International journal of molecular sciences2023; 24(14); doi: 10.3390/ijms241411446

Equine Hoof Progenitor Cells Display Increased Mitochondrial Metabolism and Adaptive Potential to a Highly Pro-Inflammatory Microenvironment.

Abstract: Medicinal signaling cells (MSC) exhibit distinct molecular signatures and biological abilities, depending on the type of tissue they originate from. Recently, we isolated and described a new population of stem cells residing in the coronary corium, equine hoof progenitor cells (HPCs), which could be a new promising cell pool for the treatment of laminitis. Therefore, this study aimed to compare native populations of HPCs to well-established adipose-derived stem cells (ASCs) in standard culture conditions and in a pro-inflammatory milieu to mimic a laminitis condition. ASCs and HPCs were either cultured in standard conditions or subjected to priming with a cytokines cocktail mixture. The cells were harvested and analyzed for expression of key markers for phenotype, mitochondrial metabolism, oxidative stress, apoptosis, and immunomodulation using RT-qPCR. The morphology and migration were assessed based on fluorescent staining. Microcapillary cytometry analyses were performed to assess the distribution in the cell cycle, mitochondrial membrane potential, and oxidative stress. Native HPCs exhibited a similar morphology to ASCs, but a different phenotype. The HPCs possessed lower migration capacity and distinct distribution across cell cycle phases. Native HPCs were characterized by different mitochondrial dynamics and oxidative stress levels. Under standard culture conditions, HPCs displayed different expression patterns of apoptotic and immunomodulatory markers than ASCs, as well as distinct miRNA expression. Interestingly, after priming with the cytokines cocktail mixture, HPCs exhibited different mitochondrial dynamics than ASCs; however, the apoptosis and immunomodulatory marker expression was similar in both populations. Native ASCs and HPCs exhibited different baseline expressions of markers involved in mitochondrial dynamics, the oxidative stress response, apoptosis and inflammation. When exposed to a pro-inflammatory microenvironment, ASCs and HPCs differed in the expression of mitochondrial condition markers and chosen miRNAs.
Publication Date: 2023-07-14 PubMed ID: 37511204PubMed Central: PMC10379971DOI: 10.3390/ijms241411446Google Scholar: Lookup
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  • Journal Article

Summary

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The research article investigated the properties and potential therapeutic uses of stem cells found in the hooves of horses, known as hoof progenitor cells (HPCs). The study compared these cells with those derived from fat tissue and evaluated how they responded to inflammatory conditions that mirror laminitis, a painful disease in the hooves of horses.

Objective and Methodology

  • Researchers aimed to compare the biological characteristics and responses of HPCs and adipose-derived stem cells (ASCs) under standard conditions and in an environment simulating laminitis inflammation.
  • Following isolation, these cells were cultivated in standard conditions as well as inflammatory conditions using a mixture of cytokines, chemicals that coordinate cellular responses to inflammation and infection.
  • Cells were then examined for expression of specific markers to ascertain their phenotype, mitochondrial metabolism, oxidative stress, cell death (apoptosis), and immune modulation. Techniques like RT-qPCR, fluorescent staining, and microcapillary cytometry were used to analyze the cells.

Findings

  • HPCs showed similar morphology but different phenotype compared to ASCs. Histological differences included lower migration capacity and variations in cell cycle distributions for HPCs.
  • Researchers also observed that HPCs had unique mitochondrial dynamics and levels of oxidative stress.
  • Under standard conditions, HPCs exhibited different expression patterns of apoptotic and immunomodulatory markers than ASCs, as well as distinct miRNA expressions.
  • Inflammatory conditions led to changes in HPCs indicative of different mitochondrial responses compared to ASCs. Nevertheless, the expression levels of death and immune markers under these conditions were similar in both populations.

Conclusion

  • The study discovered that HPCs have unique cellular and molecular features when compared to ASCs. Their responses to inflammation were also unique, suggesting different susceptibilities and responses to laminitis.
  • The findings raise the possibility of using HPCs as a new source of stem cells for treating laminitis, meriting further investigation.

Cite This Article

APA
Pielok A, Kępska M, Steczkiewicz Z, Grobosz S, Bourebaba L, Marycz K. (2023). Equine Hoof Progenitor Cells Display Increased Mitochondrial Metabolism and Adaptive Potential to a Highly Pro-Inflammatory Microenvironment. Int J Mol Sci, 24(14). https://doi.org/10.3390/ijms241411446

Publication

ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 24
Issue: 14

Researcher Affiliations

Pielok, Ariadna
  • Department of Experimental Biology, Faculty of Biology and Animal Science, Wroclaw University of Environmental and Life Sciences, Norwida 27B, 50-375 Wroclaw, Poland.
Kępska, Martyna
  • Department of Experimental Biology, Faculty of Biology and Animal Science, Wroclaw University of Environmental and Life Sciences, Norwida 27B, 50-375 Wroclaw, Poland.
Steczkiewicz, Zofia
  • Department of Experimental Biology, Faculty of Biology and Animal Science, Wroclaw University of Environmental and Life Sciences, Norwida 27B, 50-375 Wroclaw, Poland.
Grobosz, Sylwia
  • Department of Experimental Biology, Faculty of Biology and Animal Science, Wroclaw University of Environmental and Life Sciences, Norwida 27B, 50-375 Wroclaw, Poland.
Bourebaba, Lynda
  • Department of Experimental Biology, Faculty of Biology and Animal Science, Wroclaw University of Environmental and Life Sciences, Norwida 27B, 50-375 Wroclaw, Poland.
Marycz, Krzysztof
  • Department of Experimental Biology, Faculty of Biology and Animal Science, Wroclaw University of Environmental and Life Sciences, Norwida 27B, 50-375 Wroclaw, Poland.
  • International Institute of Translational Medicine, Jesionowa 11, Malin, 55-114 Wisznia Mała, Poland.

