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Journal of cellular and molecular medicine2016; 20(12); 2384-2404; doi: 10.1111/jcmm.12932

Equine metabolic syndrome impairs adipose stem cells osteogenic differentiation by predominance of autophagy over selective mitophagy.

Abstract: Adipose-derived mesenchymal stem cells (ASC) hold great promise in the treatment of many disorders including musculoskeletal system, cardiovascular and/or endocrine diseases. However, the cytophysiological condition of cells, used for engraftment seems to be fundamental factor that might determine the effectiveness of clinical therapy. In this study we investigated growth kinetics, senescence, accumulation of oxidative stress factors, mitochondrial biogenesis, autophagy and osteogenic differentiation potential of ASC isolated from horses suffered from equine metabolic syndrome (EMS). We demonstrated that EMS condition impairs multipotency/pluripotency in ASCs causes accumulation of reactive oxygen species and mitochondria deterioration. We found that, cytochrome c is released from mitochondria to the cytoplasm suggesting activation of intrinsic apoptotic pathway in those cells. Moreover, we observed up-regulation of p21 and decreased ratio of Bcl-2/BAX. Deteriorations in mitochondria structure caused alternations in osteogenic differentiation of ASC resulting in their decreased proliferation rate and reduced expression of osteogenic markers BMP-2 and collagen type I. During osteogenic differentiation of ASC , we observed autophagic turnover as probably, an alternative way to generate adenosine triphosphate and amino acids required to increased protein synthesis during differentiation. Downregulation of PGC1α, PARKIN and PDK4 in differentiated ASC confirmed impairments in mitochondrial biogenesis and function. Hence, application of ASC into endocrinological or ortophedical practice requires further investigation and analysis in the context of safeness of their application.
© 2016 The Authors. Journal of Cellular and Molecular Medicine published by John Wiley & Sons Ltd and Foundation for Cellular and Molecular Medicine.
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Publication Date: 2016-09-14 PubMed ID: 27629697PubMed Central: PMC5134411DOI: 10.1111/jcmm.12932Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research evaluates the impact of Equine Metabolic Syndrome (EMS) on adipose-derived mesenchymal stem cells (ASC) in horses. The study found that EMS impairs the pluripotency of ASCs leading to the deterioration of mitochondria, reactive oxygen species accumulation, and disruption of the osteogenic differentiation process.

Stem Cell Potential and Equine Metabolic Syndrome

  • The research focused on adipose-derived mesenchymal stem cells (ASCs), which show potential in treating a range of disorders, including those related to musculoskeletal, cardiovascular, and endocrine systems. The state of the cells utilized for engraftment could determine the effectiveness of clinical treatments.
  • Researchers examined the growth kinetics, senescence, oxidative stress factors accumulation, mitochondrial biogenesis, osteogenic differentiation potential, and autophagy of ASCs from horses with Equine Metabolic Syndrome (EMS), a metabolic disorder in horses that is akin to metabolic syndrome in humans.
  • The findings showed that EMS hampers multipotency/pluripotency in ASCs, leading to reactive oxygen species accumulation and mitochondrial deterioration. There was also evidence of the intrinsic apoptotic pathway activation in the cells.

Implications on Osteogenic Differentiation

  • The study observed that ASCs from horses with EMS exhibited realized disruptions in osteogenic differentiation that resulted in a decreased proliferation rate and reduced the expression of osteogenic markers such as BMP-2 and collagen type I.
  • During osteogenic differentiation of ASCs, autophagic turnover was observed. This process, possibly an alternate way to generate adenosine triphosphate and amino acids needed for increased protein synthesis during differentiation, is negatively affected in cells suffering from EMS.
  • Persistent downregulation of PGC1α, PARKIN, and PDK4 in differentiated ASCs confirmed impairments in mitochondrial biogenesis and function.

Applications and Further Research

  • The results of the study suggest that the application of ASCs into endocrinological or orthopedical practice requires further research. The pathology associated with EMS can negatively influence the pluripotency of ASCs and affect their therapeutic potential.
  • The exploration of ways to counteract the negative impacts of diseases like EMS on ASCs could lead to more effective clinical therapies using stem cells.

Cite This Article

APA
Marycz K, Kornicka K, Marędziak M, Golonka P, Nicpoń J. (2016). Equine metabolic syndrome impairs adipose stem cells osteogenic differentiation by predominance of autophagy over selective mitophagy. J Cell Mol Med, 20(12), 2384-2404. https://doi.org/10.1111/jcmm.12932

Publication

Journal of cellular and molecular medicine
ISSN: 1582-4934
NlmUniqueID: 101083777
Country: England
Language: English
Volume: 20
Issue: 12
Pages: 2384-2404

Researcher Affiliations

Marycz, Krzysztof
  • Electron Microscopy Laboratory, The Faculty of Biology and Animal Science, University of Environmental and Life Sciences Wroclaw, Wroclaw, Poland.
  • Wroclaw Research Centre EIT+, Wrocław, Poland.
Kornicka, Katarzyna
  • Electron Microscopy Laboratory, The Faculty of Biology and Animal Science, University of Environmental and Life Sciences Wroclaw, Wroclaw, Poland.
  • Wroclaw Research Centre EIT+, Wrocław, Poland.
Marędziak, Monika
  • Department of Animal Physiology and Biostructure, Faculty of Veterinary Medicine, University of Environmental and Life Sciences Wroclaw, Wroclaw, Poland.
Golonka, Paweł
  • Equine Clinic Equivet, Gliwice, Poland.
Nicpoń, Jakub
  • Department of Surgery, Faculty of Veterinary Medicine, University of Environmental and Life Sciences Wroclaw, Wroclaw, Poland.

