Cited by 167Mesenchymal stem cell researchMitochondrial Function and PathologyAdipose Tissue and Metabolism

The role and mechanism of mitochondrial functions and energy metabolism in the function regulation of the mesenchymal stem cells

Open access
Yan, Wanhao, Diao, Shu, Fan, Zhipeng·2021·Stem Cell Research & Therapy

Abstract

Mesenchymal stem cells (MSCs) are multipotent cells that show self-renewal, multi-directional differentiation, and paracrine and immune regulation. As a result of these properties, the MSCs have great clinical application prospects, especially in the regeneration of injured tissues, functional reconstruction, and cell therapy. However, the transplanted MSCs are prone to ageing and apoptosis and have a difficult to control direction differentiation. Therefore, it is necessary to effectively regulate the functions of the MSCs to promote their desired effects. In recent years, it has been found that mitochondria, the main organelles responsible for energy metabolism and adenosine triphosphate production in cells, play a key role in regulating different functions of the MSCs through various mechanisms. Thus, mitochondria could act as effective targets for regulating and promoting the functions of the MSCs. In this review, we discuss the research status and current understanding of the role and mechanism of mitochondrial energy metabolism, morphology, transfer modes, and dynamics on MSC functions.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s13287-021-02194-z

Cites

14 of 14 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • MSC mitochondrial metabolism is linked to secretion of trophic factors and intercellular communication, in turn impacting function in other cells.

    “This is consistent with reports that MSC mitochondrial metabolism is linked to secretion of trophic factors and intercellular communication, in turn impacting function in other cells (Yan et al., 2021; Wang et al., 2025).”

    From APOE3-Christchurch variant enhances neurovascular support functions of iPSC-derived mesenchymal stromal cells (2026) · cites this paper as Yan et al., 2021

    The section on mitochondrial transfer in the regulation of MSC functions (page unavailable) describes intercellular transfer of MSC mitochondria through nanotubes and extracellular vesicles, with effects on recipient cells. The section on mitochondrial function and energy metabolism pathways links metabolism to MSC function. Our copy does not establish the claimed link between mitochondrial metabolism and secretion of trophic factors. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 107

  1. [1]Hu L Liu Y Wang S Stem cell-based tooth and periodontal regeneration Oral Dis 2018 24 5 696 705 10.1111/odi.12703 28636235 · DOI
  2. [2]Galipeau J Sensébé L Mesenchymal stromal cells: clinical challenges and therapeutic opportunities Cell Stem Cell 2018 22 6 824 833 10.1016/j.stem.2018.05.004 29859173 PMC6434696 · DOI · Paper page
  3. [3]Chen L Qu J Cheng T Chen X Xiang C Menstrual blood-derived stem cells: toward therapeutic mechanisms, novel strategies, and future perspectives in the treatment of diseases Stem Cell Res Ther 2019 10 1 406 10.1186/s13287-019-1503-7 31864423 PMC6925480 · DOI
  4. [4]Zheng C Chen J Liu S Jin Y Stem cell-based bone and dental regeneration: a view of microenvironmental modulation Int J Oral Sci 2019 11 3 23 10.1038/s41368-019-0060-3 31423011 PMC6802669 · DOI