MeSH Terms

  • Animals
  • Horses
  • Adipose Tissue / metabolism
  • Mesenchymal Stem Cells / metabolism
  • Hoof and Claw
  • Stem Cells / metabolism
  • Cytokines / metabolism

Grant Funding

  • the Leading Research Groups support project from the subsidy increased for the period 2020-2025 in the amount of 2 % of the subsidy referred to Art. 387 (3) of the Law of 20 July 2018 on Higher Education and Science, obtained in 2019". / Wroclaw University of Environmental and Life Sciences

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 104 references
  1. Voga M, Adamic N, Vengust M, Majdic G. Stem Cells in Veterinary Medicine-Current State and Treatment Options.. Front Vet Sci 2020;7:278.
    doi: 10.3389/fvets.2020.00278pmc: PMC7326035pubmed: 32656249google scholar: lookup
  2. Hoang DM, Pham PT, Bach TQ, Ngo ATL, Nguyen QT, Phan TTK, Nguyen GH, Le PTT, Hoang VT, Forsyth NR, Heke M, Nguyen LT. Stem cell-based therapy for human diseases.. Signal Transduct Target Ther 2022 Aug 6;7(1):272.
    doi: 10.1038/s41392-022-01134-4pmc: PMC9357075pubmed: 35933430google scholar: lookup
  3. Feisst V, Meidinger S, Locke MB. From bench to bedside: use of human adipose-derived stem cells.. Stem Cells Cloning 2015;8:149-62.
    doi: 10.2147/SCCAA.S64373pmc: PMC4636091pubmed: 26586955google scholar: lookup
  4. Guan YT, Xie Y, Li DS, Zhu YY, Zhang XL, Feng YL, Chen YP, Xu LJ, Liao PF, Wang G. Comparison of biological characteristics of mesenchymal stem cells derived from the human umbilical cord and decidua parietalis.. Mol Med Rep 2019 Jul;20(1):633-639.
    doi: 10.3892/mmr.2019.10286pmc: PMC6579987pubmed: 31180542google scholar: lookup
  5. Fan XL, Zhang Y, Li X, Fu QL. Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy.. Cell Mol Life Sci 2020 Jul;77(14):2771-2794.
    doi: 10.1007/s00018-020-03454-6pmc: PMC7223321pubmed: 31965214google scholar: lookup
  6. Marzano M, Fosso B, Piancone E, Defazio G, Pesole G, De Robertis M. Stem Cell Impairment at the Host-Microbiota Interface in Colorectal Cancer.. Cancers (Basel) 2021 Feb 27;13(5).
    doi: 10.3390/cancers13050996pmc: PMC7957811pubmed: 33673612google scholar: lookup
  7. Chatre L, Verdonk F, Rocheteau P, Crochemore C, Chru00e9tien F, Ricchetti M. A novel paradigm links mitochondrial dysfunction with muscle stem cell impairment in sepsis.. Biochim Biophys Acta Mol Basis Dis 2017 Oct;1863(10 Pt B):2546-2553.
    doi: 10.1016/j.bbadis.2017.04.019pubmed: 28456665google scholar: lookup
  8. Cipriani P, Guiducci S, Miniati I, Cinelli M, Urbani S, Marrelli A, Dolo V, Pavan A, Saccardi R, Tyndall A, Giacomelli R, Cerinic MM. Impairment of endothelial cell differentiation from bone marrow-derived mesenchymal stem cells: new insight into the pathogenesis of systemic sclerosis.. Arthritis Rheum 2007 Jun;56(6):1994-2004.
    doi: 10.1002/art.22698pubmed: 17530639google scholar: lookup
  9. Oliva-Olivera W, Cou00edn-Aragu00fcez L, Lhamyani S, Clemente-Postigo M, Torres JA, Bernal-Lu00f3pez MR, El Bekay R, Tinahones FJ. Adipogenic Impairment of Adipose Tissue-Derived Mesenchymal Stem Cells in Subjects With Metabolic Syndrome: Possible Protective Role of FGF2.. J Clin Endocrinol Metab 2017 Feb 1;102(2):478-487.
    doi: 10.1210/jc.2016-2256pubmed: 27967316google scholar: lookup
  10. Durand N, Zubair AC. Autologous versus allogeneic mesenchymal stem cell therapy: Theu00a0pros and cons.. Surgery 2022 May;171(5):1440-1442.
    doi: 10.1016/j.surg.2021.10.057pubmed: 34863523google scholar: lookup
  11. Marycz K, Pielok A, Kornicka-Garbowska K. Equine Hoof Stem Progenitor Cells (HPC) CD29u2009+u2009/Nestinu2009+u2009/K15u2009+u2009- a Novel Dermal/epidermal Stem Cell Population With a Potential Critical Role for Laminitis Treatment.. Stem Cell Rev Rep 2021 Aug;17(4):1478-1485.
    doi: 10.1007/s12015-021-10187-xpmc: PMC8149919pubmed: 34037924google scholar: lookup
  12. Yang Q, Pinto VMR, Duan W, Paxton EE, Dessauer JH, Ryan W, Lopez MJ. In vitro Characteristics of Heterogeneous Equine Hoof Progenitor Cell Isolates.. Front Bioeng Biotechnol 2019;7:155.
    doi: 10.3389/fbioe.2019.00155pmc: PMC6637248pubmed: 31355191google scholar: lookup