MeSH Terms

  • Adipose Tissue / pathology
  • Animals
  • Autophagy
  • Cell Differentiation
  • Cell Proliferation
  • Cell Shape
  • Cells, Cultured
  • Female
  • Flow Cytometry
  • Horses
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Immunophenotyping
  • Kinetics
  • Male
  • Metabolic Syndrome / metabolism
  • Methylation
  • Mitochondria / metabolism
  • Mitochondrial Dynamics
  • Mitophagy
  • Multipotent Stem Cells / cytology
  • Osteoblasts / metabolism
  • Osteoblasts / pathology
  • Osteogenesis
  • Oxidative Stress
  • Reactive Oxygen Species / metabolism
  • Stem Cells / metabolism
  • Stem Cells / pathology
  • Stem Cells / ultrastructure
  • Transcription Factors / metabolism

References

This article includes 85 references
  1. Frank N. Equine metabolic syndrome. J Equine Vet Sci 2009; 29: 259–67.
  2. Grummer RR. Etiology of lipid-related metabolic disorders in periparturient dairy cows.. J Dairy Sci 1993 Dec;76(12):3882-96.
    pubmed: 8132893doi: 10.3168/jds.s0022-0302(93)77729-2google scholar: lookup
  3. Hotamisligil GS. Inflammation and metabolic disorders.. Nature 2006 Dec 14;444(7121):860-7.
    pubmed: 17167474doi: 10.1038/nature05485google scholar: lookup
  4. Goff JP, Horst RL. Physiological changes at parturition and their relationship to metabolic disorders.. J Dairy Sci 1997 Jul;80(7):1260-8.
    pubmed: 9241588doi: 10.3168/jds.s0022-0302(97)76055-7google scholar: lookup
  5. Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Targher G, Alberiche M, Bonadonna RC, Muggeo M. Prevalence of insulin resistance in metabolic disorders: the Bruneck Study.. Diabetes 1998 Oct;47(10):1643-9.
    pubmed: 9753305doi: 10.2337/diabetes.47.10.1643google scholar: lookup
  6. Basinska K, Marycz K, Śieszek A, Nicpoń J. The production and distribution of IL-6 and TNF-a in subcutaneous adipose tissue and their correlation with serum concentrations in Welsh ponies with equine metabolic syndrome.. J Vet Sci 2015;16(1):113-20.
    pmc: PMC4367141pubmed: 25269712doi: 10.4142/jvs.2015.16.1.113google scholar: lookup
  7. Johnson PJ, Wiedmeyer CE, LaCarrubba A, Ganjam VK, Messer NT 4th. Laminitis and the equine metabolic syndrome.. Vet Clin North Am Equine Pract 2010 Aug;26(2):239-55.
    pubmed: 20699172doi: 10.1016/j.cveq.2010.04.004google scholar: lookup
  8. Firshman AM, Valberg SJ. Factors affecting clinical assessment of insulin sensitivity in horses.. Equine Vet J 2007 Nov;39(6):567-75.
    pubmed: 18065318doi: 10.2746/042516407x238512google scholar: lookup
  9. Hashemian SJ, Kouhnavard M, Nasli-Esfahani E. Mesenchymal Stem Cells: Rising Concerns over Their Application in Treatment of Type One Diabetes Mellitus.. J Diabetes Res 2015;2015:675103.
    pmc: PMC4630398pubmed: 26576437doi: 10.1155/2015/675103google scholar: lookup
  10. Pileggi A. Mesenchymal stem cells for the treatment of diabetes.. Diabetes 2012 Jun;61(6):1355-6.
    pmc: PMC3357279pubmed: 22618774doi: 10.2337/db12-0355google scholar: lookup
  11. Durham AE, Hughes KJ, Cottle HJ, Rendle DI, Boston RC. Type 2 diabetes mellitus with pancreatic beta cell dysfunction in 3 horses confirmed with minimal model analysis.. Equine Vet J 2009 Dec;41(9):924-9.
    pubmed: 20383993doi: 10.2746/042516409x452152google scholar: lookup
  12. Robertson RP, Harmon J, Tran PO, Poitout V. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes.. Diabetes 2004 Feb;53 Suppl 1:S119-24.
    pubmed: 14749276doi: 10.2337/diabetes.53.2007.s119google scholar: lookup
  13. Kim N, Cho SG. Clinical applications of mesenchymal stem cells.. Korean J Intern Med 2013 Jul;28(4):387-402.
    pmc: PMC3712145pubmed: 23864795doi: 10.3904/kjim.2013.28.4.387google scholar: lookup
  14. Wei X, Yang X, Han ZP, Qu FF, Shao L, Shi YF. Mesenchymal stem cells: a new trend for cell therapy.. Acta Pharmacol Sin 2013 Jun;34(6):747-54.
    pmc: PMC4002895pubmed: 23736003doi: 10.1038/aps.2013.50google scholar: lookup
  15. Rahavi H, Hashemi SM, Soleimani M, Mohammadi J, Tajik N. Adipose tissue-derived mesenchymal stem cells exert in vitro immunomodulatory and beta cell protective functions in streptozotocin-induced diabetic mice model.. J Diabetes Res 2015;2015:878535.
    pmc: PMC4393922pubmed: 25893202doi: 10.1155/2015/878535google scholar: lookup
  16. Grzesiak J, Krzysztof M, Karol W, Joanna C. Isolation and morphological characterisation of ovine adipose-derived mesenchymal stem cells in culture.. Int J Stem Cells 2011 Nov;4(2):99-104.
    pmc: PMC3840966pubmed: 24298341doi: 10.15283/ijsc.2011.4.2.99google scholar: lookup
  17. Tropel P, Noël D, Platet N, Legrand P, Benabid AL, Berger F. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow.. Exp Cell Res 2004 May 1;295(2):395-406.
    pubmed: 15093739doi: 10.1016/j.yexcr.2003.12.030google scholar: lookup
  18. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells.. Nat Rev Mol Cell Biol 2011 Feb;12(2):126-31.
    pmc: PMC3346289pubmed: 21253000doi: 10.1038/nrm3049google scholar: lookup
  19. Tantrawatpan C, Manochantr S, Kheolamai P, U-Pratya Y, Supokawej A, Issaragrisil S. Pluripotent gene expression in mesenchymal stem cells from human umbilical cord Wharton's jelly and their differentiation potential to neural-like cells.. J Med Assoc Thai 2013 Sep;96(9):1208-17.
    pubmed: 24163998
  20. Gonzalez R, Maki CB, Pacchiarotti J, Csontos S, Pham JK, Slepko N, Patel A, Silva F. Pluripotent marker expression and differentiation of human second trimester Mesenchymal Stem Cells.. Biochem Biophys Res Commun 2007 Oct 19;362(2):491-7.
