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Dental Pulp-Derived Stem Cells Preserve Astrocyte Health During Induced Gliosis by Modulating Mitochondrial Activity and Functions

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Abstract

Astrocytes have been implicated in the onset and complication of various central nervous system (CNS) injuries and disorders. Uncontrolled astrogliosis (gliosis), while a necessary process for recovery after CNS trauma, also causes impairments in CNS performance and functions. The ability to preserve astrocyte health and better regulate the gliosis process could play a major role in controlling damage in the aftermath of acute insults and during chronic dysfunction. Here in, we demonstrate the ability of dental pulp-derived stem cells (DPSCs) in protecting the health of astrocytes during induced gliosis. First of all, we have characterized the expression of genes in primary astrocytes that are relevant to the pathological conditions of CNS by inducing gliosis. Subsequently, we found that astrocytes co-cultured with DPSCs reduced ROS production, NRF2 and GCLM expressions, mitochondrial membrane potential, and mitochondrial functions compared to the astrocytes that were not co-cultured with DPSCs in gliosis condition. In addition, hyperactive autophagy was also decreased in astrocytes that were co-cultured with DPSCs compared to the astrocytes that were not co-cultured with DPSCs during gliosis. This reversal and mitigation of gliosis in astrocytes were partly due to induction of neurogenesis in DPSCs through enhanced expressions of the neuronal genes like GFAP, NeuN, and Synapsin in DPSCs and by secretion of higher amounts of neurotropic factors, such as BDNF, GDNF, and TIMP-2. Protein–Protein docking analysis suggested that BDNF and GDNF can bind with CSPG4 and block the downstream signaling. Together these findings demonstrate novel functions of DPSCs to preserve astrocyte health during gliosis.

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Data Availability

The datasets used and/or analyzed during the current study will be available on reasonable request.

Abbreviations

AD:

Alzheimer’s disease

ARE:

Antioxidant response element

BBB:

Blood–brain barrier

BDNF:

Brain-derived neurotrophic factor

CNS:

Central nervous system

CSPG4:

Chondroitin sulfate proteoglycan 4

DCF-DA:

2′7′-Dichlorodihydrofluorescein diacetate

DPSC:

Dental pulp-derived stem cell

ECAR:

Extracellular acidification rate

ELISA:

Enzyme-linked immunoassay

FCCP:

2-[2-[4-(Trifluoromethoxy) phenyl] hydrazinylidene]-propanedinitrile

GCLM:

Glutamate-cysteine ligase modifier

GDNF:

Glial-derived neurotrophic factor

GFAP:

Glial fibrillary acid protein

ICC:

Immunocytochemistry

IL-1β:

Interleukin-1β

Keap1:

Kelch-like ECH-associated protein

MHC-II:

Major histocompatibility complex-II

MMP:

Matrix metalloproteinase

NGF:

Nerve growth factor

NMOC:

Non-mitochondrial oxygen consumption

NRF2:

Nuclear factor erythroid 2-related factor 2

OCR:

Oxygen consumption rate

ROS:

Reactive oxygen species

RT-PCR:

Real-time polymerase chain reaction

SCI:

Spinal cord injury

TBI:

Traumatic brain injury

TGF-β:

Transforming growth factor-β

TIMP-2:

Tissue inhibitor of metalloproteinases-2

TNF:

Tumor necrosis factor

VEGF:

Vascular endothelial growth factor

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Acknowledgements

We sincerely acknowledge our funding authority, the National Institutes of Health R01AR068279 (NIAMS), STTR R42EY031196 (NEI), and STTR 1R41AG057242 (NIA).

Funding

This work was supported in part by the National Institutes of Health Grants, R01AR068279 (NIAMS), STTR R42EY031196 (NEI), and STTR 1R41AG057242 (NIA). The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

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  1. Department of Pharmaceutical Sciences, Jerry H. Hodge School of Pharmacy, Texas Tech University Health Sciences Center, ARB Suite 2116, 1406 South Coulter Street, Amarillo, TX, 79106, USA

    Derek Barthels, Prateeksha Prateeksha, Saeideh Nozohouri, Heidi Villalba, Yong Zhang, Sejal Sharma, Sarah Anderson, Md Sariful Islam Howlader, Adarsh Nambiar, Thomas J. Abbruscato & Hiranmoy Das

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  1. Derek Barthels
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  2. Prateeksha Prateeksha
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  3. Saeideh Nozohouri
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All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be published. Study conception, design, and manuscript writing: DB and HD. Acquisition of data: DB, PP, SN, HV, YZ, SS, SA, MSIH, and AN. Analysis and interpretation of data: DB, FP, TJA, and HD.

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Barthels, D., Prateeksha, P., Nozohouri, S. et al. Dental Pulp-Derived Stem Cells Preserve Astrocyte Health During Induced Gliosis by Modulating Mitochondrial Activity and Functions. Cell Mol Neurobiol 43, 2105–2127 (2023). https://doi.org/10.1007/s10571-022-01291-8

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