  13. Marycz K, Weiss C, u015amieszek A, Kornicka K. Evaluation of Oxidative Stress and Mitophagy during Adipogenic Differentiation of Adipose-Derived Stem Cells Isolated from Equine Metabolic Syndrome (EMS) Horses.. Stem Cells Int 2018;2018:5340756.
    doi: 10.1155/2018/5340756pmc: PMC6011082pubmed: 29977307google scholar: lookup
  14. Suagee JK, Corl BA, Geor RJ. A Potential Role for Pro-Inflammatory Cytokines in the Development of Insulin Resistance in Horses.. Animals (Basel) 2012 May 2;2(2):243-60.
    doi: 10.3390/ani2020243pmc: PMC4494330pubmed: 26486919google scholar: lookup
  15. Katz LM, Bailey SR. A review of recent advances and current hypotheses on the pathogenesis of acute laminitis.. Equine Vet J 2012 Nov;44(6):752-61.
  16. Engiles JB, Galantino-Homer HL, Boston R, McDonald D, Dishowitz M, Hankenson KD. Osteopathology in the Equine Distal Phalanx Associated With the Development and Progression of Laminitis.. Vet Pathol 2015 Sep;52(5):928-44.
    doi: 10.1177/0300985815588604pubmed: 26063172google scholar: lookup
  17. Mularczyk M, Bourebaba N, Marycz K, Bourebaba L. Astaxanthin Carotenoid Modulates Oxidative Stress in Adipose-Derived Stromal Cells Isolated from Equine Metabolic Syndrome Affected Horses by Targeting Mitochondrial Biogenesis.. Biomolecules 2022 Jul 27;12(8).
    doi: 10.3390/biom12081039pmc: PMC9405637pubmed: 36008933google scholar: lookup
  18. Suszynska M, Poniewierska-Baran A, Gunjal P, Ratajczak J, Marycz K, Kakar SS, Kucia M, Ratajczak MZ. Expression of the erythropoietin receptor by germline-derived cells - further support for a potential developmental link between the germline and hematopoiesis.. J Ovarian Res 2014;7:66.
    doi: 10.1186/1757-2215-7-66pmc: PMC4074848pubmed: 24982693google scholar: lookup
  19. Loftus JP, Johnson PJ, Belknap JK, Pettigrew A, Black SJ. Leukocyte-derived and endogenous matrix metalloproteinases in the lamellae of horses with naturally acquired and experimentally induced laminitis.. Vet Immunol Immunopathol 2009 Jun 15;129(3-4):221-30.
    doi: 10.1016/j.vetimm.2008.11.003pubmed: 19101039google scholar: lookup
  20. Belknap J.K., Faleiros R., Black S.J., Johnson P.J., Eades S. The Laminar Leukocyte: From Sepsis to Endocrinopathic Models of Laminitis. J. Equine Vet. Sci. 2011;10:584u2013585. doi: 10.1016/j.jevs.2011.09.034.
  21. Angelone M, Conti V, Biacca C, Battaglia B, Pecorari L, Piana F, Gnudi G, Leonardi F, Ramoni R, Basini G, Dotti S, Renzi S, Ferrari M, Grolli S. The Contribution of Adipose Tissue-Derived Mesenchymal Stem Cells and Platelet-Rich Plasma to the Treatment of Chronic Equine Laminitis: A Proof of Concept.. Int J Mol Sci 2017 Oct 11;18(10).
    doi: 10.3390/ijms18102122pmc: PMC5666804pubmed: 29019941google scholar: lookup
  22. Metcalfe SM. Mesenchymal stem cells and management of COVID-19 pneumonia.. Med Drug Discov 2020 Mar;5:100019.
  23. Cofano F, Boido M, Monticelli M, Zenga F, Ducati A, Vercelli A, Garbossa D. Mesenchymal Stem Cells for Spinal Cord Injury: Current Options, Limitations, and Future of Cell Therapy.. Int J Mol Sci 2019 May 31;20(11).
    doi: 10.3390/ijms20112698pmc: PMC6600381pubmed: 31159345google scholar: lookup
  24. Zhang K, Jiang Y, Wang B, Li T, Shang D, Zhang X. Mesenchymal Stem Cell Therapy: A Potential Treatment Targeting Pathological Manifestations of Traumatic Brain Injury.. Oxid Med Cell Longev 2022;2022:4645021.
    doi: 10.1155/2022/4645021pmc: PMC9217616pubmed: 35757508google scholar: lookup
  25. Nasiri N, Hosseini S, Reihani-Sabet F, Baghaban Eslaminejad M. Targeted mesenchymal stem cell therapy equipped with a cell-tissue nanomatchmaker attenuates osteoarthritis progression.. Sci Rep 2022 Mar 7;12(1):4015.
    doi: 10.1038/s41598-022-07969-9pmc: PMC8901617pubmed: 35256711google scholar: lookup
  26. Boland L, Bitterlich LM, Hogan AE, Ankrum JA, English K. Translating MSC Therapy in the Age of Obesity.. Front Immunol 2022;13:943333.
    doi: 10.3389/fimmu.2022.943333pmc: PMC9289617pubmed: 35860241google scholar: lookup
  27. Belknap J.K., Geor R.J., editors. Equine Laminitis. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2016.
  28. Yang Q, Lopez MJ. The Equine Hoof: Laminitis, Progenitor (Stem) Cells, and Therapy Development.. Toxicol Pathol 2021 Oct;49(7):1294-1307.
    doi: 10.1177/0192623319880469pubmed: 31741428google scholar: lookup