    pubmed: 17719004doi: 10.1016/j.bbrc.2007.08.033google scholar: lookup
  21. Kita K, Gauglitz GG, Phan TT, Herndon DN, Jeschke MG. Isolation and characterization of mesenchymal stem cells from the sub-amniotic human umbilical cord lining membrane.. Stem Cells Dev 2010 Apr;19(4):491-502.
    pubmed: 19635009doi: 10.1089/scd.2009.0192google scholar: lookup
  22. Blazquez R, Sanchez-Margallo FM, de la Rosa O, Dalemans W, Alvarez V, Tarazona R, Casado JG. Immunomodulatory Potential of Human Adipose Mesenchymal Stem Cells Derived Exosomes on in vitro Stimulated T Cells.. Front Immunol 2014;5:556.
    pmc: PMC4220146pubmed: 25414703doi: 10.3389/fimmu.2014.00556google scholar: lookup
  23. Leto Barone AA, Khalifian S, Lee WP, Brandacher G. Immunomodulatory effects of adipose-derived stem cells: fact or fiction?. Biomed Res Int 2013;2013:383685.
    pmc: PMC3782761pubmed: 24106704doi: 10.1155/2013/383685google scholar: lookup
  24. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication.. Leukemia 2006 Sep;20(9):1487-95.
    pubmed: 16791265doi: 10.1038/sj.leu.2404296google scholar: lookup
  25. Marędziak M, Marycz K, Lewandowski D, Siudzińska A, Śmieszek A. Static magnetic field enhances synthesis and secretion of membrane-derived microvesicles (MVs) rich in VEGF and BMP-2 in equine adipose-derived stromal cells (EqASCs)-a new approach in veterinary regenerative medicine.. In Vitro Cell Dev Biol Anim 2015 Mar;51(3):230-40.
    pmc: PMC4368852pubmed: 25428200doi: 10.1007/s11626-014-9828-0google scholar: lookup
  26. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, Tetta C, Camussi G. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs.. PLoS One 2010 Jul 27;5(7):e11803.
    pmc: PMC2910725pubmed: 20668554doi: 10.1371/journal.pone.0011803google scholar: lookup
  27. Ratajczak MZ. Microvesicles as immune orchestra conductors.. Blood 2008 May 15;111(10):4832-3.
    pmc: PMC2384118pubmed: 18467599doi: 10.1182/blood-2008-02-136028google scholar: lookup
  28. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery.. Leukemia 2006 May;20(5):847-56.
    pubmed: 16453000doi: 10.1038/sj.leu.2404132google scholar: lookup
  29. Li WJ, Tuli R, Huang X, Laquerriere P, Tuan RS. Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold.. Biomaterials 2005 Sep;26(25):5158-66.
    pubmed: 15792543doi: 10.1016/j.biomaterials.2005.01.002google scholar: lookup
  30. Baksh D, Yao R, Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow.. Stem Cells 2007 Jun;25(6):1384-92.
    pubmed: 17332507doi: 10.1634/stemcells.2006-0709google scholar: lookup
  31. Nicpoń J, Marycz K, Grzesiak J. Therapeutic effect of adipose-derived mesenchymal stem cell injection in horses suffering from bone spavin.. Pol J Vet Sci 2013;16(4):753-4.
    pubmed: 24597313doi: 10.2478/pjvs-2013-0107google scholar: lookup
  32. De Schauwer C, Van de Walle GR, Van Soom A, Meyer E. Mesenchymal stem cell therapy in horses: useful beyond orthopedic injuries?. Vet Q 2013 Dec;33(4):234-41.
    pubmed: 23697553doi: 10.1080/01652176.2013.800250google scholar: lookup
  33. Del Bue M, Riccò S, Ramoni R, Conti V, Gnudi G, Grolli S. Equine adipose-tissue derived mesenchymal stem cells and platelet concentrates: their association in vitro and in vivo.. Vet Res Commun 2008 Sep;32 Suppl 1:S51-5.
    pubmed: 18683070doi: 10.1007/s11259-008-9093-3google scholar: lookup
  34. Marycz K, Kornicka K, Basinska K, Czyrek A. Equine Metabolic Syndrome Affects Viability, Senescence, and Stress Factors of Equine Adipose-Derived Mesenchymal Stromal Stem Cells: New Insight into EqASCs Isolated from EMS Horses in the Context of Their Aging.. Oxid Med Cell Longev 2016;2016:4710326.
    pmc: PMC4670679pubmed: 26682006doi: 10.1155/2016/4710326google scholar: lookup
  35. Benameur L, Charif N, Li Y, Stoltz JF, de Isla N. Toward an understanding of mechanism of aging-induced oxidative stress in human mesenchymal stem cells.. Biomed Mater Eng 2015;25(1 Suppl):41-6.
    pubmed: 25538054doi: 10.3233/bme-141247google scholar: lookup
  36. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging.. Cell 2005 Feb 25;120(4):483-95.
    pubmed: 15734681doi: 10.1016/j.cell.2005.02.001google scholar: lookup
  37. Cuervo AM, Bergamini E, Brunk UT, Dröge W, Ffrench M, Terman A. Autophagy and aging: the importance of maintaining "clean" cells.. Autophagy 2005 Oct-Dec;1(3):131-40.
    pubmed: 16874025doi: 10.4161/auto.1.3.2017google scholar: lookup
  38. Yang ZJ, Chee CE, Huang S, Sinicrope FA. The role of autophagy in cancer: therapeutic implications.. Mol Cancer Ther 2011 Sep;10(9):1533-41.
    pmc: PMC3170456pubmed: 21878654doi: 10.1158/1535-7163.mct-11-0047google scholar: lookup
  39. Quan W, Lim YM, Lee MS. Role of autophagy in diabetes and endoplasmic reticulum stress of pancreatic β-cells.. Exp Mol Med 2012 Feb 29;44(2):81-8.
    pmc: PMC3296816pubmed: 22257883doi: 10.3858/emm.2012.44.2.030google scholar: lookup
  40. Zhao K, Hao H, Liu J, Tong C, Cheng Y, Xie Z, Zang L, Mu Y, Han W. Bone marrow-derived mesenchymal stem cells ameliorate chronic high glucose-induced β-cell injury through modulation of autophagy.. Cell Death Dis 2015 Sep 17;6(9):e1885.
    pmc: PMC4650435pubmed: 26379190doi: 10.1038/cddis.2015.230google scholar: lookup
  41. Nixon RA. The role of autophagy in neurodegenerative disease.. Nat Med 2013 Aug;19(8):983-97.
    pubmed: 23921753doi: 10.1038/nm.3232google scholar: lookup
  42. Ding WX, Yin XM. Mitophagy: mechanisms, pathophysiological roles, and analysis.. Biol Chem 2012 Jul;393(7):547-64.
