Mitochondrial aerobic respiration is activated during hair follicle stem cell differentiation, and its dysfunction retards hair regeneration

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Abstract

Background. Emerging research revealed the essential role of mitochondria in regulating stem/progenitor cell differentiation of neural progenitor cells, mesenchymal stem cells and other stem cells through reactive oxygen species (ROS), Notch or other signaling pathway. Inhibition of mitochondrial protein synthesis results in hair loss upon injury. However, alteration of mitochondrial morphology and metabolic function during hair follicle stem cells (HFSCs) differentiation and how they affect hair regeneration has not been elaborated upon.

Methods. We compared the difference in mitochondrial morphology and activity between telogen bulge cells and anagen matrix cells. Expression levels of mitochondrial ROS and superoxide dismutase 2 (SOD2) were measured to evaluate redox balance. In addition, the level of pyruvate dehydrogenase kinase (PDK) and pyruvate dehydrogenase (PDH) were estimated to present the change in energetic metabolism during differentiation. To explore the effect of the mitochondrial metabolism on regulating hair regeneration, hair growth was observed after application of a mitochondrial respiratory inhibitor upon hair plucking.

Results. During HFSCs differentiation, mitochondria became elongated with more abundant organized cristae and showed higher activity in differentiated cells. SOD2 was enhanced for redox balance with relatively stable ROS levels in differentiated cells. PDK increased in HFSCs while differentiated cells showed enhanced PDH, indicating that respiration switched from glycolysis to oxidative phosphorylation during differentiation. Inhibiting mitochondrial respiration in differentiated hair follicle cells upon hair plucking repressed hair regeneration in vivo.

Conclusions. Upon HFSCs differentiation, mitochondria are elongated with more abundant cristae and show higher activity, accompanying with activated aerobic respiration in differentiated cells for higher energy supply. Also, dysfunction of mitochondrial respiration delays hair regeneration upon injury.

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Most cited references 33

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Controls of hair follicle cycling.

K Stenn, R Paus (2001)

Nearly 50 years ago, Chase published a review of hair cycling in which he detailed hair growth in the mouse and integrated hair biology with the biology of his day. In this review we have used Chase as our model and tried to put the adult hair follicle growth cycle in perspective. We have tried to sketch the adult hair follicle cycle, as we know it today and what needs to be known. Above all, we hope that this work will serve as an introduction to basic biologists who are looking for a defined biological system that illustrates many of the challenges of modern biology: cell differentiation, epithelial-mesenchymal interactions, stem cell biology, pattern formation, apoptosis, cell and organ growth cycles, and pigmentation. The most important theme in studying the cycling hair follicle is that the follicle is a regenerating system. By traversing the phases of the cycle (growth, regression, resting, shedding, then growth again), the follicle demonstrates the unusual ability to completely regenerate itself. The basis for this regeneration rests in the unique follicular epithelial and mesenchymal components and their interactions. Recently, some of the molecular signals making up these interactions have been defined. They involve gene families also found in other regenerating systems such as fibroblast growth factor, transforming growth factor-beta, Wnt pathway, Sonic hedgehog, neurotrophins, and homeobox. For the immediate future, our challenge is to define the molecular basis for hair follicle growth control, to regenerate a mature hair follicle in vitro from defined populations, and to offer real solutions to our patients' problems.

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Morphogenesis and renewal of hair follicles from adult multipotent stem cells.

Hideo Oshima, Ariane Rochat, Cécile Kedzia … (2001)

The upper region of the outer root sheath of vibrissal follicles of adult mice contains multipotent stem cells that respond to morphogenetic signals to generate multiple hair follicles, sebaceous glands, and epidermis, i.e., all the lineages of the hairy skin. At the time when hair production ceases and when the lower region of the follicle undergoes major structural changes, the lower region contains a significant number of clonogenic keratinocytes, and can then respond to morphogenetic signals. This demonstrates that multipotent stem cells migrate to the root of the follicle to produce whisker growth. Moreover, our results indicate that the clonogenic keratinocytes are closely related, if not identical, to the multipotent stem cells, and that the regulation of whisker growth necessitates a precise control of stem cell trafficking.

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Mitochondria: from cell death executioners to regulators of cell differentiation.

Atsuko Kasahara, Luca Scorrano (2014)

Most, if not all mitochondrial functions, including adenosine-5'-triphosphate (ATP) production and regulation of apoptosis and Ca(2+) homeostasis, are inextricably linked to mitochondrial morphology and dynamics, a process controlled by a family of GTP-dependent dynamin related 'mitochondria-shaping' proteins. Mitochondrial fusion and fission directly influence mitochondrial metabolism, apoptotic and necrotic cell death, autophagy, muscular atrophy and cell migration. In this review, we discuss the recent evidence indicating that mitochondrial dynamics influence complex signaling pathways, affect gene expression and define cell differentiation. These findings extend the importance of mitochondria to developmental biology, far beyond their mere bioenergetic role.

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Author and article information

Contributors

Ji Li

Journal

Journal ID (nlm-ta): PeerJ

Journal ID (iso-abbrev): PeerJ

Journal ID (pmc): PeerJ

Journal ID (publisher-id): PeerJ

Title: PeerJ

Publisher: PeerJ Inc. (San Francisco, USA )

ISSN (Electronic): 2167-8359

Publication date (Electronic): 3 May 2016

Publication date Collection: 2016

Volume: 4

Electronic Location Identifier: e1821

Affiliations

[1 ]Department of Dermatology, Xiangya Hospital, Central South University , Changsha, Hunan, China

[2 ]Department of Dermatology, The Third Xiangya Hospital, Central South University , Changsha, Hunan, China

[3 ]Department of Infectious Diseases and Hunan Key Laboratory of Viral Hepatitis, Xiangya Hospital, Central South University , Changsha, Hunan, China

Article

Publisher ID: 1821

DOI: 10.7717/peerj.1821

PMC ID: 4860312

PubMed ID: 27168957

SO-VID: 7f728c00-2b9b-4927-b51a-58aa1a849ac0

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

History

Date received : 5 January 2016

Date accepted : 26 February 2016

Funding

Funded by: National Natural Science Foundation of China

Award ID: 81171520

Award ID: 81371756

Award ID: 81271775

Award ID: 81402623

Funded by: Hunan Provincial Natural Science Foundation of China

Award ID: 2015JJ1023

This research was supported by the National Natural Science Foundation of China (81171520, 81371756, 81271775, 81402623), Hunan Provincial Natural Science Foundation of China (2015JJ1023). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Mitochondrial aerobic respiration is activated during hair follicle stem cell differentiation, and its dysfunction retards hair regeneration

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Stress signalling in stem cells

Most cited references 33

Controls of hair follicle cycling.

Morphogenesis and renewal of hair follicles from adult multipotent stem cells.

Mitochondria: from cell death executioners to regulators of cell differentiation.

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