  29. Freitas NPP, Silva BDP, Bezerra MRL, Pescini LYG, Olinda RG, Salgueiro CCM, Nunes JF, Martins JAM, Neto SG, Martins LT. Freeze-dried Platelet-rich Plasma and Stem Cell-conditioned Medium for Therapeutic Use in Horses.. J Equine Vet Sci 2023 Feb;121:104189.
    doi: 10.1016/j.jevs.2022.104189pubmed: 36464033google scholar: lookup
  30. Golonka P, Kornicka-Garbowska K, Marycz K. SIRT1(+) Adipose Derived Mesenchymal Stromal Stem Cells (ASCs) Suspended in Alginate Hydrogel for the Treatment of Subchondral Bone Cyst in Medial Femoral Condyle in the Horse. Clinical Report.. Stem Cell Rev Rep 2020 Dec;16(6):1328-1334.
    doi: 10.1007/s12015-020-10025-6pmc: PMC7667135pubmed: 32803696google scholar: lookup
  31. Yang Q. Equine Hoof Stratum Internum K14+CD105+ Progenitor Cells: Equine Hoof Stratum Internum K14+CD105+ Progenitor Cells: Culture, Characterization, and Model of Epithelial to Mesenchymal Culture, Characterization, and Model of Epithelial to Mesenchymal Transition Transition. Louisiana State University; Baton Rouge, LA, USA: 2019.
  32. Musina RA, Bekchanova ES, Sukhikh GT. Comparison of mesenchymal stem cells obtained from different human tissues.. Bull Exp Biol Med 2005 Apr;139(4):504-9.
    doi: 10.1007/s10517-005-0331-1pubmed: 16027890google scholar: lookup
  33. Roy H, Bhardwaj S, Ylu00e4-Herttuala S. Biology of vascular endothelial growth factors.. FEBS Lett 2006 May 22;580(12):2879-87.
    doi: 10.1016/j.febslet.2006.03.087pubmed: 16631753google scholar: lookup
  34. Elias I, Franckhauser S, Bosch F. New insights into adipose tissue VEGF-A actions in the control of obesity and insulin resistance.. Adipocyte 2013 Apr 1;2(2):109-12.
    doi: 10.4161/adip.22880pmc: PMC3661112pubmed: 23805408google scholar: lookup
  35. Hirschberg RM, Plendl J. Pododermal angiogenesis and angioadaptation in the bovine claw.. Microsc Res Tech 2005 Feb;66(2-3):145-55.
    doi: 10.1002/jemt.20154pubmed: 15880503google scholar: lookup
  36. Loftus JP, Black SJ, Pettigrew A, Abrahamsen EJ, Belknap JK. Early laminar events involving endothelial activation in horses with black walnut- induced laminitis.. Am J Vet Res 2007 Nov;68(11):1205-11.
    doi: 10.2460/ajvr.68.11.1205pubmed: 17975975google scholar: lookup
  37. Lv B, Li F, Fang J, Xu L, Sun C, Han J, Hua T, Zhang Z, Feng Z, Jiang X. Hypoxia inducible factor 1u03b1 promotes survival of mesenchymal stem cells under hypoxia.. Am J Transl Res 2017;9(3):1521-1529.
    pmc: PMC5376042pubmed: 28386377
  38. Xie L, Zeng X, Hu J, Chen Q. Characterization of Nestin, a Selective Marker for Bone Marrow Derived Mesenchymal Stem Cells.. Stem Cells Int 2015;2015:762098.
    doi: 10.1155/2015/762098pmc: PMC4506912pubmed: 26236348google scholar: lookup
  39. Wislet-Gendebien S, Wautier F, Leprince P, Rogister B. Astrocytic and neuronal fate of mesenchymal stem cells expressing nestin.. Brain Res Bull 2005 Dec 15;68(1-2):95-102.
  40. Jones E, Viu00f1uela-Fernandez I, Eager RA, Delaney A, Anderson H, Patel A, Robertson DC, Allchorne A, Sirinathsinghji EC, Milne EM, MacIntyre N, Shaw DJ, Waran NK, Mayhew J, Fleetwood-Walker SM. Neuropathic changes in equine laminitis pain.. Pain 2007 Dec 5;132(3):321-331.
    doi: 10.1016/j.pain.2007.08.035pubmed: 17935886google scholar: lookup
  41. Maleki M, Ghanbarvand F, Reza Behvarz M, Ejtemaei M, Ghadirkhomi E. Comparison of mesenchymal stem cell markers in multiple human adult stem cells.. Int J Stem Cells 2014 Nov;7(2):118-26.
    doi: 10.15283/ijsc.2014.7.2.118pmc: PMC4249894pubmed: 25473449google scholar: lookup
  42. Ries C, Egea V, Karow M, Kolb H, Jochum M, Neth P. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines.. Blood 2007 May 1;109(9):4055-63.
    doi: 10.1182/blood-2006-10-051060pubmed: 17197427google scholar: lookup
  43. Quintero-Fabiu00e1n S, Arreola R, Becerril-Villanueva E, Torres-Romero JC, Arana-Argu00e1ez V, Lara-Riegos J, Ramu00edrez-Camacho MA, Alvarez-Su00e1nchez ME. Role of Matrix Metalloproteinases in Angiogenesis and Cancer.. Front Oncol 2019;9:1370.
    doi: 10.3389/fonc.2019.01370pmc: PMC6915110pubmed: 31921634google scholar: lookup
  44. Kyaw-Tanner M, Pollitt CC. Equine laminitis: increased transcription of matrix metalloproteinase-2 (MMP-2) occurs during the developmental phase.. Equine Vet J 2004 Apr;36(3):221-5.