    pmc: PMC3630798pubmed: 22944659doi: 10.1515/hsz-2012-0119google scholar: lookup
  43. nDoubling Time ‐ Online computing with 2 points [Internet]. Available at: http://www.doubling-time.com/compute.php [cited 14 January 2016].
  44. Marędziak M, Marycz K, Smieszek A, Lewandowski D, Toker NY. The influence of static magnetic fields on canine and equine mesenchymal stem cells derived from adipose tissue.. In Vitro Cell Dev Biol Anim 2014 Jun;50(6):562-71.
    pmc: PMC4062816pubmed: 24477562doi: 10.1007/s11626-013-9730-1google scholar: lookup
  45. Chen T, Zhou Y, Tan WS. Influence of lactic acid on the proliferation, metabolism, and differentiation of rabbit mesenchymal stem cells.. Cell Biol Toxicol 2009 Dec;25(6):573-86.
    pubmed: 19130272doi: 10.1007/s10565-008-9113-7google scholar: lookup
  46. 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.
    pubmed: 2440339doi: 10.1006/abio.1987.9999google scholar: lookup
  47. Kodama K, Horikoshi M, Toda K, Yamada S, Hara K, Irie J, Sirota M, Morgan AA, Chen R, Ohtsu H, Maeda S, Kadowaki T, Butte AJ. Expression-based genome-wide association study links the receptor CD44 in adipose tissue with type 2 diabetes.. Proc Natl Acad Sci U S A 2012 May 1;109(18):7049-54.
    pmc: PMC3344989pubmed: 22499789doi: 10.1073/pnas.1114513109google scholar: lookup
  48. Kodama K, Toda K, Morinaga S, Yamada S, Butte AJ. Anti-CD44 antibody treatment lowers hyperglycemia and improves insulin resistance, adipose inflammation, and hepatic steatosis in diet-induced obese mice.. Diabetes 2015 Mar;64(3):867-75.
    pmc: PMC4392898pubmed: 25294945doi: 10.2337/db14-0149google scholar: lookup
  49. Kang HS, Liao G, DeGraff LM, Gerrish K, Bortner CD, Garantziotis S, Jetten AM. CD44 plays a critical role in regulating diet-induced adipose inflammation, hepatic steatosis, and insulin resistance.. PLoS One 2013;8(3):e58417.
    pmc: PMC3591334pubmed: 23505504doi: 10.1371/journal.pone.0058417google scholar: lookup
  50. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, Neschen S, White MF, Bilz S, Sono S, Pypaert M, Shulman GI. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents.. J Clin Invest 2005 Dec;115(12):3587-93.
    pmc: PMC1280967pubmed: 16284649doi: 10.1172/jci25151google scholar: lookup
  51. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes.. N Engl J Med 2004 Feb 12;350(7):664-71.
    pmc: PMC2995502pubmed: 14960743doi: 10.1056/nejmoa031314google scholar: lookup
  52. Páramo B, Hernández-Fonseca K, Estrada-Sánchez AM, Jiménez N, Hernández-Cruz A, Massieu L. Pathways involved in the generation of reactive oxygen and nitrogen species during glucose deprivation and its role on the death of cultured hippocampal neurons.. Neuroscience 2010 Jun 2;167(4):1057-69.
    pubmed: 20226235doi: 10.1016/j.neuroscience.2010.02.074google scholar: lookup
  53. Shigenaga MK, Hagen TM, Ames BN. Oxidative damage and mitochondrial decay in aging.. Proc Natl Acad Sci U S A 1994 Nov 8;91(23):10771-8.
    pmc: PMC45108pubmed: 7971961doi: 10.1073/pnas.91.23.10771google scholar: lookup
  54. Forni MF, Peloggia J, Trudeau K, Shirihai O, Kowaltowski AJ. Murine Mesenchymal Stem Cell Commitment to Differentiation Is Regulated by Mitochondrial Dynamics.. Stem Cells 2016 Mar;34(3):743-55.
    pmc: PMC4803524pubmed: 26638184doi: 10.1002/stem.2248google scholar: lookup
  55. Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U. Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells.. Stem Cells 2011 Mar;29(3):486-95.
    pmc: PMC4374603pubmed: 21425411doi: 10.1002/stem.590google scholar: lookup
  56. Tanaka A. Parkin-mediated selective mitochondrial autophagy, mitophagy: Parkin purges damaged organelles from the vital mitochondrial network.. FEBS Lett 2010 Apr 2;584(7):1386-92.
    pmc: PMC2843751pubmed: 20188730doi: 10.1016/j.febslet.2010.02.060google scholar: lookup
  57. Pesah Y, Pham T, Burgess H, Middlebrooks B, Verstreken P, Zhou Y, Harding M, Bellen H, Mardon G. Drosophila parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress.. Development 2004 May;131(9):2183-94.
    pubmed: 15073152doi: 10.1242/dev.01095google scholar: lookup
  58. Guo M. Drosophila as a model to study mitochondrial dysfunction in Parkinson's disease.. Cold Spring Harb Perspect Med 2012 Nov 1;2(11).
    pmc: PMC3543109pubmed: 23024178doi: 10.1101/cshperspect.a009944google scholar: lookup
  59. Dave KD, De Silva S, Sheth NP, Ramboz S, Beck MJ, Quang C, Switzer RC 3rd, Ahmad SO, Sunkin SM, Walker D, Cui X, Fisher DA, McCoy AM, Gamber K, Ding X, Goldberg MS, Benkovic SA, Haupt M, Baptista MA, Fiske BK, Sherer TB, Frasier MA. Phenotypic characterization of recessive gene knockout rat models of Parkinson's disease.. Neurobiol Dis 2014 Oct;70:190-203.
    pubmed: 24969022doi: 10.1016/j.nbd.2014.06.009google scholar: lookup
  60. Jin SM, Youle RJ. PINK1- and Parkin-mediated mitophagy at a glance.. J Cell Sci 2012 Feb 15;125(Pt 4):795-9.
    pmc: PMC3656616pubmed: 22448035doi: 10.1242/jcs.093849google scholar: lookup
  61. Joshi A, Kundu M. Mitophagy in hematopoietic stem cells: the case for exploration.. Autophagy 2013 Nov 1;9(11):1737-49.
    pmc: PMC4028333pubmed: 24135495doi: 10.4161/auto.26681google scholar: lookup
  62. Diaz F, Moraes CT. Mitochondrial biogenesis and turnover.. Cell Calcium 2008 Jul;44(1):24-35.
    pmc: PMC3175594pubmed: 18395251doi: 10.1016/j.ceca.2007.12.004google scholar: lookup
  63. Boudina S, Graham TE. Mitochondrial function/dysfunction in white adipose tissue.. Exp Physiol 2014 Sep;99(9):1168-78.
    pubmed: 25128326doi: 10.1113/expphysiol.2014.081414google scholar: lookup
