degree of reliance on spatial versus non-spatial strategies. Cued trials determine whether performance factors that are unrelated to place learning are present. Escape from water is relatively immune from activity or body mass differences, making it ideal for many experimental models. The MWM has proven to be a robust and reliable test that is strongly correlated with hippocampal synaptic plasticity and NMDA receptor function. We present protocols for performing variants of the MWM test, from which results can be obtained from individual animals in as few as 6 days.
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            Ethical guidelines for investigations of experimental pain in conscious animals

            Manfred Zimmermann (1983)
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              A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia

              K. Hargreaves, R Dubner, F. Brown … (1988)
              A method to measure cutaneous hyperalgesia to thermal stimulation in unrestrained animals is described. The testing paradigm uses an automated detection of the behavioral end-point; repeated testing does not contribute to the development of the observed hyperalgesia. Carrageenan-induced inflammation resulted in significantly shorter paw withdrawal latencies as compared to saline-treated paws and these latency changes corresponded to a decreased thermal nociceptive threshold. Both the thermal method and the Randall-Selitto mechanical method detected dose-related hyperalgesia and its blockade by either morphine or indomethacin. However, the thermal method showed greater bioassay sensitivity and allowed for the measurement of other behavioral parameters in addition to the nociceptive threshold.
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                Author and article information

                Contributors
                Tian Yu
                Zhi Xiao
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 24 August 2022
                Publication date Collection: 16 September 2022
                Publication date (Electronic): 24 August 2022
                Volume: 25
                Issue: 9
                Electronic Location Identifier: 104989
                Affiliations
                [1 ]Guizhou Key Laboratory of Brain Science, Zunyi Medical University, Xuefu West Road 6, Xinpu District, Zunyi 563000, China
                [2 ]Guizhou Key Laboratory of Anesthesia and Organ Protection, Zunyi Medical University, Xuefu West Road 6, Xinpu District, Zunyi 563000, China
                [3 ]Graduate School, Zunyi Medical University, Zunyi 563000, China
                [4 ]Clinical School, Zunyi Medical University, Zunyi 563000, China
                [5 ]Department of Pain Medicine, Affiliated Hospital of Zunyi Medical University, Zunyi 563000, China
                Author notes
                [∗ ]Corresponding author zyyutian@ 123456126.com
                [∗∗ ]Corresponding author zhixiao@ 123456zmu.edu.cn
                [6]

                Co-senior author

                [7]

                Lead contact

                Article
                Publisher Item ID: S2589-0042(22)01261-5 Publisher ID: 104989
                DOI: 10.1016/j.isci.2022.104989
                PMC ID: 9460187
                PubMed ID: 36093041
                SO-VID: 71489046-4d55-4938-9c96-e4f3d59bb8a1
                Copyright © © 2022 The Author(s)
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 6 May 2022
                Date revision received : 2 July 2022
                Date accepted : 17 August 2022
                Categories
                Subject: Article

                Keywords: behavioral neuroscience,molecular neuroscience,developmental neuroscience,cellular neuroscience
                Data availability:
                Keywords: behavioral neuroscience, molecular neuroscience, developmental neuroscience, cellular neuroscience

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