    pubmed: 15147128doi: 10.2746/0425164044877242google scholar: lookup
  45. Fu X, Halim A, Tian B, Luo Q, Song G. MT1-MMP downregulation via the PI3K/Akt signaling pathway is required for the mechanical stretching-inhibited invasion of bone-marrow-derived mesenchymal stem cells.. J Cell Physiol 2019 Aug;234(8):14133-14144.
    doi: 10.1002/jcp.28105pubmed: 30659604google scholar: lookup
  46. Song YH, Shon SH, Shan M, Stroock AD, Fischbach C. Adipose-derived stem cells increase angiogenesis through matrix metalloproteinase-dependent collagen remodeling.. Integr Biol (Camb) 2016 Feb;8(2):205-15.
    doi: 10.1039/C5IB00277Jpmc: PMC4755818pubmed: 26758423google scholar: lookup
  47. Hsu YC, Wu YT, Yu TH, Wei YH. Mitochondria in mesenchymal stem cell biology and cell therapy: From cellular differentiation to mitochondrial transfer.. Semin Cell Dev Biol 2016 Apr;52:119-31.
    doi: 10.1016/j.semcdb.2016.02.011pubmed: 26868759google scholar: lookup
  48. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T, Kurth MJ, Shaw JT, Hinshaw JE, Green DR, Nunnari J. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization.. Dev Cell 2008 Feb;14(2):193-204.
  49. Tanaka A, Youle RJ. A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis.. Mol Cell 2008 Feb 29;29(4):409-10.
    doi: 10.1016/j.molcel.2008.02.005pubmed: 18313377google scholar: lookup
  50. Zhong Q, Kowluru RA. Diabetic retinopathy and damage to mitochondrial structure and transport machinery.. Invest Ophthalmol Vis Sci 2011 Nov 7;52(12):8739-46.
    doi: 10.1167/iovs.11-8045pmc: PMC3263781pubmed: 22003103google scholar: lookup
  51. Li M, Wang L, Wang Y, Zhang S, Zhou G, Lieshout R, Ma B, Liu J, Qu C, Verstegen MMA, Sprengers D, Kwekkeboom J, van der Laan LJW, Cao W, Peppelenbosch MP, Pan Q. Mitochondrial Fusion Via OPA1 and MFN1 Supports Liver Tumor Cell Metabolism and Growth.. Cells 2020 Jan 4;9(1).
    doi: 10.3390/cells9010121pmc: PMC7017104pubmed: 31947947google scholar: lookup
  52. Eiyama A, Okamoto K. PINK1/Parkin-mediated mitophagy in mammalian cells.. Curr Opin Cell Biol 2015 Apr;33:95-101.
    doi: 10.1016/j.ceb.2015.01.002pubmed: 25697963google scholar: lookup
  53. Safiulina D, Kuum M, Choubey V, Hickey MA, Kaasik A. Mitochondrial transport proteins RHOT1 and RHOT2 serve as docking sites for PRKN-mediated mitophagy.. Autophagy 2019 May;15(5):930-931.
  54. Alicka M, Major P, Wysocki M, Marycz K. Adipose-Derived Mesenchymal Stem Cells Isolated from Patients with Type 2 Diabetes Show Reduced "Stemness" through an Altered Secretome Profile, Impaired Anti-Oxidative Protection, and Mitochondrial Dynamics Deterioration.. J Clin Med 2019 May 30;8(6).
    doi: 10.3390/JCM8060765pmc: PMC6617220pubmed: 31151180google scholar: lookup
  55. Alicka M, Kornicka-Garbowska K, Kucharczyk K, Ku0119pska M, Ru04e7cken M, Marycz K. Age-dependent impairment of adipose-derived stem cells isolated from horses.. Stem Cell Res Ther 2020 Jan 3;11(1):4.
    doi: 10.1186/s13287-019-1512-6pmc: PMC6942290pubmed: 31900232google scholar: lookup
  56. Di Nottia M, Marchese M, Verrigni D, Mutti CD, Torraco A, Oliva R, Fernandez-Vizarra E, Morani F, Trani G, Rizza T, Ghezzi D, Ardissone A, Nesti C, Vasco G, Zeviani M, Minczuk M, Bertini E, Santorelli FM, Carrozzo R. A homozygous MRPL24 mutation causes a complex movement disorder and affects the mitoribosome assembly.. Neurobiol Dis 2020 Jul;141:104880.
    doi: 10.1016/j.nbd.2020.104880pubmed: 32344152google scholar: lookup
  57. Bourebaba N, Kornicka-Garbowska K, Marycz K, Bourebaba L, Kowalczuk A. Laurus nobilis ethanolic extract attenuates hyperglycemia and hyperinsulinemia-induced insulin resistance in HepG2 cell line through the reduction of oxidative stress and improvement of mitochondrial biogenesis - Possible implication in pharmacotherapy.. Mitochondrion 2021 Jul;59:190-213.
    doi: 10.1016/j.mito.2021.06.003pubmed: 34091077google scholar: lookup
  58. Yu P, Zhang J, Yu S, Luo Z, Hua F, Yuan L, Zhou Z, Liu Q, Du X, Chen S, Zhang L, Xu G. Protective Effect of Sevoflurane Postconditioning against Cardiac Ischemia/Reperfusion Injury via Ameliorating Mitochondrial Impairment, Oxidative Stress and Rescuing Autophagic Clearance.. PLoS One 2015;10(8):e0134666.
