1,042
Views
0
CrossRef citations to date
0
Altmetric
Expert Opinion

Considerations for Developing Mitochondrial Transplantation Techniques for Individualized Medicine

, , , , , & ORCID Icon show all
Pages 125-134 | Received 09 Aug 2023, Accepted 06 Feb 2024, Published online: 29 Feb 2024

References

  • Monzel AS , EnríquezJA , PicardM. Multifaceted mitochondria: moving mitochondrial science beyond function and dysfunction. Nat. Metab.5(4), 546–562 (2023).
  • Neikirk K , VueZ , KattiPet al. Systematic transmission electron microscopy-based identification and 3D reconstruction of cellular degradation machinery. Adv. Biol.7(6), 2200221 (2023).
  • Gorman GS , ChinneryPF , DiMauroSet al. Mitochondrial diseases. Nat. Rev. Dis. Primers2(1), 1–22 (2016).
  • Gäbelein CG , FengQ , SarajlicEet al. Mitochondria transplantation between living cells. PLOS Biol.20(3), e3001576 (2022).
  • Clark MA , ShayJW. Mitochondrial transformation of mammalian cells. Nature295(5850), 605–607 (1982).
  • King MP , AttardiG. Injection of mitochondria into human cells leads to a rapid replacement of the endogenous mitochondrial DNA. Cell52(6), 811–819 (1988).
  • McCully JD , LevitskyS , del NidoPJ , CowanDB. Mitochondrial transplantation for therapeutic use. Clin. Transl. Med.5, 16 (2016).
  • McCully JD , CowanDB , PacakCA , ToumpoulisIK , DayalanH , LevitskyS. Injection of isolated mitochondria during early reperfusion for cardioprotection. Am. J. Physiol.-Heart Circul. Physiol.296(1), H94–H105 (2009).
  • Gomzikova MO , JamesV , RizvanovAA. Mitochondria donation by mesenchymal stem cells: current understanding and mitochondria transplantation strategies. Front. Cell Developm. Biol.653322, 9 (2021).
  • Melanie Walker . University of Washington. Washington U of. “Autologous Mitochondrial Transplant for Cerebral Ischemia: Cerebral Ischemia Clinical Trial…” (2023). https://trialbulletin.com/lib/entry/ct-04998357
  • Yamada Y , ItoM , AraiM , HibinoM , TsujiokaT , HarashimaH. Challenges in promoting mitochondrial transplantation therapy. Int. J. Mol. Sci.21(17), 6365 (2020).
  • Fu A , ShiX , ZhangH , FuB. Mitotherapy for fatty liver by intravenous administration of exogenous mitochondria in male mice. Front. Pharmacol.241, 8 (2017).
  • Gollihue JL , PatelSP , MashburnC , EldahanKC , SullivanPG , RabchevskyAG. Optimization of mitochondrial isolation techniques for intraspinal transplantation procedures. J. Neurosci. Methods287, 1–12 (2017).
  • Yu Z , HouY , ZhouW , ZhaoZ , LiuZ , FuA. The effect of mitochondrial transplantation therapy from different gender on inhibiting cell proliferation of malignant melanoma. Int. J. Biolog. Sci.17, 2021–2033 (2021).
  • Wang Z-H , ChenL , LiW , ChenL , WangY-P. Mitochondria transfer and transplantation in human health and diseases. Mitochondrion65, 80–87 (2022).
  • Martin CR , PreedyVR , RajendramR. Assessments, Treatments and Modeling in Aging and Neurological Disease: The Neuroscience of Aging.Academic Press, MA, USA (2021).
  • Wu G-H , Smith-GeaterC , Galaz-MontoyaJGet al. CryoET reveals organelle phenotypes in Huntington disease patient iPSC-derived and mouse primary neurons. Nat. Commun.14(1), 692 (2023).
  • Shirendeb UP , CalkinsMJ , ManczakMet al. Mutant huntingtin’s interaction with mitochondrial protein Drp1 impairs mitochondrial biogenesis and causes defective axonal transport and synaptic degeneration in Huntington’s disease. Hum. Mol. Genet.21(2), 406–420 (2012).
  • Guo X , DisatnikM-H , MonbureauM , ShamlooM , Mochly-RosenD , QiX. Inhibition of mitochondrial fragmentation diminishes Huntington’s disease–associated neurodegeneration. J. Clin. Invest.123(12), 5371–5388 (2013).