  5. [5]Wang L Yang L Tian L Cannabinoid receptor 1 mediates homing of bone marrow-derived mesenchymal stem cells triggered by chronic liver injury J Cell Physiol 2017 232 1 110 121 10.1002/jcp.25395 27028843 · DOI
  6. [6]Ma Y, Ma J, Zhao Y, et al. Comparison of phenotypic markers and neural differentiation potential of human bone marrow stromal cells from the cranial bone and iliac crest. J Cell Physiol. 2019; 10.1002/jcp.28167. Online ahead of print 30677139 · DOI
  7. [7]Wang J Chen Z Sun M Characterization and therapeutic applications of mesenchymal stem cells for regenerative medicine Tissue Cell 2020 64 101330 10.1016/j.tice.2020.101330 32473704 · DOI
  8. [8]Seetharaman R Mahmood A Kshatriya P Patel D Srivastava A An overview on stem cells in tissue regeneration Curr Pharm Des 2019 25 18 2086 2098 10.2174/1381612825666190705211705 31298159 · DOI
  9. [9]Braakman I Bulleid NJ Protein folding and modification in the mammalian endoplasmic reticulum Annu Rev Biochem 2011 80 71 99 10.1146/annurev-biochem-062209-093836 21495850 · DOI
  10. [10]Viotti C ER to golgi-dependent protein secretion: the conventional pathway Methods Mol Biol 2016 1459 3 29 10.1007/978-1-4939-3804-9_1 27665548 · DOI
  11. [11]Wang Y, Liu Y, Chen E, Pan Z. The role of mitochondrial dysfunction in mesenchymal stem cell senescence. Cell Tissue Res. 2020; 10.1007/s00441-020-03272-z. Online ahead of print 32803322 · DOI
  12. [12]Li Q Gao Z Chen Y Guan MX The role of mitochondria in osteogenic, adipogenic and chondrogenic differentiation of mesenchymal stem cells Protein Cell 2017 8 6 439 445 10.1007/s13238-017-0385-7 28271444 PMC5445026 · DOI
  13. [13]Rafalski VA Mancini E Brunet A Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate J Cell Sci 2012 125 Pt 23 5597 5608 10.1242/jcs.114827 23420198 PMC3575699 · DOI
  14. [14]Wanet A Arnould T Najimi M Renard P Connecting mitochondria, metabolism, and stem cell fate Stem Cells Dev 2015 24 17 1957 1971 10.1089/scd.2015.0117 26134242 PMC4543487 · DOI
  15. [15]Paliwal S Chaudhuri R Agrawal A Mohanty S Regenerative abilities of mesenchymal stem cells through mitochondrial transfer J Biomed Sci 2018 25 1 31 10.1186/s12929-018-0429-1 29602309 PMC5877369 · DOI
  16. [17]Hu C Zhao L Peng C Li L Regulation of the mitochondrial reactive oxygen species: Strategies to control mesenchymal stem cell fates ex vivo and in vivo J Cell Mol Med 2018 22 11 5196 5207 10.1111/jcmm.13835 30160351 PMC6201215 · DOI
  17. [18]Wallace DC Mitochondria as chi Genetics 2008 179 2 727 735 10.1534/genetics.104.91769 18558648 PMC2429869 · DOI
  18. [19]Vyas S Zaganjor E Haigis MC Mitochondria and cancer Cell. 2016 166 3 555 566 10.1016/j.cell.2016.07.002 27471965 PMC5036969 · DOI · Paper page
  19. [20]Paliwal S Chaudhuri R Agrawal A Mohanty S Human tissue-specific MSCs demonstrate differential mitochondria transfer abilities that may determine their regenerative abilities Stem Cell Res Ther 2018 9 1 298 10.1186/s13287-018-1012-0 30409230 PMC6225697 · DOI
  20. [21]Sánchez-Aragó M García-Bermúdez J Martínez-Reyes I Santacatterina F Cuezva JM Degradation of IF1 controls energy metabolism during osteogenic differentiation of stem cells EMBO Rep. 2013 14 7 638 644 10.1038/embor.2013.72 23722655 PMC3701239 · DOI