  64. Prowse AB, Chong F, Elliott DA, Elefanty AG, Stanley EG, Gray PP, Munro TP, Osborne GW. Analysis of mitochondrial function and localisation during human embryonic stem cell differentiation in vitro.. PLoS One 2012;7(12):e52214.
    pmc: PMC3526579pubmed: 23284940doi: 10.1371/journal.pone.0052214google scholar: lookup
  65. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells.. Stem Cells 2008 Apr;26(4):960-8.
    pubmed: 18218821doi: 10.1634/stemcells.2007-0509google scholar: lookup
  66. Dentelli P, Barale C, Togliatto G, Trombetta A, Olgasi C, Gili M, Riganti C, Toppino M, Brizzi MF. A diabetic milieu promotes OCT4 and NANOG production in human visceral-derived adipose stem cells.. Diabetologia 2013 Jan;56(1):173-84.
    pubmed: 23064289doi: 10.1007/s00125-012-2734-7google scholar: lookup
  67. Pan GJ, Chang ZY, Schöler HR, Pei D. Stem cell pluripotency and transcription factor Oct4.. Cell Res 2002 Dec;12(5-6):321-9.
    pubmed: 12528890doi: 10.1038/sj.cr.7290134google scholar: lookup
  68. Altomonte J, Richter A, Harbaran S, Suriawinata J, Nakae J, Thung SN, Meseck M, Accili D, Dong H. Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice.. Am J Physiol Endocrinol Metab 2003 Oct;285(4):E718-28.
    pubmed: 12783775doi: 10.1152/ajpendo.00156.2003google scholar: lookup
  69. Zhou J, Liao W, Yang J, Ma K, Li X, Wang Y, Wang D, Wang L, Zhang Y, Yin Y, Zhao Y, Zhu WG. FOXO3 induces FOXO1-dependent autophagy by activating the AKT1 signaling pathway.. Autophagy 2012 Dec;8(12):1712-23.
    pmc: PMC3541283pubmed: 22931788doi: 10.4161/auto.21830google scholar: lookup
  70. Samocha-Bonet D, Campbell LV, Mori TA, Croft KD, Greenfield JR, Turner N, Heilbronn LK. Overfeeding reduces insulin sensitivity and increases oxidative stress, without altering markers of mitochondrial content and function in humans.. PLoS One 2012;7(5):e36320.
    pmc: PMC3346759pubmed: 22586466doi: 10.1371/journal.pone.0036320google scholar: lookup
  71. Singh R, Cuervo AM. Autophagy in the cellular energetic balance.. Cell Metab 2011 May 4;13(5):495-504.
    pmc: PMC3099265pubmed: 21531332doi: 10.1016/j.cmet.2011.04.004google scholar: lookup
  72. Katayama M, Kawaguchi T, Berger MS, Pieper RO. DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells.. Cell Death Differ 2007 Mar;14(3):548-58.
    pubmed: 16946731doi: 10.1038/sj.cdd.4402030google scholar: lookup
  73. Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy.. Cell Death Differ 2009 Jul;16(7):1040-52.
    pubmed: 19407826doi: 10.1038/cdd.2009.49google scholar: lookup
  74. Green DR, Levine B. To be or not to be? How selective autophagy and cell death govern cell fate.. Cell 2014 Mar 27;157(1):65-75.
    pmc: PMC4020175pubmed: 24679527doi: 10.1016/j.cell.2014.02.049google scholar: lookup
  75. Nuschke A, Rodrigues M, Stolz DB, Chu CT, Griffith L, Wells A. Human mesenchymal stem cells/multipotent stromal cells consume accumulated autophagosomes early in differentiation.. Stem Cell Res Ther 2014 Dec 17;5(6):140.
    pmc: PMC4446103pubmed: 25523618doi: 10.1186/scrt530google scholar: lookup
  76. Zhao Y, Chen G, Zhang W, Xu N, Zhu JY, Jia J, Sun ZJ, Wang YN, Zhao YF. Autophagy regulates hypoxia-induced osteoclastogenesis through the HIF-1α/BNIP3 signaling pathway.. J Cell Physiol 2012 Feb;227(2):639-48.
    pubmed: 21465467doi: 10.1002/jcp.22768google scholar: lookup
  77. Aymard E, Barruche V, Naves T, Bordes S, Closs B, Verdier M, Ratinaud MH. Autophagy in human keratinocytes: an early step of the differentiation?. Exp Dermatol 2011 Mar;20(3):263-8.
    pubmed: 21166723doi: 10.1111/j.1600-0625.2010.01157.xgoogle scholar: lookup
  78. Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins.. Growth Factors 2004 Dec;22(4):233-41.
    pubmed: 15621726doi: 10.1080/08977190412331279890google scholar: lookup
  79. Wongdee K, Charoenphandhu N. Osteoporosis in diabetes mellitus: Possible cellular and molecular mechanisms.. World J Diabetes 2011 Mar 15;2(3):41-8.
    pmc: PMC3083906pubmed: 21537459doi: 10.4239/wjd.v2.i3.41google scholar: lookup
  80. Almeida M. Unraveling the role of FoxOs in bone--insights from mouse models.. Bone 2011 Sep;49(3):319-27.
    pmc: PMC3143252pubmed: 21664311doi: 10.1016/j.bone.2011.05.023google scholar: lookup
  81. Bartell SM, Kim HN, Ambrogini E, Han L, Iyer S, Serra Ucer S, Rabinovitch P, Jilka RL, Weinstein RS, Zhao H, O'Brien CA, Manolagas SC, Almeida M. FoxO proteins restrain osteoclastogenesis and bone resorption by attenuating H2O2 accumulation.. Nat Commun 2014 Apr 30;5:3773.
    pmc: PMC4015330pubmed: 24781012doi: 10.1038/ncomms4773google scholar: lookup
  82. Horvath S. DNA methylation age of human tissues and cell types.. Genome Biol 2013;14(10):R115.
    pmc: PMC4015143pubmed: 24138928doi: 10.1186/gb-2013-14-10-r115google scholar: lookup
  83. Zhao J, Goldberg J, Bremner JD, Vaccarino V. Global DNA methylation is associated with insulin resistance: a monozygotic twin study.. Diabetes 2012 Feb;61(2):542-6.
    pmc: PMC3266395pubmed: 22210312doi: 10.2337/db11-1048google scholar: lookup
  84. Kim AY, Park YJ, Pan X, Shin KC, Kwak SH, Bassas AF, Sallam RM, Park KS, Alfadda AA, Xu A, Kim JB. Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance.. Nat Commun 2015 Jul 3;6:7585.
    pmc: PMC4506505pubmed: 26139044doi: 10.1038/ncomms8585google scholar: lookup
  85. Bayarsaihan D. Epigenetic mechanisms in inflammation.. J Dent Res 2011 Jan;90(1):9-17.
    pmc: PMC3144097pubmed: 21178119doi: 10.1177/0022034510378683google scholar: lookup