  • Ryu J , KimJ , ChoS-Jet al. Proactive transplantation of human neural stem cells prevents degeneration of striatal neurons in a rat model of Huntington disease. Neurobiol. Dis.16, 68–77 (2004).
  • Shi X , ZhaoM , FuC , FuA. Intravenous administration of mitochondria for treating experimental Parkinson’s disease. Mitochondrion34, 91–100 (2017).
  • Lightowlers RN , Chrzanowska-LightowlersZM , RussellOM. Mitochondrial transplantation – a possible therapeutic for mitochondrial dysfunction?EMBO Reports21(9), e50964 (2020).
  • Headley CA , TsaoPS. Building the case for mitochondrial transplantation as an anti-aging cardiovascular therapy. Front. Cardiovasc. Med.1141124, 10 (2023).
  • Saeb-Parsy K , MartinJL , SummersDM , WatsonCJE , KriegT , MurphyMP. Mitochondria as therapeutic targets in transplantation. Trend. Mol. Med.27(2), 185–198 (2021).
  • D’Amato M , MorraF , DiMeo I , TirantiV. Mitochondrial transplantation in mitochondrial medicine: current challenges and future perspectives. Int. J. Mol. Sci.24(3), 1969 (2023).
  • Liu Z , SunY , QiZ , CaoL , DingS. Mitochondrial transfer/transplantation: an emerging therapeutic approach for multiple diseases. Cell Biosci.12(1), 66 (2022).
  • Nakamura Y , LoEH , HayakawaK. Placental mitochondria therapy for cerebral ischemia-reperfusion injury in mice. Stroke51(10), 3142–3146 (2020).
  • Djafarzadeh S , JakobSM. Isolation of intact mitochondria from skeletal muscle by differential centrifugation for high-resolution respirometry measurements. J. Vis. Exp. (121), e55251 10.3791/55251 (2017).
  • Zhang T , MiaoC. Mitochondrial transplantation as a promising therapy for mitochondrial diseases. Acta Pharmaceut. Sinica B13(3), 1028–1035 (2023).
  • Caicedo A , ApontePM , CabreraF , HidalgoC , KhouryM. Artificial mitochondria transfer: current challenges, advances, and future applications. Stem Cells Int.2017, e7610414 (2017).
  • Chang J-C , WuS-L , LiuK-Het al. Allogeneic/xenogeneic transplantation of peptide-labeled mitochondria in Parkinson’s disease: restoration of mitochondria functions and attenuation of 6-hydroxydopamine-induced neurotoxicity. Transl. Res.170, 40–56.e3 (2016).
  • Bobkova NV , ZhdanovaDY , BelosludtsevaNV , PenkovNV , MironovaGD. Intranasal administration of mitochondria improves spatial memory in olfactory bulbectomized mice. Exp. Biol. Med.247(5), 416–425 (2022).
  • Wang Z-B , HaoJ-X , MengT-Get al. Transfer of autologous mitochondria from adipose tissue-derived stem cells rescues oocyte quality and infertility in aged mice. Aging9(12), 2480–2488 (2017).
  • Masuzawa A , BlackKM , PacakCAet al. Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury. Am. J. Physiol.-Heart Circulat. Physiol.304(7), H966–H982 (2013).
  • Yang Y-W , KoobMD. Transferring isolated mitochondria into tissue culture cells. Nucleic Acids Res.40(19), e148 (2012).
  • Cabrera F , OrtegaM , VelardeFet al. Primary allogeneic mitochondrial mix (PAMM) transfer/transplant by MitoCeption to address damage in PBMCs caused by ultraviolet radiation. BMC Biotechnol.19(1), 42 (2019).
  • Mishra M , RaikS , RattanV , BhattacharyyaS. Mitochondria transfer as a potential therapeutic mechanism in Alzheimer’s disease-like pathology. Brain Res.1819, 148544 (2023).
  • Macheiner T , FenglerVHI , AgreiterMet al. Magnetomitotransfer: an efficient way for direct mitochondria transfer into cultured human cells. Sci. Rep.6(1), 35571 (2016).
  • Caicedo A , FritzV , BrondelloJ-Met al. MitoCeption as a new tool to assess the effects of mesenchymal stem/stromal cell mitochondria on cancer cell metabolism and function. Sci. Rep.5(1), 9073 (2015).
