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Cells
Volume 13
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10.3390/cells13030204
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Article

Prospective Approach to Deciphering the Impact of Intercellular Mitochondrial Transfer from Human Neural Stem Cells and Brain Tumor-Initiating Cells to Neighboring Astrocytes

by
Jerusha Boyineni
1,
Jason Michael Wood
2,
Aditya Ravindra
1,
Ethan Boley
1,
Sarah E. Donohue
3,
Marcelo Bento Soares
1,4,5 and
Sergey Malchenko
1,*
1
Department of Cancer Biology and Pharmacology, University of Illinois College of Medicine Peoria, Peoria, IL 61605, USA
2
Research Informatics Core, University of Illinois at Chicago, Chicago, IL 60607, USA
3
Research Services, University of Illinois College of Medicine Peoria, Peoria, IL 61605, USA
4
Department of Psychiatry & Behavioral Medicine, University of Illinois College of Medicine Peoria, Peoria, IL 61605, USA
5
Department of Neurosurgery, University of Illinois College of Medicine Peoria, Peoria, IL 61605, USA
*
Author to whom correspondence should be addressed.
Cells 2024, 13(3), 204; https://doi.org/10.3390/cells13030204
Submission received: 5 December 2023 / Revised: 18 January 2024 / Accepted: 20 January 2024 / Published: 23 January 2024
(This article belongs to the Special Issue The Pivotal Role of Tumor Stem Cells in Glioblastoma)
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Abstract

The communication between neural stem cells (NSCs) and surrounding astrocytes is essential for the homeostasis of the NSC niche. Intercellular mitochondrial transfer, a unique communication system that utilizes the formation of tunneling nanotubes for targeted mitochondrial transfer between donor and recipient cells, has recently been identified in a wide range of cell types. Intercellular mitochondrial transfer has also been observed between different types of cancer stem cells (CSCs) and their neighboring cells, including brain CSCs and astrocytes. CSC mitochondrial transfer significantly enhances overall tumor progression by reprogramming neighboring cells. Despite the urgent need to investigate this newly identified phenomenon, mitochondrial transfer in the central nervous system remains largely uncharacterized. In this study, we found evidence of intercellular mitochondrial transfer from human NSCs and from brain CSCs, also known as brain tumor-initiating cells (BTICs), to astrocytes in co-culture experiments. Both NSC and BTIC mitochondria triggered similar transcriptome changes upon transplantation into the recipient astrocytes. In contrast to NSCs, the transplanted mitochondria from BTICs had a significant proliferative effect on the recipient astrocytes. This study forms the basis for mechanistically deciphering the impact of intercellular mitochondrial transfer on recipient astrocytes, which will potentially provide us with new insights into the mechanisms of mitochondrial retrograde signaling.
Keywords: neural stem cells; cancer stem cells; astrocytes; intercellular mitochondrial transfer neural stem cells; cancer stem cells; astrocytes; intercellular mitochondrial transfer

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MDPI and ACS Style

Boyineni, J.; Wood, J.M.; Ravindra, A.; Boley, E.; Donohue, S.E.; Soares, M.B.; Malchenko, S. Prospective Approach to Deciphering the Impact of Intercellular Mitochondrial Transfer from Human Neural Stem Cells and Brain Tumor-Initiating Cells to Neighboring Astrocytes. Cells 2024, 13, 204. https://doi.org/10.3390/cells13030204

AMA Style

Boyineni J, Wood JM, Ravindra A, Boley E, Donohue SE, Soares MB, Malchenko S. Prospective Approach to Deciphering the Impact of Intercellular Mitochondrial Transfer from Human Neural Stem Cells and Brain Tumor-Initiating Cells to Neighboring Astrocytes. Cells. 2024; 13(3):204. https://doi.org/10.3390/cells13030204

Chicago/Turabian Style

Boyineni, Jerusha, Jason Michael Wood, Aditya Ravindra, Ethan Boley, Sarah E. Donohue, Marcelo Bento Soares, and Sergey Malchenko. 2024. "Prospective Approach to Deciphering the Impact of Intercellular Mitochondrial Transfer from Human Neural Stem Cells and Brain Tumor-Initiating Cells to Neighboring Astrocytes" Cells 13, no. 3: 204. https://doi.org/10.3390/cells13030204

APA Style

Boyineni, J., Wood, J. M., Ravindra, A., Boley, E., Donohue, S. E., Soares, M. B., & Malchenko, S. (2024). Prospective Approach to Deciphering the Impact of Intercellular Mitochondrial Transfer from Human Neural Stem Cells and Brain Tumor-Initiating Cells to Neighboring Astrocytes. Cells, 13(3), 204. https://doi.org/10.3390/cells13030204

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