Citations

This article has been cited 51 times.
  1. Stefaniuk-Szmukier M, Piórkowska K, Ropka-Molik K. Equine Metabolic Syndrome: A Complex Disease Influenced by Multifactorial Genetic Factors. Genes (Basel) 2023 Jul 27;14(8).
    doi: 10.3390/genes14081544pubmed: 37628596google scholar: lookup
  2. Hou W, Chen M, Ye C, Chen E, Li W, Zhang W. Parkin Inhibits RANKL-Induced Osteoclastogenesis and Ovariectomy-Induced Bone Loss. Biomolecules 2022 Oct 31;12(11).
    doi: 10.3390/biom12111602pubmed: 36358952google scholar: lookup
  3. Sarkar J, Das M, Howlader MSI, Prateeksha P, Barthels D, Das H. Epigallocatechin-3-gallate inhibits osteoclastic differentiation by modulating mitophagy and mitochondrial functions. Cell Death Dis 2022 Oct 28;13(10):908.
    doi: 10.1038/s41419-022-05343-1pubmed: 36307395google scholar: lookup
  4. Sharun K, Jambagi K, Kumar R, Gugjoo MB, Pawde AM, Tuli HS, Dhama K, Amarpal. Clinical applications of adipose-derived stromal vascular fraction in veterinary practice. Vet Q 2022 Dec;42(1):151-166.
    doi: 10.1080/01652176.2022.2102688pubmed: 35841195google scholar: lookup
  5. 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/cells11091437pubmed: 35563743google scholar: lookup
  6. Depuydt E, Broeckx SY, Chiers K, Patruno M, Da Dalt L, Duchateau L, Saunders J, Pille F, Martens A, Van Hecke L, Spaas JH. Cellular and Humoral Immunogenicity Investigation of Single and Repeated Allogeneic Tenogenic Primed Mesenchymal Stem Cell Treatments in Horses Suffering From Tendon Injuries. Front Vet Sci 2021;8:789293.
    doi: 10.3389/fvets.2021.789293pubmed: 35281431google scholar: lookup
  7. Fei D, Xia Y, Zhai Q, Wang Y, Zhou F, Zhao W, He X, Wang Q, Jin Y, Li B. Exosomes Regulate Interclonal Communication on Osteogenic Differentiation Among Heterogeneous Osteogenic Single-Cell Clones Through PINK1/Parkin-Mediated Mitophagy. Front Cell Dev Biol 2021;9:687258.
    doi: 10.3389/fcell.2021.687258pubmed: 34604210google scholar: lookup
  8. Cequier A, Sanz C, Rodellar C, Barrachina L. The Usefulness of Mesenchymal Stem Cells beyond the Musculoskeletal System in Horses. Animals (Basel) 2021 Mar 25;11(4).
    doi: 10.3390/ani11040931pubmed: 33805967google scholar: lookup
  9. Bourebaba L, Kornicka-Garbowska K, Al Naem M, Röcken M, Łyczko J, Marycz K. MSI-1436 improves EMS adipose derived progenitor stem cells in the course of adipogenic differentiation through modulation of ER stress, apoptosis, and oxidative stress. Stem Cell Res Ther 2021 Feb 3;12(1):97.
    doi: 10.1186/s13287-020-02102-xpubmed: 33536069google scholar: lookup
  10. Sávio-Silva C, Beyerstedt S, Soinski-Sousa PE, Casaro EB, Balby-Rocha MTA, Simplício-Filho A, Alves-Silva J, Rangel ÉB. Mesenchymal Stem Cell Therapy for Diabetic Kidney Disease: A Review of the Studies Using Syngeneic, Autologous, Allogeneic, and Xenogeneic Cells. Stem Cells Int 2020;2020:8833725.
    doi: 10.1155/2020/8833725pubmed: 33505469google scholar: lookup
  11. Jifcovici A, Solano MA, Fitzpatrick N, Findji L, Blunn G, Sanghani-Kerai A. Comparison of Fat Harvested from Flank and Falciform Regions for Stem Cell Therapy in Dogs. Vet Sci 2021 Jan 25;8(2).
    doi: 10.3390/vetsci8020019pubmed: 33503997google scholar: lookup
  12. Acar MB, Ayaz-Güner Ş, Di Bernardo G, Güner H, Murat A, Peluso G, Özcan S, Galderisi U. Obesity induced by high-fat diet is associated with critical changes in biological and molecular functions of mesenchymal stromal cells present in visceral adipose tissue. Aging (Albany NY) 2020 Dec 27;12(24):24894-24913.
    doi: 10.18632/aging.202423pubmed: 33361524google scholar: lookup
  13. Wang S, Deng Z, Ma Y, Jin J, Qi F, Li S, Liu C, Lyu FJ, Zheng Q. The Role of Autophagy and Mitophagy in Bone Metabolic Disorders. Int J Biol Sci 2020;16(14):2675-2691.
    doi: 10.7150/ijbs.46627pubmed: 32792864google scholar: lookup
  14. Tesseraud S, Avril P, Bonnet M, Bonnieu A, Cassar-Malek I, Chabi B, Dessauge F, Gabillard JC, Perruchot MH, Seiliez I. Autophagy in farm animals: current knowledge and future challenges. Autophagy 2021 Aug;17(8):1809-1827.
    doi: 10.1080/15548627.2020.1798064pubmed: 32686564google scholar: lookup
  15. 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.2020.00278pubmed: 32656249google scholar: lookup
  16. Wu H, Meng Z, Jiao Y, Ren Y, Yang X, Liu H, Wang R, Cui Y, Pan L, Cao Y. The endoplasmic reticulum stress induced by tunicamycin affects the viability and autophagy activity of chondrocytes. J Clin Lab Anal 2020 Oct;34(10):e23437.
    doi: 10.1002/jcla.23437pubmed: 32592208google scholar: lookup
  17. Boulestreau J, Maumus M, Rozier P, Jorgensen C, Noël D. Mesenchymal Stem Cell Derived Extracellular Vesicles in Aging. Front Cell Dev Biol 2020;8:107.
    doi: 10.3389/fcell.2020.00107pubmed: 32154253google scholar: lookup
  18. Feng K, Chen H, Xu C. Chondro-protective effects of celastrol on osteoarthritis through autophagy activation and NF-κB signaling pathway inhibition. Inflamm Res 2020 Apr;69(4):385-400.
    doi: 10.1007/s00011-020-01327-zpubmed: 32112120google scholar: lookup
  19. Kornicka-Garbowska K, Pędziwiatr R, Woźniak P, Kucharczyk K, Marycz K. Microvesicles isolated from 5-azacytidine-and-resveratrol-treated mesenchymal stem cells for the treatment of suspensory ligament injury in horse-a case report. Stem Cell Res Ther 2019 Dec 18;10(1):394.