  • Wu T-H , SagulloE , CaseDet al. Mitochondrial transfer by photothermal nanoblade restores metabolite profile in mammalian cells. Cell Metabol.23(5), 921–929 (2016).
  • Wu Y-C , WuT-H , ClemensDLet al. Massively parallel delivery of large cargo into mammalian cells with light pulses. Nat. Methods12(5), 439–444 (2015).
  • Chang J-C , HoelF , LiuK-Het al. Peptide-mediated delivery of donor mitochondria improves mitochondrial function and cell viability in human cybrid cells with the MELAS A3243G mutation. Sci. Rep.7(1), 10710 (2017).
  • Wu S , ZhangA , LiSet al. Polymer functionalization of isolated mitochondria for cellular transplantation and metabolic phenotype alteration. Adv. Sci.5(3), 1700530 (2018).
  • Bodenstein DF , PowlowskiP , ZachosKAet al. Optimization of differential filtration-based mitochondrial isolation for mitochondrial transplant to cerebral organoids. Stem Cell Res. Ther.14(1), 202 (2023).
  • Liao P-C , BergaminiC , FatoR , PallottiF. Chapter 1 – Isolation of mitochondria from cells and tissues. In: Methods in Cell Biology (Volume 155).SchonEA, PonLA ( Eds). Academic Press, MA, USA, 3–31 (2020).
  • Caldeira D de AF , de OliveiraDF , Cavalcanti-de-AlbuquerqueJP , NascimentoJHM , ZinWA , MacielL. Isolation of mitochondria from fresh mice lung tissue. Front. Physiol.748261, 12 (2021).
  • Hornig-Do H-T , GüntherG , BustM , LehnartzP , BosioA , WiesnerRJ. Isolation of functional pure mitochondria by superparamagnetic microbeads. Anal. Biochem.389(1), 1–5 (2009).
  • Bury AG , VincentAE , TurnbullDM , ActisP , HudsonG. Mitochondrial isolation: when size matters. Wellcome Open Res.5, 226 (2020).
  • Hirschenson J , Melgar-BermudezE , MaillouxRJ. The uncoupling proteins: a systematic review on the mechanism used in the prevention of oxidative stress. Antioxidants11(2), 322 (2022).
  • Chan SHH , WuC-A , WuKLH , HoY-H , ChangAYW , ChanJYH. Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ. Res.105(9), 886–896 (2009).
  • Tzameli I . The evolving role of mitochondria in metabolism. Trends Endocrinol. Metab.23(9), 417–419 (2012).
  • Kidwell CU , CasaliniJR , PradeepSet al. Transferred mitochondria accumulate reactive oxygen species, promoting proliferation. Elife12, e85494 (2023).
  • Jia X , WangQ , JiJet al. Mitochondrial transplantation ameliorates hippocampal damage following status epilepticus. Animal Models Exp. Med.6(1), 41–50 (2023).
  • Chang J-C , ChangH-S , WuY-Cet al. Mitochondrial transplantation regulates antitumour activity, chemoresistance and mitochondrial dynamics in breast cancer. J. Exp. Clin. Cancer Res.38(1), 30 (2019).
  • Brand MD , GoncalvesRLS , OrrALet al. Suppressors of superoxide-H2O2 production at site IQ of mitochondrial complex I protect against stem cell hyperplasia and ischemia-reperfusion injury. Cell Metab.24(4), 582–592 (2016).
  • Aharoni-Simon M , Ben-YaakovK , Sharvit-BaderMet al. Oxidative stress facilitates exogenous mitochondria internalization and survival in retinal ganglion precursor-like cells. Sci. Rep.12(1), 5122 (2022).
  • Chan DC . Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet.46, 265–287 (2012).
  • Zhu L , ZhangJ , ZhouJet al. Mitochondrial transplantation attenuates hypoxic pulmonary hypertension. Oncotarget7(31), 48925–48940 (2016).
  • Ali Pour P , KenneyMC , KheradvarA. Bioenergetics consequences of mitochondrial transplantation in cardiomyocytes. J. Am. Heart Assoc.9(7), e014501 (2020).
  • Chang J-C , LiuK-H , LiY-Cet al. Functional recovery of human cells harbouring the mitochondrial DNA mutation MERRF A8344G via peptide-mediated mitochondrial delivery. Neurosignals21(3–4), 160–173 (2012).