  21. [23]Hirschey MD Zhao Y Metabolic regulation by lysine malonylation, succinylation, and glutarylation Mol Cell Proteomics. 2015 14 9 2308 2315 10.1074/mcp.R114.046664 25717114 PMC4563717 · DOI
  22. [24]Zhang Y Marsboom G Toth PT Rehman J Mitochondrial respiration regulates adipogenic differentiation of human mesenchymal stem cells Plos One. 2013 8 10 e77077 10.1371/journal.pone.0077077 24204740 PMC3800007 · DOI
  23. [25]Shum LC White NS Mills BN Bentley KL Eliseev RA Energy metabolism in mesenchymal stem cells during osteogenic differentiation Stem Cells Dev. 2016 25 2 114 122 10.1089/scd.2015.0193 26487485 PMC4733323 · DOI
  24. [26]Sandhir R Halder A Sunkaria A Mitochondria as a centrally positioned hub in the innate immune response Biochim Biophys Acta Mol Basis Dis. 2017 1863 5 1090 1097 10.1016/j.bbadis.2016.10.020 27794419 · DOI · Paper page
  25. [27]Wang L Guo X Guo X Zhang X Ren J Decitabine promotes apoptosis in mesenchymal stromal cells isolated from patients with myelodysplastic syndromes by inducing reactive oxygen species generation Eur J Pharmacol. 2019 863 172676 10.1016/j.ejphar.2019.172676 31542488 · DOI
  26. [29]Quinn KP Sridharan GV Hayden RS Quantitative metabolic imaging using endogenous fluorescence to detect stem cell differentiation Sci Rep 2013 3 3432 10.1038/srep03432 24305550 PMC3851884 · DOI
  27. [30]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 34 3 743 755 10.1002/stem.2248 26638184 PMC4803524 · DOI
  28. [31]Shen Y Wu L Qin D Carbon black suppresses the osteogenesis of mesenchymal stem cells: the role of mitochondria Part Fibre Toxicol 2018 15 1 16 10.1186/s12989-018-0253-5 29650039 PMC5897950 · DOI
  29. [32]Jiang D Gao F Zhang Y Mitochondrial transfer of mesenchymal stem cells effectively protects corneal epithelial cells from mitochondrial damage Cell Death Dis 2016 7 11 e2467 10.1038/cddis.2016.358 27831562 PMC5260876 · DOI
  30. [33]Jiang B Yan L Wang X Concise review: mesenchymal stem cells derived from human pluripotent cells, an unlimited and quality-controllable source for therapeutic applications Stem Cells 2019 37 5 572 581 10.1002/stem.2964 30561809 · DOI
  31. [34]Chang CH Curtis JD Maggi LB Jr Posttranscriptional control of T cell effector function by aerobic glycolysis Cell 2013 153 6 1239 1251 10.1016/j.cell.2013.05.016 23746840 PMC3804311 · DOI · Paper page
  32. [35]Jiang D Chen FX Zhou H Bioenergetic crosstalk between mesenchymal stem cells and various ocular cells through the intercellular trafficking of mitochondria Theranostics 2020 10 16 7260 7272 10.7150/thno.46332 32641991 PMC7330858 · DOI
  33. [36]Jackson MV Morrison TJ Doherty DF Mitochondrial transfer via tunneling nanotubes is an important mechanism by which mesenchymal stem cells enhance macrophage phagocytosis in the in vitro and in vivo models of ARDS Stem Cells 2016 34 8 2210 2223 10.1002/stem.2372 27059413 PMC4982045 · DOI · Paper page
  34. [37]Burt R Dey A Aref S Activated stromal cells transfer mitochondria to rescue acute lymphoblastic leukemia cells from oxidative stress Blood 2019 134 17 1415 1429 10.1182/blood.2019001398 31501154 PMC6856969 · DOI
  35. [38]Luz-Crawford P Hernandez J Djouad F Mesenchymal stem cell repression of Th17 cells is triggered by mitochondrial transfer Stem Cell Res Ther 2019 10 1 232 10.1186/s13287-019-1307-9 31370879 PMC6676586 · DOI · Paper page
