Horizontal transfer of mitochondria

Short description: Movement of whole mitochondria between cells

Horizontal transfer of mitochondria is the movement of whole mitochondria and mitochondrial DNA between cells. Mitochondria from donor cells are transported and incorporated into the endogenous mitochondrial network of recipient cells contributing to changes in the bioenergetics profile and in other functional properties of recipient cells.[1] Horizontal cell-to-cell transfer of mitochondria and mitochondrial genome can occur among mammalian cells in vitro and in vivo.[2] Mitochondrial transfer supports the exogenous replacement of damaged mitochondria, thereby rescuing mitochondrial defects.[3][4] Stem cells, immortalized cells or primary cells are usually used as mitochondrial donors in most studies.[2] These cells may transfer mitochondria to surrounding cells in their niche, thus affecting cell differentiation, proliferation, tissue homeostasis, development and ageing.[1]

## Contents

* 1 Mechanism
* 2 In vitro transfer
* 3 In vivo transfer
* 4 Cancer
* 5 References

## Mechanism

Horizontal transfer of mitochondria is mediated by actin-rich membrane protrusions named tunneling nanotubes (TNTs).[5] The establishment of a nanotube begins with the formation of a filopodium-like membrane protrusion that retracts after reaching the recipient cell, leaving an ultrafine structure that is separated from the substrate.[1] Chemical inhibitors or mechanical stress impairs the formation of TNTs and reduces mitochondrial exchange.[1][6] On the other hand, certain types of stress agents such as doxorubicin[7] or ethidium bromide[8] increase TNT formation. Other proposed mechanisms of transfer include membrane microvesicles, cell fusion, dendrites, and mitochondrial extrusion.[1][9]

## In vitro transfer

The first evidence of functional mitochondrial transfer in vitro has been documented between human mesenchymal stem cells (hMSCs) and human lung carcinoma cells. Healthy mitochondria from hMSCs moved to recipient lung carcinoma cells with nonfunctional mitochondria and repaired their function.[10] Intercellular transfer of mitochondria in culture has been documented from MSCs and endothelial cells to breast cancer cell lines, ovarian cancer cell lines or to osteosarcoma cell line.[11] Mitochondrial transfer can occur also between cancer cells such as mesothelioma[12] and laryngeal carcinoma cells.[13] Non-tumor cells such as human renal epithelial cells, human retinal pigment epithelial cells or human monocyte-derived macrophages have been shown to transfer their mitochondria as well.[14] All these data suggest that this phenomenon, regardless of the exact mechanisms involved, may be a fundamental physiological process well worthwhile exploring in a whole organism setting.

## In vivo transfer

One of the first evidences of in vivo horizontal mitochondrial gene transfer was found in a transmissible canine venereal tumor (CTVT), highly adapted cancer transmitted during mating of feral dogs. Phylogenetic analyses of mitochondrial sequences revealed that CTVT cells periodically acquire mitochondria from its host and ensure overcoming high mutation rate that would promote the accumulation of deleterious mutations in their own mitochondria and long-term survival.[15] Transfer of intact mitochondria can contribute to tissue repair in vivo. Bone marrow-derived stem cells (BMSCs) injected into mice with acute lung injury transfer their mitochondria to lung alveoli cells and protect them against injury.[16] Overexpression of Miro1, a protein connecting mitochondria to cytoskeletal motor proteins, leads to enhanced transfer of mitochondria from MSCs into stressed epithelial cells via TNTs in mice.[17] In vivo horizontal transfer of mitochondria can occur in cancer cells which upon mitochondrial damage acquire mtDNA from surrounding donor healthy cells. This process restores transcription and translation of mtDNA-encoded genes as well as respiration.[18]

Injured neurons cannot be quickly replaced after ischemia without transfer of mitochondria from other cells.[19] Transfer of functional mitochondria from astrocytes to ischemically-damaged neurons has been shown to promote recovery in the brain.[9][19] Stem cells are also a source of mitochondria for ischemic brain cells.[19]

## Cancer

Mitochondrial transfer occurs between tumor cells and other cells of the cancer microenvironment. Highly glycolytic cancer-associated fibroblasts donate their disposable mitochondria to adjacent prostate cancer cells enhancing the respiratory capacity of the cancer cells.[9] Mitochondrial transfer in cancer cells contributes to chemotherapy resistance.[9]