  • Barrera M , KoobS , DikovD , VogelF , ReichertAS. OPA1 functionally interacts with MIC60 but is dispensable for crista junction formation. FEBS Lett.590(19), 3309–3322 (2016).
  • Vue Z , NeikirkK , VangLet al. Three-dimensional mitochondria reconstructions of murine cardiac muscle changes in size across aging. Am. J. Physiol.-Heart Circulat. Physiol.325(5), H965–H982 (2023).
  • Elorza AA , SoffiaJP. mtDNA heteroplasmy at the core of aging-associated heart failure. an integrative view of OXPHOS and mitochondrial life cycle in cardiac mitochondrial physiology. Front. Cell Develop. Biol.625020, 9 (2021).
  • Lechuga-Vieco AV , Latorre-PellicerA , CalvoEet al. Heteroplasmy of wild-type mitochondrial DNA variants in mice causes metabolic heart disease with pulmonary hypertension and frailty. Circulation145(14), 1084–1101 (2022).
  • Pereira CV , GitschlagBL , PatelMR. Cellular mechanisms of mtDNA heteroplasmy dynamics. Crit. Rev. Biochem. Mol. Biol.56(5), 510–525 (2021).
  • Vyas CM , OgataS , IiiCFRet al. Lifestyle and behavioral factors and mitochondrial DNA copy number in a diverse cohort of mid-life and older adults. PLOS ONE15(8), e0237235 (2020).
  • Brenner C , BarrittJ , WilladsenS , CohenJ. Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil. Steril.74(3), 573–578 (2000).
  • Morimoto Y , GamageUSK , YamochiTet al. Mitochondrial transfer into human oocytes improved embryo quality and clinical outcomes in recurrent pregnancy failure cases. Int. J. Mol. Sci.24(3), 2738 (2023).
  • Maeda H , KamiD , MaedaR , ShikumaA , GojoS. Generation of somatic mitochondrial DNA-replaced cells for mitochondrial dysfunction treatment. Sci. Rep.11(1), 10897 (2020).
  • Hashimoto M , BacmanSR , PeraltaSet al. MitoTALEN: a general approach to reduce mutant mtDNA loads and restore oxidative phosphorylation function in mitochondrial diseases. Mol. Ther.23(10), 1592–1599 (2015).
  • Lin L , XuH , BishawiMet al. Circulating mitochondria in organ donors promote allograft rejection. Am. J. Transplant.19(7), 1917–1929 (2019).
  • Cogliati S , EnriquezJA , ScorranoL. Mitochondrial cristae: where beauty meets functionality. Trends Biochem. Sci.41(3), 261–273 (2016).
  • Glancy B , KimY , KattiP , WillinghamTB. The functional impact of mitochondrial structure across subcellular scales. Front. Physiol.11, 541040 (2020).
  • Lam J , KattiP , BieteMet al. A universal approach to analyzing transmission electron microscopy with ImageJ. Cells10(9), 2177 (2021).
  • Neikirk K , LopezE-G , MarshallAGet al. Call to action to properly utilize electron microscopy to measure organelles to monitor disease. Eur. J. Cell Biol.102(4), 151365 (2023).
  • Hinton A , KattiP , ChristensenTAet al. A Comprehensive approach to sample preparation for electron microscopy and the assessment of mitochondrial morphology in tissue and cultured cells. Adv. Biol.7(10), e2200202 (2023).
  • Wakabayashi T . Megamitochondria formation - physiology and pathology. J. Cell Mol. Med.6(4), 497–538 (2002).
  • Garza-Lopez E , VueZ , KattiPet al. Protocols for generating surfaces and measuring 3d organelle morphology using amira. Cells11(1), 65 (2022).
  • Marshall AG , NeikirkK , StephensDCet al. Serial block face-scanning electron microscopy as a burgeoning technology. Adv. Biol.e2300139 (2023).
  • Marshall AG , DamoSM , HintonA. Revisiting focused ion beam scanning electron microcopy. Trends Biochem. Sci.48(6), 585–586 (2023).
  • Kleele T , ReyT , WinterJet al. Distinct fission signatures predict mitochondrial degradation or biogenesis. Nature593(7859), 435–439 (2021).
  • Giacomello M , PellegriniL. The coming of age of the mitochondria–ER contact: a matter of thickness. Cell Death Different.23(9), 1417–1427 (2016).
  • Ma X , QianH , ChenA , NiH-M , DingW-X. Perspectives on mitochondria–ER and mitochondria–lipid droplet contact in hepatocytes and hepatic lipid metabolism. Cells10(9), 2273 (2021).