  36. [41]Morrison TJ Jackson MV Cunningham EK Mesenchymal stromal cells modulate macrophages in clinically relevant lung injury models by extracellular vesicle mitochondrial transfer Am J Respir Crit Care Med 2017 196 10 1275 1286 10.1164/rccm.201701-0170OC 28598224 PMC5694830 · DOI · Paper page
  37. [42]Xu X Duan S Yi F Mitochondrial regulation in pluripotent stem cells Cell Metab 2013 18 3 325 332 10.1016/j.cmet.2013.06.005 23850316 · DOI
  38. [44]Wood Dos Santos T Cristina Pereira Q Teixeira L Effects of polyphenols on thermogenesis and mitochondrial biogenesis Int J Mol Sci 2018 19 9 2757 10.3390/ijms19092757 PMC6164046 30217101 · DOI
  39. [45]Li PA Hou X Hao S Mitochondrial biogenesis in neurodegeneration J Neurosci Res 2017 95 10 2025 2029 10.1002/jnr.24042 28301064 · DOI
  40. [46]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 52 119 131 10.1016/j.semcdb.2016.02.011 26868759 · DOI
  41. [47]Wanet A Remacle N Najar M Mitochondrial remodeling in hepatic differentiation and dedifferentiation Int J Biochem Cell Biol 2014 54 174 185 10.1016/j.biocel.2014.07.015 25084555 · DOI
  42. [48]Otera H Mihara K Molecular mechanisms and physiologic functions of mitochondrial dynamics J Biochem 2011 149 3 241 251 10.1093/jb/mvr002 21233142 · DOI
  43. [50]Otera H Ishihara N Mihara K New insights into the function and regulation of mitochondrial fission Biochim Biophys Acta 2013 1833 5 1256 1268 10.1016/j.bbamcr.2013.02.002 23434681 · DOI
  44. [51]Han YS Kim SM Lee JH Melatonin protects chronic kidney disease mesenchymal stem cells against senescence via PrPC-dependent enhancement of the mitochondrial function J Pineal Res 2019 66 1 e12535 10.1111/jpi.12535 30372554 · DOI
  45. [52]Pasztorek M Rossmanith E Mayr C Influence of platelet lysate on 2D and 3D amniotic mesenchymal stem cell cultures Front Bioeng Biotechnol 2019 7 338 10.3389/fbioe.2019.00338 31803733 PMC6873824 · DOI
  46. [53]Park S Choi SG Yoo SM Pyruvate stimulates mitophagy via PINK1 stabilization Cell Signal 2015 27 9 1824 1830 10.1016/j.cellsig.2015.05.020 26071202 · DOI
  47. [54]Lazarou M Sliter DA Kane LA The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy Nature 2015 524 7565 309 314 10.1038/nature14893 26266977 PMC5018156 · DOI · Paper page
  48. [55]Vafai SB Mootha VK Mitochondrial disorders as windows into an ancient organelle Nature 2012 491 7424 374 383 10.1038/nature11707 23151580 · DOI
  49. [57]Nuschke A Rodrigues M Stolz DB Human mesenchymal stem cells/multipotent stromal cells consume accumulated autophagosomes early in differentiation Stem Cell Res Ther 2014 5 6 140 10.1186/scrt530 25523618 PMC4446103 · DOI
  50. [58]Song BQ Chi Y Li X Inhibition of notch signaling promotes the adipogenic differentiation of mesenchymal stem cells through autophagy activation and PTEN-PI3K/AKT/mTOR pathway Cell Physiol Biochem 2015 36 5 1991 2002 10.1159/000430167 26202359 · DOI
  51. [59]Zhang H Menzies KJ Auwerx J The role of mitochondria in stem cell fate and aging Development 2018 145 8 dev143420 10.1242/dev.143420 29654217 PMC5964648 · DOI
  52. [60]Tsujimoto T Mori T Houri K miR-155 inhibits mitophagy through suppression of BAG5, a partner protein of PINK1 Biochem Biophys Res Commun 2020 523 3 707 712 10.1016/j.bbrc.2020.01.022 31948758 · DOI