  59. Ragni E, Perucca Orfei C, De Luca P, Mondadori C, Viganu00f2 M, Colombini A, de Girolamo L. Inflammatory priming enhances mesenchymal stromal cell secretome potential as a clinical product for regenerative medicine approaches through secreted factors and EV-miRNAs: the example of joint disease.. Stem Cell Res Ther 2020 Apr 28;11(1):165.
    doi: 10.1186/s13287-020-01677-9pmc: PMC7189600pubmed: 32345351google scholar: lookup
  60. Wang Q, Yang Q, Wang Z, Tong H, Ma L, Zhang Y, Shan F, Meng Y, Yuan Z. Comparative analysis of human mesenchymal stem cells from fetal-bone marrow, adipose tissue, and Warton's jelly as sources of cell immunomodulatory therapy.. Hum Vaccin Immunother 2016;12(1):85-96.
  61. Sivanathan KN, Rojas-Canales D, Grey ST, Gronthos S, Coates PT. Transcriptome Profiling of IL-17A Preactivated Mesenchymal Stem Cells: A Comparative Study to Unmodified and IFN-u03b3 Modified Mesenchymal Stem Cells.. Stem Cells Int 2017;2017:1025820.
    doi: 10.1155/2017/1025820pmc: PMC5331321pubmed: 28293262google scholar: lookup
  62. Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially.. PLoS One 2010 Feb 2;5(2):e9016.
  63. Miceli V, Bulati M, Iannolo G, Zito G, Gallo A, Conaldi PG. Therapeutic Properties of Mesenchymal Stromal/Stem Cells: The Need of Cell Priming for Cell-Free Therapies in Regenerative Medicine.. Int J Mol Sci 2021 Jan 14;22(2).
    doi: 10.3390/ijms22020763pmc: PMC7828743pubmed: 33466583google scholar: lookup
  64. Fan H, Zhao G, Liu L, Liu F, Gong W, Liu X, Yang L, Wang J, Hou Y. Pre-treatment with IL-1u03b2 enhances the efficacy of MSC transplantation in DSS-induced colitis.. Cell Mol Immunol 2012 Nov;9(6):473-81.
    doi: 10.1038/cmi.2012.40pmc: PMC4002219pubmed: 23085948google scholar: lookup
  65. Yang A, Lu Y, Xing J, Li Z, Yin X, Dou C, Dong S, Luo F, Xie Z, Hou T, Xu J. IL-8 Enhances Therapeutic Effects of BMSCs on Bone Regeneration via CXCR2-Mediated PI3k/Akt Signaling Pathway.. Cell Physiol Biochem 2018;48(1):361-370.
    doi: 10.1159/000491742pubmed: 30016780google scholar: lookup
  66. Pricola KL, Kuhn NZ, Haleem-Smith H, Song Y, Tuan RS. Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism.. J Cell Biochem 2009 Oct 15;108(3):577-88.
    doi: 10.1002/jcb.22289pmc: PMC2774119pubmed: 19650110google scholar: lookup
  67. Loke XY, Imran SAM, Tye GJ, Wan Kamarul Zaman WS, Nordin F. Immunomodulation and Regenerative Capacity of MSCs for Long-COVID.. Int J Mol Sci 2021 Nov 17;22(22).
    doi: 10.3390/ijms222212421pmc: PMC8625432pubmed: 34830303google scholar: lookup
  68. Valle-Prieto A, Conget PA. Human mesenchymal stem cells efficiently manage oxidative stress.. Stem Cells Dev 2010 Dec;19(12):1885-93.
    doi: 10.1089/scd.2010.0093pubmed: 20380515google scholar: lookup
  69. Fukui M, Zhu BT. Mitochondrial superoxide dismutase SOD2, but not cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells.. Free Radic Biol Med 2010 Mar 15;48(6):821-30.
  70. Biswas SK. Does the Interdependence between Oxidative Stress and Inflammation Explain the Antioxidant Paradox?. Oxid Med Cell Longev 2016;2016:5698931.
    doi: 10.1155/2016/5698931pmc: PMC4736408pubmed: 26881031google scholar: lookup
  71. Laskoski LM, Dittrich RL, Valadu00e3o CA, Brum JS, Brandu00e3o Y, Brito HF, de Sousa RS. Oxidative stress in hoof laminar tissue of horses with lethal gastrointestinal diseases.. Vet Immunol Immunopathol 2016 Mar;171:66-72.
    doi: 10.1016/j.vetimm.2016.02.008pubmed: 26964719google scholar: lookup
  72. Chen KC, Chen CR, Chen CY, Peng CC, Peng RY. Bicalutamide Exhibits Potential to Damage Kidney via Destroying Complex I and Affecting Mitochondrial Dynamics.. J Clin Med 2021 Dec 27;11(1).
    doi: 10.3390/jcm11010135pmc: PMC8745250pubmed: 35011880google scholar: lookup
  73. Buhrmann C, Mobasheri A, Matis U, Shakibaei M. Curcumin mediated suppression of nuclear factor-u03baB promotes chondrogenic differentiation of mesenchymal stem cells in a high-density co-culture microenvironment.. Arthritis Res Ther 2010;12(4):R127.
    doi: 10.1186/ar3065pmc: PMC2945017pubmed: 20594343google scholar: lookup