    doi: 10.1186/s13287-019-1469-5pubmed: 31852535google scholar: lookup
  20. Bourebaba L, Michalak I, Baouche M, Kucharczyk K, Marycz K. Cladophora glomerata methanolic extract promotes chondrogenic gene expression and cartilage phenotype differentiation in equine adipose-derived mesenchymal stromal stem cells affected by metabolic syndrome. Stem Cell Res Ther 2019 Dec 17;10(1):392.
    doi: 10.1186/s13287-019-1499-zpubmed: 31847882google scholar: lookup
  21. Al Naem M, Bourebaba L, Kucharczyk K, Röcken M, Marycz K. Therapeutic mesenchymal stromal stem cells: Isolation, characterization and role in equine regenerative medicine and metabolic disorders. Stem Cell Rev Rep 2020 Apr;16(2):301-322.
    doi: 10.1007/s12015-019-09932-0pubmed: 31797146google scholar: lookup
  22. Oh JY, Kim EH, Lee YJ, Sai S, Lim SH, Park JW, Chung HK, Kim J, Vares G, Takahashi A, Jeong YK, Kim MS, Kong CB. Synergistic Autophagy Effect of miR-212-3p in Zoledronic Acid-Treated In Vitro and Orthotopic In Vivo Models and in Patient-Derived Osteosarcoma Cells. Cancers (Basel) 2019 Nov 18;11(11).
    doi: 10.3390/cancers11111812pubmed: 31752184google scholar: lookup
  23. Marycz K, Szłapka-Kosarzewska J, Geburek F, Kornicka-Garbowska K. Systemic Administration of Rejuvenated Adipose-Derived Mesenchymal Stem Cells Improves Liver Metabolism in Equine Metabolic Syndrome (EMS)- New Approach in Veterinary Regenerative Medicine. Stem Cell Rev Rep 2019 Dec;15(6):842-850.
    doi: 10.1007/s12015-019-09913-3pubmed: 31620992google scholar: lookup
  24. Fafián-Labora JA, Morente-López M, Arufe MC. Effect of aging on behaviour of mesenchymal stem cells. World J Stem Cells 2019 Jun 26;11(6):337-346.
    doi: 10.4252/wjsc.v11.i6.337pubmed: 31293716google scholar: lookup
  25. Bourebaba L, Bedjou F, Röcken M, Marycz K. Nortropane alkaloids as pharmacological chaperones in the rescue of equine adipose-derived mesenchymal stromal stem cells affected by metabolic syndrome through mitochondrial potentiation, endoplasmic reticulum stress mitigation and insulin resistance alleviation. Stem Cell Res Ther 2019 Jun 18;10(1):178.
    doi: 10.1186/s13287-019-1292-zpubmed: 31215461google scholar: lookup
  26. Marycz K, Houston JMI, Weiss C, Röcken M, Kornicka K. 5-Azacytidine and Resveratrol Enhance Chondrogenic Differentiation of Metabolic Syndrome-Derived Mesenchymal Stem Cells by Modulating Autophagy. Oxid Med Cell Longev 2019;2019:1523140.
    doi: 10.1155/2019/1523140pubmed: 31214275google scholar: lookup
  27. Kornicka K, Geburek F, Röcken M, Marycz K. Stem Cells in Equine Veterinary Practice-Current Trends, Risks, and Perspectives. J Clin Med 2019 May 14;8(5).
    doi: 10.3390/jcm8050675pubmed: 31091732google scholar: lookup
  28. Bourebaba L, Röcken M, Marycz K. Osteochondritis dissecans (OCD) in Horses - Molecular Background of its Pathogenesis and Perspectives for Progenitor Stem Cell Therapy. Stem Cell Rev Rep 2019 Jun;15(3):374-390.
    doi: 10.1007/s12015-019-09875-6pubmed: 30796679google scholar: lookup
  29. Mahmoud M, Abu-Shahba N, Azmy O, El-Badri N. Impact of Diabetes Mellitus on Human Mesenchymal Stromal Cell Biology and Functionality: Implications for Autologous Transplantation. Stem Cell Rev Rep 2019 Apr;15(2):194-217.
    doi: 10.1007/s12015-018-9869-ypubmed: 30680660google scholar: lookup
  30. Smieszek A, Kornicka K, Szłapka-Kosarzewska J, Androvic P, Valihrach L, Langerova L, Rohlova E, Kubista M, Marycz K. Metformin Increases Proliferative Activity and Viability of Multipotent Stromal Stem Cells Isolated from Adipose Tissue Derived from Horses with Equine Metabolic Syndrome. Cells 2019 Jan 22;8(2).
    doi: 10.3390/cells8020080pubmed: 30678275google scholar: lookup
  31. Alicka M, Marycz K. The Effect of Chronic Inflammation and Oxidative and Endoplasmic Reticulum Stress in the Course of Metabolic Syndrome and Its Therapy. Stem Cells Int 2018;2018:4274361.
    doi: 10.1155/2018/4274361pubmed: 30425746google scholar: lookup
  32. Kornicka K, Szłapka-Kosarzewska J, Śmieszek A, Marycz K. 5-Azacytydine and resveratrol reverse senescence and ageing of adipose stem cells via modulation of mitochondrial dynamics and autophagy. J Cell Mol Med 2019 Jan;23(1):237-259.
    doi: 10.1111/jcmm.13914pubmed: 30370650google scholar: lookup
  33. Kornicka K, Śmieszek A, Węgrzyn AS, Röcken M, Marycz K. Immunomodulatory Properties of Adipose-Derived Stem Cells Treated with 5-Azacytydine and Resveratrol on Peripheral Blood Mononuclear Cells and Macrophages in Metabolic Syndrome Animals. J Clin Med 2018 Oct 24;7(11).
    doi: 10.3390/jcm7110383pubmed: 30356025google scholar: lookup
  34. Aghajani Nargesi A, Zhu XY, Hickson LJ, Conley SM, van Wijnen AJ, Lerman LO, Eirin A. Metabolic Syndrome Modulates Protein Import into the Mitochondria of Porcine Mesenchymal Stem Cells. Stem Cell Rev Rep 2019 Jun;15(3):427-438.
    doi: 10.1007/s12015-018-9855-4pubmed: 30338499google scholar: lookup
  35. Kornicka K, Śmieszek A, Szłapka-Kosarzewska J, Irwin Houston JM, Roecken M, Marycz K. Characterization of Apoptosis, Autophagy and Oxidative Stress in Pancreatic Islets Cells and Intestinal Epithelial Cells Isolated from Equine Metabolic Syndrome (EMS) Horses. Int J Mol Sci 2018 Oct 8;19(10).