  53. [61]Suda T Takubo K Semenza GL Metabolic regulation of hematopoietic stem cells in the hypoxic niche Cell Stem Cell 2011 9 4 298 310 10.1016/j.stem.2011.09.010 21982230 · DOI · Paper page
  54. [62]Pattappa G Thorpe SD Jegard NC Continuous and uninterrupted oxygen tension influences the colony formation and oxidative metabolism of human mesenchymal stem cells Tissue Eng Part C Methods 2013 19 1 68 79 10.1089/ten.tec.2011.0734 22731854 · DOI
  55. [63]Baker N Boyette LB Tuan RS Characterization of bone marrow-derived mesenchymal stem cells in aging Bone 2015 70 37 47 10.1016/j.bone.2014.10.014 25445445 · DOI
  56. [65]Tang Y Luo B Deng Z Mitochondrial aerobic respiration is activated during hair follicle stem cell differentiation, and its dysfunction retards hair regeneration PeerJ 2016 4 e1821 10.7717/peerj.1821 27168957 PMC4860312 · DOI
  57. [66]Shares BH Busch M White N Shum L Eliseev RA Active mitochondria support osteogenic differentiation by stimulating β-catenin acetylation J Biol Chem 2018 293 41 16019 16027 10.1074/jbc.RA118.004102 30150300 PMC6187642 · DOI
  58. [67]Rahman MS Kim YS PINK1-PRKN mitophagy suppression by mangiferin promotes a brown-fat-phenotype via PKA-p38 MAPK signalling in murine C3H10T1/2 mesenchymal stem cells Metabolism 2020 107 154228 10.1016/j.metabol.2020.154228 32289346 · DOI
  59. [68]Jin Y Shen Y Su X The small GTPases Rab27b regulates mitochondrial fatty acid oxidative metabolism of cardiac mesenchymal stem cells Front Cell Dev Biol 2020 8 209 10.3389/fcell.2020.00209 32351955 PMC7174509 · DOI
  60. [69]Matilainen O Quirós PM Auwerx J Mitochondria and epigenetics-crosstalk in homeostasis and stress Trends Cell Biol 2017 27 6 453 463 10.1016/j.tcb.2017.02.004 28274652 · DOI
  61. [71]Folmes CD Nelson TJ Dzeja PP Terzic A Energy metabolism plasticity enables stemness programs Ann N Y Acad Sci 2012 1254 82 89 10.1111/j.1749-6632.2012.06487.x 22548573 PMC3495059 · DOI
  62. [72]Everts B Amiel E van der Windt GJ Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells Blood 2012 120 7 1422 1431 10.1182/blood-2012-03-419747 22786879 PMC3423780 · DOI · Paper page
  63. [73]Seok J Jung HS Park S Alteration of fatty acid oxidation by increased CPT1A on replicative senescence of placenta-derived mesenchymal stem cells Stem Cell Res Ther 2020 11 1 1 10.1186/s13287-019-1471-y 31900237 PMC6941254 · DOI
  64. [75]Hu Y Huang L Shen M Pioglitazone protects compression-mediated apoptosis in nucleus pulposus mesenchymal stem cells by suppressing oxidative stress Oxid Med Cell Longev 2019 2019 4764071 31885796 PMC6893265
  65. [76]Feng J, Li X, Zhu S, et al. Photobiomodulation with 808-nm diode laser enhances gingival wound healing by promoting migration of human gingival mesenchymal stem cells via ROS/JNK/NF-κB/MMP-1 pathway. Lasers Med Sci. 2020; 10.1007/s10103-020-03040-z. Online ahead of print 32451640 · DOI
  66. [77]Varum S Rodrigues AS Moura MB Energy metabolism in human pluripotent stem cells and their differentiated counterparts Plos One 2011 6 6 e20914 10.1371/journal.pone.0020914 21698063 PMC3117868 · DOI · Paper page
  67. [78]Wang W Zhang Y Lu W Liu K Mitochondrial reactive oxygen species regulate adipocyte differentiation of mesenchymal stem cells in hematopoietic stress induced by arabinosylcytosine Plos One 2015 10 3 e0120629 10.1371/journal.pone.0120629 25768922 PMC4359087 · DOI