  74. Shakibaei M, Schulze-Tanzil G, John T, Mobasheri A. Curcumin protects human chondrocytes from IL-l1beta-induced inhibition of collagen type II and beta1-integrin expression and activation of caspase-3: an immunomorphological study.. Ann Anat 2005 Nov;187(5-6):487-97.
    doi: 10.1016/J.AANAT.2005.06.007pubmed: 16320828google scholar: lookup
  75. Chang J, Liu F, Lee M, Wu B, Ting K, Zara JN, Soo C, Al Hezaimi K, Zou W, Chen X, Mooney DJ, Wang CY. NF-u03baB inhibits osteogenic differentiation of mesenchymal stem cells by promoting u03b2-catenin degradation.. Proc Natl Acad Sci U S A 2013 Jun 4;110(23):9469-74.
    doi: 10.1073/PNAS.1300532110pmc: PMC3677422pubmed: 23690607google scholar: lookup
  76. Collino F, Bruno S, Deregibus MC, Tetta C, Camussi G. MicroRNAs and mesenchymal stem cells.. Vitam Horm 2011;87:291-320.
  77. Mei Y, Bian C, Li J, Du Z, Zhou H, Yang Z, Zhao RC. miR-21 modulates the ERK-MAPK signaling pathway by regulating SPRY2 expression during human mesenchymal stem cell differentiation.. J Cell Biochem 2013 Jun;114(6):1374-84.
    doi: 10.1002/jcb.24479pubmed: 23239100google scholar: lookup
  78. Trohatou O, Zagoura D, Bitsika V, Pappa KI, Antsaklis A, Anagnou NP, Roubelakis MG. Sox2 suppression by miR-21 governs human mesenchymal stem cell properties.. Stem Cells Transl Med 2014 Jan;3(1):54-68.
    doi: 10.5966/sctm.2013-0081pmc: PMC3902287pubmed: 24307698google scholar: lookup
  79. Laine SK, Alm JJ, Virtanen SP, Aro HT, Laitala-Leinonen TK. MicroRNAs miR-96, miR-124, and miR-199a regulate gene expression in human bone marrow-derived mesenchymal stem cells.. J Cell Biochem 2012 Aug;113(8):2687-95.
    doi: 10.1002/jcb.24144pubmed: 22441842google scholar: lookup
  80. Huang K, Fu J, Zhou W, Li W, Dong S, Yu S, Hu Z, Wang H, Xie Z. MicroRNA-125b regulates osteogenic differentiation of mesenchymal stem cells by targeting Cbfu03b2 in vitro.. Biochimie 2014 Jul;102:47-55.
    doi: 10.1016/j.biochi.2014.02.005pubmed: 24560795google scholar: lookup
  81. Clark EA, Kalomoiris S, Nolta JA, Fierro FA. Concise review: MicroRNA function in multipotent mesenchymal stromal cells.. Stem Cells 2014 May;32(5):1074-82.
    doi: 10.1002/stem.1623pubmed: 24860868google scholar: lookup
  82. Baglio SR, Rooijers K, Koppers-Lalic D, Verweij FJ, Pu00e9rez Lanzu00f3n M, Zini N, Naaijkens B, Perut F, Niessen HW, Baldini N, Pegtel DM. Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species.. Stem Cell Res Ther 2015 Jul 1;6(1):127.
    doi: 10.1186/S13287-015-0116-Zpmc: PMC4529699pubmed: 26129847google scholar: lookup
  83. Wu Y, Zhang Z, Li J, Zhong H, Yuan R, Deng Z, Wu X. Mechanism of Adipose-Derived Mesenchymal Stem Cell-Derived Extracellular Vesicles Carrying miR-21-5p in Hyperoxia-Induced Lung Injury.. Stem Cell Rev Rep 2022 Mar;18(3):1007-1024.
    doi: 10.1007/s12015-021-10311-xpubmed: 34882302google scholar: lookup
  84. Wu T, Liu Y, Fan Z, Xu J, Jin L, Gao Z, Wu Z, Hu L, Wang J, Zhang C, Chen W, Wang S. miR-21 Modulates the Immunoregulatory Function of Bone Marrow Mesenchymal Stem Cells Through the PTEN/Akt/TGF-u03b21 Pathway.. Stem Cells 2015 Nov;33(11):3281-90.
    doi: 10.1002/stem.2081pubmed: 26086742google scholar: lookup
  85. Sun Y, Xu L, Huang S, Hou Y, Liu Y, Chan KM, Pan XH, Li G. mir-21 overexpressing mesenchymal stem cells accelerate fracture healing in a rat closed femur fracture model.. Biomed Res Int 2015;2015:412327.
    doi: 10.1155/2015/412327pmc: PMC4386680pubmed: 25879024google scholar: lookup
  86. Wang J, Huang R, Xu Q, Zheng G, Qiu G, Ge M, Shu Q, Xu J. Mesenchymal Stem Cell-Derived Extracellular Vesicles Alleviate Acute Lung Injury Via Transfer of miR-27a-3p.. Crit Care Med 2020 Jul;48(7):e599-e610.
    doi: 10.1097/CCM.0000000000004315pubmed: 32317602google scholar: lookup
  87. You L, Pan L, Chen L, Gu W, Chen J. MiR-27a is Essential for the Shift from Osteogenic Differentiation to Adipogenic Differentiation of Mesenchymal Stem Cells in Postmenopausal Osteoporosis.. Cell Physiol Biochem 2016;39(1):253-65.
    doi: 10.1159/000445621pubmed: 27337099google scholar: lookup
  88. Ye J, Gimble JM. Regulation of stem cell differentiation in adipose tissue by chronic inflammation.. Clin Exp Pharmacol Physiol 2011 Dec;38(12):872-8.
