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Intercellular nanotubes mediate mitochondrial trafficking between cancer and immune cells

  • 1.

    Wei, S. C. et al. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell 170, 1120–1133.e17 (2017).

    CAS 
    Article 

    Google Scholar 

  • 2.

    Sharma, P. & Allison, J. P. Dissecting the mechanisms of immune checkpoint therapy. Nat. Rev. Immunol. 20, 75–76 (2020).

    CAS 
    Article 

    Google Scholar 

  • 3.

    Wolchok, J. Putting the immunologic brakes on cancer. Cell 175, 1452–1454 (2018).

    CAS 
    Article 

    Google Scholar 

  • 4.

    Kulkarni, A. et al. A designer self-assembled supramolecule amplifies macrophage immune responses against aggressive cancer. Nat. Biomed. Eng. 2, 589–599 (2018).

    CAS 
    Article 

    Google Scholar 

  • 5.

    Wei, S. C., Duffy, C. R. & Allison, J. P. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 8, 1069–1086 (2018).

    Article 

    Google Scholar 

  • 6.

    Tseng, D. et al. Anti-CD47 antibody–mediated phagocytosis of cancer by macrophages primes an effective antitumor T-cell response. Proc. Natl Acad. Sci. USA 110, 11103–11108 (2013).

    CAS 
    Article 

    Google Scholar 

  • 7.

    Sharma, P. & Allison, J. P. The future of immune checkpoint therapy. Science 348, 56–61 (2015).

    CAS 
    Article 

    Google Scholar 

  • 8.

    Önfelt, B., Nedvetzki, S., Yanagi, K. & Davis, D. M. Cutting edge: membrane nanotubes connect immune cells. J. Immunol. 173, 1511–1513 (2004).

    Article 

    Google Scholar 

  • 9.

    Sowinski, S. et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10, 211–219 (2008).

    Article 

    Google Scholar 

  • 10.

    Gousset, K. et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 11, 328–336 (2009).

    Article 

    Google Scholar 

  • 11.

    Osswald, M. et al. Brain tumour cells interconnect to a functional and resistant network. Nature 528, 93–98 (2015).

    Article 

    Google Scholar 

  • 12.

    Connor, Y. et al. Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype. Nat. Commun. 6, 8671 (2015).

  • 13.

    Rustom, A., Saffrich, R., Markovic, I., Walther, P. & Gerdes, H.-H. Nanotubular highways for intercellular organelle transport. Science 303, 1007–1010 (2004).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Ahmad, T. et al. Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J. 33, 994–1010 (2014).

    CAS 

    Google Scholar 

  • 15.

    Wang, X. & Gerdes, H. H. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ. 22, 1181–1191 (2015).

    Google Scholar 

  • 16.

    Lu, J. et al. Tunneling nanotubes promote intercellular mitochondria transfer followed by increased invasiveness in bladder cancer cells. Oncotarget 8, 15539–15552 (2017).

    Article 

    Google Scholar 

  • 17.

    Sena, L. A. et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225–236 (2013).

    CAS 
    Article 

    Google Scholar 

  • 18.

    Kumar, A. et al. Enhanced oxidative phosphorylation in NKT cells is essential for their survival and function. Proc. Natl Acad. Sci. USA 116, 7439–7448 (2019).

    CAS 
    Article 

    Google Scholar 

  • 19.

    Vyas, S., Zaganjor, E. & Haigis, M. C. Mitochondria and cancer. Cell 166, 555–566 (2016).

    CAS 
    Article 

    Google Scholar 

  • 20.

    Goldman, A. et al. Targeting tumor phenotypic plasticity and metabolic remodeling in adaptive cross-drug tolerance. Sci. Signal. 12, eaas8779 (2019).

    Article 

    Google Scholar 

  • 21.

    Clutton, G., Mollan, K., Hudgens, M. & Goonetilleke, N. A reproducible, objective method using MitoTracker® fluorescent dyes to assess mitochondrial mass in T cells by flow cytometry. Cytometry 95, 450–456 (2019).

    CAS 
    Article 

    Google Scholar 

  • 22.

    Pham, A. H., McCaffery, J. M. & Chan, D. C. Mouse lines with photo-activatable mitochondria to study mitochondrial dynamics. Genesis 50, 833–843 (2012).

    CAS 
    Article 

    Google Scholar 

  • 23.

    Pelletier, M., Billingham, L. K., Ramaswamy, M. & Siegel, R. M. in Methods Enzymol, Vol. 542 (eds Galluzzi, L. & Kroemer, G.) 125–149 (Academic Press, 2014).

  • 24.

    Kaplon, J. et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature 498, 109–112 (2013).

    Article 

    Google Scholar 

  • 25.

    Hase, K. et al. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell Biol. 11, 1427–1432 (2009).

    Article 

    Google Scholar 

  • 26.

    Hashimoto, M. et al. Potential role of the formation of tunneling nanotubes in HIV-1 spread in macrophages. J. Immunol. 196, 1832–1841 (2016).

    CAS 
    Article 

    Google Scholar 

  • 27.

    Moskalenko, S. et al. The exocyst is a Ral effector complex. Nat. Cell Biol. 4, 66–72 (2002).

    CAS 
    Article 

    Google Scholar 

  • 28.

    Hanna, S. J. et al. The role of Rho-GTPases and actin polymerization during macrophage tunneling nanotube biogenesis. Sci. Rep. 7, 8547 (2017).

    Article 

    Google Scholar 

  • 29.

    Guo, W., Tamanoi, F. & Novick, P. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 3, 353–360 (2001).

    CAS 
    Article 

    Google Scholar 

  • 30.

    Fransson, Å., Ruusala, A. & Aspenström, P. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem. Biophys. Res. Commun. 344, 500–510 (2006).

    CAS 
    Article 

    Google Scholar 

  • 31.

    Glater, E. E., Megeath, L. J., Stowers, R. S. & Schwarz, T. L. Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 173, 545–557 (2006).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Arkwright, P. D. et al. Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes. Cell Res. 20, 72–88.

  • 33.

    Bustelo, X. R., Sauzeau, V. & Berenjeno, I. M. GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bioessays 29, 356–370 (2007).

    CAS 
    Article 

    Google Scholar 

  • 34.

    Majumder, B. et al. Predicting clinical response to anticancer drugs using an ex vivo platform that captures tumour heterogeneity. Nat. Commun. 6, 6169 (2015).

    CAS 
    Article 

    Google Scholar 

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