    doi: 10.3390/ijms19103068pubmed: 30297648google scholar: lookup
  36. Zhu Y, Ma WQ, Han XQ, Wang Y, Wang X, Liu NF. Advanced glycation end products accelerate calcification in VSMCs through HIF-1α/PDK4 activation and suppress glucose metabolism. Sci Rep 2018 Sep 13;8(1):13730.
    doi: 10.1038/s41598-018-31877-6pubmed: 30213959google scholar: lookup
  37. Marycz K, Kornicka K, Irwin-Houston JM, Weiss C. Combination of resveratrol and 5-azacytydine improves osteogenesis of metabolic syndrome mesenchymal stem cells. J Cell Mol Med 2018 Oct;22(10):4771-4793.
    doi: 10.1111/jcmm.13731pubmed: 29999247google scholar: lookup
  38. Marycz K, Weiss C, Śmieszek 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: 10.1155/2018/5340756pubmed: 29977307google scholar: lookup
  39. Liu Q, Chen F, Wang L, Zhang Y. [Research progress of the donor factors and experimental factors affecting adipogenic differentiation of adipose derived stem cells]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2017 Nov 15;31(11):1390-1395.
    doi: 10.7507/1002-1892.201704057pubmed: 29798597google scholar: lookup
  40. Dias I, Salviano Í, Mencalha A, de Carvalho SN, Thole AA, Carvalho L, Cortez E, Stumbo AC. Neonatal overfeeding impairs differentiation potential of mice subcutaneous adipose mesenchymal stem cells. Stem Cell Rev Rep 2018 Aug;14(4):535-545.
    doi: 10.1007/s12015-018-9812-2pubmed: 29667027google scholar: lookup
  41. Shen Y, Wu L, Qin D, Xia Y, Zhou Z, Zhang X, Wu X. Carbon black suppresses the osteogenesis of mesenchymal stem cells: the role of mitochondria. Part Fibre Toxicol 2018 Apr 12;15(1):16.
    doi: 10.1186/s12989-018-0253-5pubmed: 29650039google scholar: lookup
  42. Kornicka K, Houston J, Marycz K. Dysfunction of Mesenchymal Stem Cells Isolated from Metabolic Syndrome and Type 2 Diabetic Patients as Result of Oxidative Stress and Autophagy may Limit Their Potential Therapeutic Use. Stem Cell Rev Rep 2018 Jun;14(3):337-345.
    doi: 10.1007/s12015-018-9809-xpubmed: 29611042google scholar: lookup
  43. Szydlarska J, Weiss C, Marycz K. The Effect of Methyl-β-cyclodextrin on Apoptosis, Proliferative Activity, and Oxidative Stress in Adipose-Derived Mesenchymal Stromal Cells of Horses Suffering from Metabolic Syndrome (EMS). Molecules 2018 Jan 30;23(2).
    doi: 10.3390/molecules23020287pubmed: 29385746google scholar: lookup
  44. Nawrocka D, Kornicka K, Śmieszek A, Marycz K. Spirulina platensis Improves Mitochondrial Function Impaired by Elevated Oxidative Stress in Adipose-Derived Mesenchymal Stromal Cells (ASCs) and Intestinal Epithelial Cells (IECs), and Enhances Insulin Sensitivity in Equine Metabolic Syndrome (EMS) Horses. Mar Drugs 2017 Aug 3;15(8).
    doi: 10.3390/md15080237pubmed: 28771165google scholar: lookup
  45. Marycz K, Kornicka K, Grzesiak J, Śmieszek A, Szłapka J. Macroautophagy and Selective Mitophagy Ameliorate Chondrogenic Differentiation Potential in Adipose Stem Cells of Equine Metabolic Syndrome: New Findings in the Field of Progenitor Cells Differentiation. Oxid Med Cell Longev 2016;2016:3718468.
    doi: 10.1155/2016/3718468pubmed: 28053691google scholar: lookup
  46. Hu Y, Lu H, Fang H, Chen B, Chen Z, Jiang M, Zhou Y, Li Z, Gao S, Huang Z, Zhou C, Liu Y, Chen Z, Fan Y. Targeting SIRT3 to regulate mitophagy-dependent ferroptosis for preventing glucocorticoid-induced osteoporosis. Int J Surg 2025 Oct 1;111(10):6647-6662.
    doi: 10.1097/JS9.0000000000002783pubmed: 40607908google scholar: lookup
  47. Han LJ, Zhu JZ, Liu HC, Lin XS, Yang SZ. Integrative genomic analysis and diagnostic modeling of osteoporosis: unraveling the interplay of autophagy, osteogenesis, adipogenesis, and immune infiltration. Front Med (Lausanne) 2025;12:1544390.
    doi: 10.3389/fmed.2025.1544390pubmed: 40313558google scholar: lookup
  48. Fan S, Li J, Zheng G, Ma Z, Peng X, Xie Z, Liu W, Yu W, Lin J, Su Z, Xu P, Wang P, Wu Y, Shen H, Ye G. WAC Facilitates Mitophagy-mediated MSC Osteogenesis and New Bone Formation via Protecting PINK1 from Ubiquitination-Dependent Degradation. Adv Sci (Weinh) 2025 Jan;12(2):e2404107.
    doi: 10.1002/advs.202404107pubmed: 39555688google scholar: lookup
  49. Ferreira-Baptista C, Ferreira R, Fernandes MH, Gomes PS, Colaço B. Influence of the Anatomical Site on Adipose Tissue-Derived Stromal Cells' Biological Profile and Osteogenic Potential in Companion Animals. Vet Sci 2023 Nov 24;10(12).
    doi: 10.3390/vetsci10120673pubmed: 38133224google scholar: lookup
  50. Bourebaba L, Serwotka-Suszczak A, Bourebaba N, Zyzak M, Marycz K. The PTP1B Inhibitor Trodusquemine (MSI-1436) Improves Glucose Uptake in Equine Metabolic Syndrome Affected Liver through Anti-Inflammatory and Antifibrotic Activity. Int J Inflam 2023;2023:3803056.
    doi: 10.1155/2023/3803056pubmed: 37808009google scholar: lookup
  51. Xu X, Wang J, Xia Y, Yin Y, Zhu T, Chen F, Hai C. Autophagy, a double-edged sword for oral tissue regeneration. J Adv Res 2024 May;59:141-159.
    doi: 10.1016/j.jare.2023.06.010pubmed: 37356803google scholar: lookup
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