  • Nichtová Z , Fernandez-SanzC , DeLa Fuente Set al. Enhanced mitochondria-SR tethering triggers adaptive cardiac muscle remodeling. Circ. Res.132(11), e171–e187 (2023).
  • Vue Z , Garza-LopezE , NeikirkKet al. 3D reconstruction of murine mitochondria reveals changes in structure during aging linked to the MICOS complex. Aging Cell22(12), e14009 (2023).
  • Crabtree A , NeikirkK , MarshallAGet al. Defining mitochondrial cristae morphology changes induced by aging in brown adipose tissue. Adv. Biol.8(1), e2300186 (2023).
  • Schaum N , LehallierB , HahnOet al. Ageing hallmarks exhibit organ-specific temporal signatures. Nature583(7817), 596–602 (2020).
  • Liu D , GaoY , LiuJet al. Intercellular mitochondrial transfer as a means of tissue revitalization. Sig. Transduct. Target Ther.6(1), 1–18 (2021).
  • Capelluto F , AlbericoH , Ledo-HopgoodP , TillyJ , WoodsD. Lineage-mismatched mitochondrial replacement in an inducible mitochondrial depletion model effectively restores the original proteomic landscape of recipient cells. Advan. Biol.7(6), e2200246 (2023).
  • Lin M-W , FangS-Y , HsuJet al. Mitochondrial transplantation attenuates neural damage and improves locomotor function after traumatic spinal cord injury in rats. Front. Neurosci.16, 800883 (2022).
  • Sun X , ChenH , GaoRet al. Intravenous transplantation of an ischemic-specific peptide-TPP-mitochondrial compound alleviates myocardial ischemic reperfusion injury. ACS Nano17, 896–909 (2023).
  • Wang X , GerdesH-H. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ.22(7), 1181–1191 (2015).
  • Todkar K , ChikhiL , DesjardinsV , El-MortadaF , PépinG , GermainM. Selective packaging of mitochondrial proteins into extracellular vesicles prevents the release of mitochondrial DAMPs. Nat. Commun.12(1), 1971 (2021).
  • Singh AK , GolanK , AlthoffMJet al. Connexin-43 Is a negative regulator of mitochondrial fission, mitophagy and apoptosis of dividing hematopoietic stem cells through the Drp1-Pink1 axis. Blood132(Suppl. 1), 639 (2018).
  • Cetin-Ferra S , FrancisSC , CooperATet al. Mitochondrial connexins and mitochondrial contact sites with gap junction structure. Inter. J. Mol. Sci.24(10), 9036 (2023).
  • Fairley LH , GrimmA , EckertA. Mitochondria transfer in brain injury and disease. Cells11(22), 3603 (2022).
  • Hwang JW , LeeMJ , ChungTNet al. The immune modulatory effects of mitochondrial transplantation on cecal slurry model in rat. Crit. Care25, 20 (2021).
  • Kesner EE , Saada-ReichA , Lorberboum-GalskiH. Characteristics of mitochondrial transformation into human cells. Sci. Rep.6, 26057 (2016).
  • Zhang B , GaoY , LiQet al. Effects of brain-derived mitochondria on the function of neuron and vascular endothelial cell after traumatic brain injury. World Neurosurg.138, e1–e9 (2019).
  • Chang J-C , ChaoY-C , ChangH-Set al. Intranasal delivery of mitochondria for treatment of Parkinson’s Disease model rats lesioned with 6-hydroxydopamine. Sci. Rep.11(1), 10597 (2021).
  • Norat P , SokolowskiJD , GorickCMet al. Intraarterial transplantation of mitochondria after ischemic stroke reduces cerebral infarction. Stroke: Vasc. Intervent. Neurol.3(3), e000644 (2023).
  • Kshersagar J , PulgamL , DamleMN , TardalkarK , SharmaR , JoshiMG. Transplantation of human placenta derived mitochondria promotes cell communication in endometrium in a murine model of disturbed endometrium. Stem Cell Rev. Rep.19(5), 1384–1401 (2023).
  • Bell JAH , SchmilovichZ , BuchmanDZ , EscafM , CostelloJ , MessnerHA. First ready, first to go: ethical priority-setting of allogeneic stem cell transplant at a major cancer centre. Health Policy15(3), 102–115 (2020).