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Low-intensity focused ultrasound stimulation promotes stroke recovery via astrocytic HMGB1 and CAMK2N1 in mice

Lin Qi, Cheng Wang, Lidong Deng, Jia-Ji Pan, Qian Suo, Shengju Wu, Lin Cai, Xudong Shi, Junfeng Sun, Yongting Wang, Yaohui Tang, Weibao Qiu, Guo-Yuan Yang, Jixian Wang, Zhijun Zhang

Stroke and Vascular Neurology 2024, 9, 505-518 · 10.1136/svn-2023-002614

rodentstrokebehaviouremg mephistology molecularcerebral haemodynamics

Abstract

Background Low-intensity focused ultrasound stimulation (LIFUS) has been developed to enhance neurological repair and remodelling during the late acute stage of ischaemic stroke in rodents. However, the cellular and molecular mechanisms of neurological repair and remodelling after LIFUS in ischaemic stroke are unclear. Methods Ultrasound stimulation was treated in adult male mice 7 days after transient middle cerebral artery occlusion. Angiogenesis was measured by laser speckle imaging and histological analyses. Electromyography and fibre photometry records were used for synaptogenesis. Brain atrophy volume and neurobehaviour were assessed 0-14 days after ischaemia. iTRAQ proteomic analysis was performed to explore the differentially expressed protein. scRNA-seq was used for subcluster analysis of astrocytes. Fluorescence in situ hybridisation and Western blot detected the expression of HMGB1 and CAMK2N1. Results Optimal ultrasound stimulation increased cerebral blood flow, and improved neurobehavioural outcomes in ischaemic mice (p Conclusion Our results demonstrated that LIFUS promoted angiogenesis and synaptogenesis after focal cerebral ischaemia by upregulating HMGB1 and downregulating CAMK2N1 in a subcluster of astrocytes, suggesting that LIFUS activated specific astrocyte subcluster could be a key target for ischaemic brain therapy.

Abstract via europepmc.

Speciesmouse (C57BL/6J)
Subjectsnot reported animals
Sessions per subjectnot reported
Randomisedyes
Blindingsingle
Sham / controlno treatment control
Auditory controlnot reported
Readout timingboth
Anaesthesianot reported
Readoutsbehaviour, emg mep, histology molecular, cerebral haemodynamicsLaser speckle imaging of cerebral blood flow; fibre photometry (GCaMP6s) calcium imaging; Western blot; fluorescence in situ hybridisation (FISH); qPCR; immunostaining (CD31/Ki67, lectin); Golgi-Cox staining; scRNA-seq; iTRAQ proteomics
Direction of effectexcitatoryLIFUS increased the frequency of fibre-photometry calcium transients and EMG amplitude in stimulated (US, IS US) mice relative to unstimulated groups, indicating increased neural/motor activity during stimulation, alongside promotion of angiogenesis and synaptogenesis.
Adverse eventsobservedCresyl violet staining results showed that US3 damaged the ipsilateral hemisphere in both young and aged healthy mice compared with the control, indicated that 10 min was an overtime of stimulation.

Exposures

Exposure 1: LIFUS to ipsilateral hemisphere after MCAO

Target: hemisphere unspecified — “ipsilateral hemisphere (perifocal region of MCAO territory)
Device: custom-built · Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences · Ultrasound Neurostimulation System

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)not reportedimplied by duty cycle ÷ PRF: 0.5 ms (not stated by the paper)
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)50✓✓
Sonication duration (s)0.3✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Ispta, domain unspecified (W/cm²)0.022, 0.101, 0.201swept✓✓
Protocol, in the paper’s words

500 kHz pulse repetition frequency (PRF), 300 ms sonication duration (SD) and 50% duty cycle (DC) were used across all the ultrasound experiments (figure 1D). Separately, ultrasonic intensity (22, 101, 201 mW/cm2) and total stimulation duration (1, 3, 5, or 10 min, every other day) were varied to optimise the treatment; 3 min at 101 mW/cm2 every other day (US1) was chosen as the optimal protocol starting 7 days after MCAO.

Flags from extraction

  • exposures[0].timing.pulse_repetition_frequency_hzMain text states PRF = 500 kHz (identical to the 500 kHz carrier frequency, likely an error), while the Figure 1D legend states 'PRF was 1 kHz and 1/PRF was 1 s' (internally inconsistent, since 1 kHz implies a 1 ms period, not 1 s). The two statements conflict and neither could be confirmed, so PRF is left not_reported.
  • exposures[0].timing.sonication_duration_sThe paper labels 300 ms as 'sonication duration (SD)' in the pulse-diagram parameters, but separately reports total per-session ultrasound exposure durations of 1, 3, 5, or 10 minutes; it is unclear which corresponds to the schema's one-uninterrupted-train duration, so left not_reported and both durations are described in protocol_description.
  • n_subjectsPaper reports many different per-experiment group sizes (n=120 total mice allocated; n=12/group for behaviour and imaging; ~n=4/group for other assays; n=3-7 in various figure panels) without stating a single total number of animals exposed to ultrasound.
  • n_sessions_per_subjectUltrasound was given 'every other day' from day 7 post-MCAO, but the total number of stimulation sessions per animal is not explicitly stated.
  • sham_typeThe comparison for the ultrasound intervention is an untreated (no-device) stroke group (IS); the paper does not describe a device-based sham (e.g., powered-off transducer) for these experiments, so no listed vocabulary term fits precisely.
  • exposures[0].unspecified_domain.ispta_w_cm2Paper does not state whether the 22/101/201 mW/cm2 ultrasonic intensity values are free-field or in-situ; domain left unspecified.