Platelets Facilitate the Wound-Healing Capability of Mesenchymal Stem Cells by Mitochondrial Transfer and Metabolic Reprogramming

Levoux, Jennyfer; Prola, Alexandre; Lafuste, Peggy; Gervais, Marianne; Chevallier, Nathalie; Koumaiha, Zeynab; Kefi, Kaouthar; Braud, Laura; Schmitt, Alain; Yacia, Azzedine; Schirmann, Aurélie; Hersant, Barbara; Sid-Ahmed, Mounia; Larbi, Sabrina Ben; Komrsková, Kateřina; Rohlena, Jakub; Relaix, Frédéric; Neužil, Jiřı́; Rodriguez, Anne‐Marie

doi:10.1016/j.cmet.2020.12.006

Cited by 117 publications

(109 citation statements)

References 85 publications

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“…These were defined by their ability to be stained with mitochondrial dyes (mitotracker or JC-1), their oxygen consumption and their ultrastructure. Subsequent studies showed evidence for the presence of cell-free mitochondria associated with cell lines, microglia and biological fluids ( Joshi et al, 2019 ; Puhm et al, 2019 ; Al Amir Dache et al, 2020 ; Choong et al, 2020 ; Levoux et al, 2021 ; Peruzzotti-Jametti et al, 2021 ).…”

Section: Evidence For the Release Of Mitochondrial Materials From Cellsmentioning

confidence: 99%

Mitochondrial Extracellular Vesicles – Origins and Roles

Amari

Germain

2021

Front. Mol. Neurosci.

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Extracellular vesicles (EVs) have emerged in the last decade as critical cell-to-cell communication devices used to carry nucleic acids and proteins between cells. EV cargo includes plasma membrane and endosomal proteins, but EVs also contain material from other cellular compartments, including mitochondria. Within cells, mitochondria are responsible for a large range of metabolic reactions, but they can also produce damaging levels of reactive oxygen species and induce inflammation when damaged. Consistent with this, recent evidence suggests that EV-mediated transfer of mitochondrial content alters metabolic and inflammatory responses of recipient cells. As EV mitochondrial content is also altered in some pathologies, this could have important implications for their diagnosis and treatment. In this review, we will discuss the nature and roles of mitochondrial EVs, with a special emphasis on the nervous system.

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Section: Evidence For the Release Of Mitochondrial Materials From Cellsmentioning

confidence: 99%

Mitochondrial Extracellular Vesicles – Origins and Roles

Amari

Germain

2021

Front. Mol. Neurosci.

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“…The clot holds a role as an initial matrix scaffold rich in growth factors that will recruit cells for further wound healing stages ( Etulain, 2018 ). Platelets were also shown to produce a positive effect on mouse skin wound healing by enhancing the angiogenic potential of mesenchymal SCs ( Levoux et al, 2021 ). Upon activation, platelets release respiration-competent mitochondria that are internalised by recipient mesenchymal SCs, where it stimulates their metabolism to produce increased levels of certain metabolites.…”

Section: Wound Repair Mechanisms In Skin Oesophagus and Oral Epitheliamentioning

confidence: 99%

“…Upon activation, platelets release respiration-competent mitochondria that are internalised by recipient mesenchymal SCs, where it stimulates their metabolism to produce increased levels of certain metabolites. Particularly citrate, which works as the main fuel for de novo fatty acid synthesis that in turn increase secretion of pro-angiogenic factors by mesenchymal SCs ( Levoux et al, 2021 ). The inflammatory phase of wounding response starts with the recruitment of immune cells that travel to the injury site in order to remove pathogenic microbes.…”

Section: Wound Repair Mechanisms In Skin Oesophagus and Oral Epitheliamentioning

confidence: 99%

A Scarless Healing Tale: Comparing Homeostasis and Wound Healing of Oral Mucosa With Skin and Oesophagus

Pereira

Sequeira

2021

Front. Cell Dev. Biol.