## References

1. ↑ 1.0 1.1 1.2 1.3 1.4 Torralba, D.; Baixauli, F.; Sánchez-Madrid, F. (2016). "Mitochondria know no boundaries: Mechanisms and functions of intercellular mitochondrial transfer". Frontiers in Cell and Developmental Biology 4: 107. doi:10.3389/fcell.2016.00107. PMID 27734015.
2. ↑ 2.0 2.1 Berridge, M.V; McConnell, M.J; Grasso, C.; Bajzikova, M.; Kovarova, J.; Neuzil, J. (2016). "Horizontal transfer of mitochondria between mammalian cells: beyond co-culture approaches". Current Opinion in Genetics & Development 38: 75–82. doi:10.1016/j.gde.2016.04.003. PMID 27219870.
3. ↑ Patananan, A.N; Wu, T.H.; Chiou, P.Y.; Teitell, M. A. (2016). "Modifying the Mitochondrial Genome". Cell Metabolism 23 (5): 785–796. doi:10.1016/j.cmet.2016.04.004. PMID 27166943.
4. ↑ Hayakawa, K.; Esposito, E.; Wang, X.; Terasaki, Y.; Liu, Y.; Xing, Ch.; Ji, X.; Lo, E.H. (2016). "Transfer of mitochondria from astrocytes to neurons after stroke". Nature 535 (7613): 551–555. doi:10.1038/nature18928. PMID 27466127. Bibcode: 2016Natur.535..551H.
5. ↑ Rustom, A.; Saffrich, R.; Markovic, I.; Walther, P.; Gerdes, H.H (2004). "Nanotubular highways for intercellular organelle transport". Science 303 (5660): 1007–1010. doi:10.1126/science.1093133. PMID 14963329. Bibcode: 2004Sci...303.1007R.
6. ↑ Bukoreshtliev, N.V.; Wang, X.; Hodneland, E.; Gurke, S.; Barroso, J.F.V.; Gerdes, H.H (2009). "Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells". FEBS Letters 583 (9): 1481–1488. doi:10.1016/j.febslet.2009.03.065. PMID 19345217.
7. ↑ Yasuda, K.; Park, H.Ch.; Ratliff, B.; Addabbo, F.; Hatzopoulos, A.K.; Chander, P.; Goligorsky, M.S. (2010). "Adriamycin Nephropathy". The American Journal of Pathology 176 (4): 1685–1695. doi:10.2353/ajpath.2010.091071. PMID 20167859.
8. ↑ Cho, Y.M.; Kim, J.H.; Kim, M.; Park, S.J.; Koh, S.H.; Ahn, H.S.; Kang, G.H.; Lee, J.B et al. (2012). "Mesenchymal Stem Cells Transfer Mitochondria to the Cells with Virtually No Mitochondrial Function but Not with Pathogenic mtDNA Mutations". PLOS ONE 7 (3): e32778. doi:10.1371/journal.pone.0032778. PMID 22412925. Bibcode: 2012PLoSO...732778C.
9. ↑ 9.0 9.1 9.2 9.3 "Intercellular mitochondrial transfer as a means of tissue revitalization". Signal Transduction and Targeted Therapy 6 (1): 65. 2021. doi:10.1038/s41392-020-00440-z. PMID 33589598.
10. ↑ Spees, J.L; Olson, S.D; Whitney, M.J; Prockop, D.J (2006). "Mitochondrial transfer between cells can rescue aerobic respiration". Proc Natl Acad Sci USA 103 (5): 1283–1288. doi:10.1073/pnas.0510511103. PMID 16432190. Bibcode: 2006PNAS..103.1283S.
11. ↑ Neuzil, J.; Dong, L.; Berridge, M.V. (2015). "Mitochondrial DNA in Tumor Initiation, Progression, and Metastasis: Role of Horizontal mtDNA Transfer" (in en). Cancer Research 75 (16): 3203–3208. doi:10.1158/0008-5472.CAN-15-0859. ISSN 0008-5472. http://cancerres.aacrjournals.org/content/75/16/3203.
12. ↑ Lou, E.; Fujisawa, S.; Morozov, A.; Barlas, A.; Romin, Y.; Dogan, Y.; Gholami, S.; Moreira, A.L. et al. (2012). "Tunneling Nanotubes Provide a Unique Conduit for Intercellular Transfer of Cellular Contents in Human Malignant Pleural Mesothelioma". PLOS ONE 7 (3): e33093. doi:10.1371/journal.pone.0033093. PMID 22427958. Bibcode: 2012PLoSO...733093L.
13. ↑ Antanavičiūtė, I.; Rysevaitė, K.; Liutkevičius, V.; Marandykina, A.; Rimkutė, L.; Sveikatienė, R.; Uloza, V.; Skeberdis, V. et al. (2014). "Long-Distance Communication between Laryngeal Carcinoma Cells". PLOS ONE 9 (6): e99196. doi:10.1371/journal.pone.0099196. PMID 24945745. Bibcode: 2014PLoSO...999196A.
14. ↑ Caicedo, A.; Aponte, P.M.; Cabrera, F.; Hidalgo, C.; Khoury, M. (2017). "Artificial Mitochondria Transfer: Current Challenges, Advances, and Future Applications". Stem Cells International 2017: 1–23. doi:10.1155/2017/7610414. PMID 28751917.
15. ↑ Rebbeck, C.A; Leroi, A.M; Burt, A. (2011). "Mitochondrial capture by a transmissible cancer". Science 331 (6015): 303. doi:10.1126/science.1197696. PMID 21252340. Bibcode: 2011Sci...331..303R.
16. ↑ Islam, M.N; Das, S.R; Emin, M.T; Wei, M.; Sun, L.; Westphalen, K.; Rowlands, D.J; Quadri, S.K et al. (2012). "Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury". Nature Medicine 18 (5): 759–765. doi:10.1038/nm.2736. PMID 22504485.
17. ↑ Ahmad, T.Expression error: Unrecognized word "et". (2014). "Miro1 regulates intercellular mitochondrial transport and enhances mesenchymal stem cell rescue efficacy". EMBO J 33 (9): 994–1010. doi:10.1002/embj.201386030. PMID 24431222.
18. ↑ Tan, A.S; Baty, J.W; Dong, L.F; Bezawork-Geleta, A.; Endaya, B.; Goodwin, J.; Bajzikova, M.; Kovarova, J. et al. (2015). "Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA". Cell Metabolism 21 (1): 81–91. doi:10.1016/j.cmet.2014.12.003. PMID 25565207.
19. ↑ 19.0 19.1 19.2 "Mitochondrial quality control in acute ischemic stroke". Journal of Cerebral Blood Flow & Metabolism 41 (12): 3157–3170. 2021. doi:10.1177/0271678X211046992. PMID 34551609.

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