  68. [79]Prigione A Fauler B Lurz R Lehrach H Adjaye J The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells Stem Cells. 2010 28 4 721 33 10.1002/stem.404 20201066 · DOI
  69. [80]Atashi F Modarressi A Pepper MS The role of reactive oxygen species in mesenchymal stem cell adipogenic and osteogenic differentiation: a review Stem Cells Dev. 2015 24 10 1150 63 10.1089/scd.2014.0484 25603196 PMC4424969 · DOI
  70. [81]Tangtrongsup S Kisiday JD Modulating the oxidative environment during mesenchymal stem cells chondrogenesis with serum increases collagen accumulation in agarose culture J Orthop Res. 2018 36 1 506 14 28548680
  71. [82]Babizhayev MA Yegorov YE Tissue formation and tissue engineering through host cell recruitment or a potential injectable cell-based biocomposite with replicative potential: molecular mechanisms controlling cellular senescence and the involvement of controlled transient telomerase activation therapies J Biomed Mater Res A. 2015 103 12 3993 4023 10.1002/jbm.a.35515 26034007 · DOI
  72. [83]Chen PM Lin CH Li NT c-Maf regulates pluripotency genes, proliferation/self-renewal, and lineage commitment in ROS-mediated senescence of human mesenchymal stem cells Oncotarget. 2015 6 34 35404 18 10.18632/oncotarget.6178 26496036 PMC4742114 · DOI
  73. [84]Jin HJ Lee HJ Heo J Senescence-Associated MCP-1 Secretion Is Dependent on a Decline in BMI1 in Human Mesenchymal Stromal Cells Antioxid Redox Signal. 2016 24 9 471 85 10.1089/ars.2015.6359 26573462 PMC4800271 · DOI
  74. [85]Gu Y Li T Ding Y Changes in mesenchymal stem cells following long-term culture in vitro Mol Med Rep. 2016 13 6 5207 15 10.3892/mmr.2016.5169 27108540 · DOI
  75. [86]Zheng Q Zhao Y Guo J Iron overload promotes mitochondrial fragmentation in mesenchymal stromal cells from myelodysplastic syndrome patients through activation of the AMPK/MFF/Drp1 pathway Cell Death Dis. 2018 9 5 515 10.1038/s41419-018-0552-7 29725013 PMC5938711 · DOI
  76. [87]Chen Y Xiong S Zhao F Effect of magnesium on reducing the UV-induced oxidative damage in marrow mesenchymal stem cells J Biomed Mater Res A. 2019 107 6 1253 63 10.1002/jbm.a.36634 30701665 · DOI
  77. [88]Oh JY Choi GE Lee HJ 17β-Estradiol protects mesenchymal stem cells against high glucose-induced mitochondrial oxidants production via Nrf2/Sirt3/MnSOD signaling Free Radic Biol Med. 2019 130 328 42 10.1016/j.freeradbiomed.2018.11.003 30412732 · DOI
  78. [89]Li CJ Chen PK Sun LY Pang CY Enhancement of Mitochondrial Transfer by Antioxidants in Human Mesenchymal Stem Cells Oxid Med Cell Longev. 2017 2017 8510805 28596814 PMC5449759
  79. [90]Stannard GA Heather LC Hypoxia-inducible factor 1 signalling, metabolism and its therapeutic potential in cardiovascular disease Biochim Biophys Acta Mol Basis Dis. 2019 1865 4 831 43 10.1016/j.bbadis.2018.09.024 30266651 · DOI
  80. [91]Mahato B Home P Rajendran G Regulation of mitochondrial function and cellular energy metabolism by protein kinase C-λ/ι: a novel mode of balancing pluripotency Stem Cells. 2014 32 11 2880 92 10.1002/stem.1817 25142417 PMC4198455 · DOI
  81. [92]Li B Li C Zhu M Hypoxia-induced mesenchymal stromal cells exhibit an enhanced therapeutic effect on radiation-induced lung injury in mice due to an increased proliferation potential and enhanced antioxidant ability Cell Physiol Biochem. 2017 44 4 1295 310 10.1159/000485490 29183009 · DOI