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Epithelial tissues are the most rapidly dividing tissues in the body, holding a natural ability for renewal and regeneration. This ability is crucial for survival as epithelia are essential to provide the ultimate barrier against the external environment, protecting the underlying tissues. Tissue stem and progenitor cells are responsible for self-renewal and repair during homeostasis and following injury. Upon wounding, epithelial tissues undergo different phases of haemostasis, inflammation, proliferation and remodelling, often resulting in fibrosis and scarring. In this review, we explore the phenotypic differences between the skin, the oesophagus and the oral mucosa. We discuss the plasticity of these epithelial stem cells and contribution of different fibroblast subpopulations for tissue regeneration and wound healing. While these epithelial tissues share global mechanisms of stem cell behaviour for tissue renewal and regeneration, the oral mucosa is known for its outstanding healing potential with minimal scarring. We aim to provide an updated review of recent studies that combined cell therapy with bioengineering exporting the unique scarless properties of the oral mucosa to improve skin and oesophageal wound healing and to reduce fibrotic tissue formation. These advances open new avenues toward the ultimate goal of achieving scarless wound healing.

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“…[116,124,125]. Homogenizers need to provide sterilized and effective homogeni- MSCs primarily take up platelet derived mitochondria via dynamin dependent, clathrin mediated endocytosis [121], but MSCs have also been shown to donate mitochondria to neural stem cells (NSCs) through actin based intercellular structures and the mitochondrial motor protein Rho-GTPase 1 (Miro1) during cisplatin induced damage in vitro [101].…”

Section: Mitochondrial Isolationmentioning

confidence: 99%

“…Several tissues are damaged during chemotherapeutic treatment, which decreases the viability of autologous transplantation, a type of transplant that has not been shown to induce immune responses [108,141]. Many studies have overcome the use of autologous mitochondria by using other sources, such as MSCs [89,121,135], UC-MSCs, and bone marrow-mesenchymal stem cells (BM-MSCs) [50]. Like stem cell based therapy [50,79,89], mitochondria obtained from stem cells have provided a powerful treatment to repair acute organ damage due to their regenerative capacity [50].…”

Section: Mt As a Possible Therapy Against Cisplatin-induced Cardiorenal Alterationsmentioning

confidence: 99%

Mitochondrial Transplantation: Is It a Feasible Therapy to Prevent the Cardiorenal Side Effects of Cisplatin?

Amador-Martínez

Hernández-Cruz

Jiménez-Uribe

et al. 2021

Future Pharmacology

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Mitochondrial transplantation (MT) is a new experimental approach that has demonstrated positive results reverting mitochondrial alterations in cardiac and kidney dysfunction mainly mediated by oxidative stress. On the other hand, cisplatin is an effective and widely used antineoplastic drug in treating several cancers; however, cisplatin has notorious side effects in different organs, such as the heart, kidneys, liver, and brain; the kidney being one of the most affected. The genitourinary system is the principal excretion pathway of cisplatin, since it is removed from the blood primarily by glomerular filtration and tubular secretion, and it may cause a sudden reduction in the renal function (acute kidney injury “AKI”), in part, by inducing mitochondrial dysfunction and the consequent oxidative stress in the tubular segment. In addition, AKI may associate with cardiac alterations, as occurs in acute cardiorenal syndrome. Due to the high prevalence of renal and cardiac side effects produced by cisplatin, here we discuss the possible use of MT as a novel therapy that could protect tissues by alleviating mitochondrial dysfunction and reducing reactive oxygen species (ROS) production.

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Platelets Facilitate the Wound-Healing Capability of Mesenchymal Stem Cells by Mitochondrial Transfer and Metabolic Reprogramming

Cited by 117 publications

References 85 publications

Mitochondrial Extracellular Vesicles – Origins and Roles

Mitochondrial Extracellular Vesicles – Origins and Roles

A Scarless Healing Tale: Comparing Homeostasis and Wound Healing of Oral Mucosa With Skin and Oesophagus

Mitochondrial Transplantation: Is It a Feasible Therapy to Prevent the Cardiorenal Side Effects of Cisplatin?

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