  89. Jung YD, Park SK, Kang D, Hwang S, Kang MH, Hong SW, Moon JH, Shin JS, Jin DH, You D, Lee JY, Park YY, Hwang JJ, Kim CS, Suh N. Epigenetic regulation of miR-29a/miR-30c/DNMT3A axis controls SOD2 and mitochondrial oxidative stress in human mesenchymal stem cells.. Redox Biol 2020 Oct;37:101716.
    doi: 10.1016/j.redox.2020.101716pmc: PMC7509080pubmed: 32961441google scholar: lookup
  90. Huang Y, Zhu N, Chen T, Chen W, Kong J, Zheng W, Ruan J. Triptolide Suppressed the Microglia Activation to Improve Spinal Cord Injury Through miR-96/IKKu03b2/NF-u03baB Pathway.. Spine (Phila Pa 1976) 2019 Jun 15;44(12):E707-E714.
    doi: 10.1097/BRS.0000000000002989pubmed: 31150368google scholar: lookup
  91. Zhan JB, Zheng J, Zeng LY, Fu Z, Huang QJ, Wei X, Zeng M. Downregulation of miR-96-5p Inhibits mTOR/NF-u03bab Signaling Pathway via DEPTOR in Allergic Rhinitis.. Int Arch Allergy Immunol 2021;182(3):210-219.
    doi: 10.1159/000509403pubmed: 33477144google scholar: lookup
  92. Wu P, Cao Y, Zhao R, Wang Y. miR-96-5p regulates wound healing by targeting BNIP3/FAK pathway.. J Cell Biochem 2019 Aug;120(8):12904-12911.
    doi: 10.1002/jcb.28561pubmed: 30883918google scholar: lookup
  93. Uwiera R.R.E., Egyedy A.F., Ametaj B.N. Periparturient Diseases of Dairy Cows. Springer; Cham, Switzerland: 2017. Laminitis: A Multisystems Veterinary Perspective with Omics Technologies; pp. 185u2013200.
  94. Mobasheri A, Critchlow K, Clegg PD, Carter SD, Canessa CM. Chronic equine laminitis is characterised by loss of GLUT1, GLUT4 and ENaC positive laminar keratinocytes.. Equine Vet J 2004 Apr;36(3):248-54.
    doi: 10.2746/0425164044877224pubmed: 15147133google scholar: lookup
  95. Zhang L, Stokes N, Polak L, Fuchs E. Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment.. Cell Stem Cell 2011 Mar 4;8(3):294-308.
    doi: 10.1016/j.stem.2011.01.014pmc: PMC3086714pubmed: 21362569google scholar: lookup
  96. Boissart C, Nissan X, Giraud-Triboult K, Peschanski M, Benchoua A. miR-125 potentiates early neural specification of human embryonic stem cells.. Development 2012 Apr;139(7):1247-57.
    doi: 10.1242/dev.073627pubmed: 22357933google scholar: lookup
  97. Takeda YS, Xu Q. Neuronal Differentiation of Human Mesenchymal Stem Cells Using Exosomes Derived from Differentiating Neuronal Cells.. PLoS One 2015;10(8):e0135111.
  98. Shi L, Feng L, Liu Y, Duan JQ, Lin WP, Zhang JF, Li G. MicroRNA-218 Promotes Osteogenic Differentiation of Mesenchymal Stem Cells and Accelerates Bone Fracture Healing.. Calcif Tissue Int 2018 Aug;103(2):227-236.
    doi: 10.1007/s00223-018-0410-8pubmed: 29523928google scholar: lookup
  99. Chen S, Xu Z, Shao J, Fu P, Wu H. MicroRNA-218 promotes early chondrogenesis of mesenchymal stem cells and inhibits later chondrocyte maturation.. BMC Biotechnol 2019 Jan 15;19(1):6.
    doi: 10.1186/s12896-018-0496-0pmc: PMC6334453pubmed: 30646874google scholar: lookup
  100. Sun Y, Peng R, Peng H, Liu H, Wen L, Wu T, Yi H, Li A, Zhang Z. miR-451 suppresses the NF-kappaB-mediated proinflammatory molecules expression through inhibiting LMP7 in diabetic nephropathy.. Mol Cell Endocrinol 2016 Sep 15;433:75-86.
    doi: 10.1016/j.mce.2016.06.004pubmed: 27264074google scholar: lookup
  101. Sun X, Zhang H. miR-451 elevation relieves inflammatory pain by suppressing microglial activation-evoked inflammatory response via targeting TLR4.. Cell Tissue Res 2018 Dec;374(3):487-495.
    doi: 10.1007/s00441-018-2898-7pubmed: 30069596google scholar: lookup
  102. Maru0119dziak M, Marycz K, Tomaszewski KA, Kornicka K, Henry BM. The Influence of Aging on the Regenerative Potential of Human Adipose Derived Mesenchymal Stem Cells.. Stem Cells Int 2016;2016:2152435.
    doi: 10.1155/2016/2152435pmc: PMC4749808pubmed: 26941800google scholar: lookup
  103. Smieszek A, Marcinkowska K, Pielok A, Sikora M, Valihrach L, Carnevale E, Marycz K. Obesity Affects the Proliferative Potential of Equine Endometrial Progenitor Cells and Modulates Their Molecular Phenotype Associated with Mitochondrial Metabolism.. Cells 2022 Apr 24;11(9).
    doi: 10.3390/cells11091437pmc: PMC9100746pubmed: 35563743google scholar: lookup
  104. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.. Anal Biochem 1987 Apr;162(1):156-9.
    doi: 10.1006/abio.1987.9999pubmed: 2440339google scholar: lookup

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