  82. [93]Contreras-Lopez R Elizondo-Vega R Paredes MJ HIF1α-dependent metabolic reprogramming governs mesenchymal stem/stromal cell immunoregulatory functions FASEB J. 2020 34 6 8250 64 10.1096/fj.201902232R 32333618 · DOI
  83. [94]Takubo K Nagamatsu G Kobayashi CI Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells Cell Stem Cell. 2013 12 1 49 61 10.1016/j.stem.2012.10.011 23290136 PMC6592822 · DOI
  84. [95]Hsu SH Chen CT Wei YH Inhibitory effects of hypoxia on metabolic switch and osteogenic differentiation of human mesenchymal stem cells Stem Cells. 2013 31 12 2779 88 10.1002/stem.1441 23733376 · DOI
  85. [96]Fujisawa K Hara K Takami T Evaluation of the effects of ascorbic acid on metabolism of human mesenchymal stem cells Stem Cell Res Ther. 2018 9 1 93 10.1186/s13287-018-0825-1 29625581 PMC5889584 · DOI
  86. [97]Alptekin A Ye B Ding HF Transcriptional regulation of stem cell and cancer stem cell metabolism Curr Stem Cell Rep. 2017 3 1 19 27 10.1007/s40778-017-0071-y 28920013 PMC5597247 · DOI
  87. [98]Huang PI Chen YC Chen LH PGC-1α mediates differentiation of mesenchymal stem cells to brown adipose cells J Atheroscler Thromb. 2011 18 11 966 80 10.5551/jat.7401 21817823 · DOI
  88. [99]St-Pierre J Drori S Uldry M Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell. 2006 127 2 397 408 10.1016/j.cell.2006.09.024 17055439 · DOI · Paper page
  89. [100]Katsyuba E Auwerx J Modulating NAD+ metabolism, from bench to bedside EMBO J. 2017 36 18 2670 83 10.15252/embj.201797135 28784597 PMC5599801 · DOI
  90. [101]Wu Y Williams EG Dubuis S Multilayered genetic and omics dissection of mitochondrial activity in a mouse reference population Cell. 2014 158 6 1415 30 10.1016/j.cell.2014.07.039 25215496 PMC4179868 · DOI · Paper page
  91. [103]Lin CH Li NT Cheng HS Yen ML Oxidative stress induces imbalance of adipogenic/osteoblastic lineage commitment in mesenchymal stem cells through decreasing SIRT1 functions J Cell Mol Med. 2018 22 2 786 96 28975701 PMC5783884
  92. [104]Chen H Liu X Chen H Role of SIRT1 and AMPK in mesenchymal stem cells differentiation Ageing Res Rev. 2014 13 55 64 10.1016/j.arr.2013.12.002 24333965 · DOI
  93. [105]Denu RA Hematti P Effects of oxidative stress on mesenchymal stem cell biology Oxid Med Cell Longev. 2016 2016 2989076 10.1155/2016/2989076 27413419 PMC4928004 · DOI
  94. [106]Gao J Feng Z Wang X SIRT3/SOD2 maintains osteoblast differentiation and bone formation by regulating mitochondrial stress Cell Death Differ. 2018 25 2 229 40 10.1038/cdd.2017.144 28914882 PMC5762839 · DOI
  95. [107]Jeong SG Cho GW Trichostatin A modulates intracellular reactive oxygen species through SOD2 and FOXO1 in human bone marrow-mesenchymal stem cells Cell Biochem Funct. 2015 33 1 37 43 10.1002/cbf.3084 25515622 · DOI
  96. [109]Konari N Nagaishi K Kikuchi S Fujimiya M Mitochondria transfer from mesenchymal stem cells structurally and functionally repairs renal proximal tubular epithelial cells in diabetic nephropathy in vivo Sci Rep. 2019 9 1 5184 10.1038/s41598-019-40163-y 30914727 PMC6435708 · DOI
  97. [110]Hardie DG Ross FA Hawley SA AMPK: a nutrient and energy sensor that maintains energy homeostasis Nat Rev Mol Cell Biol. 2012 13 4 251 62 10.1038/nrm3311 22436748 PMC5726489 · DOI · Paper page
  98. [111]Zhao X, Pathak JL, Huang W, et al. Metformin enhances osteogenic differentiation of stem cells from human exfoliated deciduous teeth through AMPK pathway. J Tissue Eng Regen Med. 2020. 10.1002/term.3142. 33049108 · DOI
  99. [112]Kim EK Lim S Park JM Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase J Cell Physiol. 2012 227 4 1680 7 10.1002/jcp.22892 21678424 · DOI
  100. [113]Faubert B, Vincent EE, Poffenberger MC, Jones RG. The AMP-activated protein kinase (AMPK) and cancer: many faces of a metabolic regulator. Cancer Lett. 2015;356(2 Pt A):165-70. 24486219
  101. [114]Pantovic A Krstic A Janjetovic K Coordinated time-dependent modulation of AMPK/Akt/mTOR signaling and autophagy controls osteogenic differentiation of human mesenchymal stem cells Bone. 2013 52 1 524 31 10.1016/j.bone.2012.10.024 23111315 · DOI
  102. [115]Tormos KV Anso E Hamanaka RB Mitochondrial complex III ROS regulate adipocyte differentiation Cell Metab. 2011 14 4 537 44 10.1016/j.cmet.2011.08.007 21982713 PMC3190168 · DOI
  103. [117]Cedikova M Kripnerová M Dvorakova J Mitochondria in white, brown, and beige adipocytes Stem Cells Int. 2016 2016 6067349 10.1155/2016/6067349 27073398 PMC4814709 · DOI
  104. [118]Merlin J Sato M Chia LY Rosiglitazone and a β3-adrenoceptor agonist are both required for functional browning of white adipocytes in culture Front Endocrinol (Lausanne). 2018 9 249 10.3389/fendo.2018.00249 29910772 PMC5992408 · DOI
  105. [119]Michurina S Stafeev I Podkuychenko N Decreased UCP-1 expression in beige adipocytes from adipose-derived stem cells of type 2 diabetes patients associates with mitochondrial ROS accumulation during obesity Diabetes Res Clin Pract. 2020 169 108410 10.1016/j.diabres.2020.108410 32882342 · DOI
  106. [120]Di Somma M Schaafsma W Grillo E Natural histogel-based bio-scaffolds for sustaining angiogenesis in beige adipose tissue Cells. 2019 8 11 1457 10.3390/cells8111457 PMC6912328 31752157 · DOI
  107. [121]Andrews ZB Diano S Horvath TL Mitochondrial uncoupling proteins in the CNS: in support of function and survival Nat Rev Neurosci. 2005 6 11 829 40 10.1038/nrn1767 16224498 · DOI

Cited by

Sorted by citations

Authors
Yan, W., Diao, S., & Fan, Z.
Affiliations
Capital Medical University (CN)
Corresponding author
Fan, Zhipeng
Venue
Stem Cell Research & Therapy
Published
2021-02-17
Volume
12
Issue
1
Pages
140-140
ISSN
1757-6512 (ISSN-L)
OpenAlex
W3129300023
Cited by
167
References
14
Citations by year
2026: 34 · 2025: 44 · 2024: 34 · 2023: 35 · 2022: 15 · 2021: 5
FWCI
3.17
Type
journal article
Language
en
Open access
Locations
  • Stem Cell Research & Therapy (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Sciences Foundation of China (81625005, 81800923)
  • CAMS Innovation Fund for Medical Sciences (2019-I2M-5-031)
  • Program from Beijing Key Laboratory of Tooth Regeneration and Function Reconstruction (KFKT2019012)
Topics
  • Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Keywords
mesenchymal stem cells, mitochondria, mitochondrial bioenergetics, mitochondrial dynamics, mitochondrial morphology, mitochondrial transfer, stem cell differentiation, stem cell aging, apoptosis, cell therapy
MeSH terms
Cell Differentiation, Energy Metabolism, Mitochondria, Mesenchymal Stem Cell Transplantation, Mesenchymal Stem Cells, Cell- and Tissue-Based Therapy

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review