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Open Access 01-12-2019 | Review

Perspectives of cellular communication through tunneling nanotubes in cancer cells and the connection to radiation effects

Authors: Nicole Matejka, Judith Reindl

Published in: Radiation Oncology | Issue 1/2019

Abstract

Direct cell-to-cell communication is crucial for the survival of cells in stressful situations such as during or after radiation exposure. This communication can lead to non-targeted effects, where non-treated or non-infected cells show effects induced by signal transduction from non-healthy cells or vice versa. In the last 15 years, tunneling nanotubes (TNTs) were identified as membrane connections between cells which facilitate the transfer of several cargoes and signals. TNTs were identified in various cell types and serve as promoter of treatment resistance e.g. in chemotherapy treatment of cancer. Here, we discuss our current understanding of how to differentiate tunneling nanotubes from other direct cellular connections and their role in the stress reaction of cellular networks. We also provide a perspective on how the capability of cells to form such networks is related to the ability to surpass stress and how this can be used to study radioresistance of cancer cells.

Buszczak M, Inaba M, Yamashita YM. Signaling by cellular protrusions: keeping the conversation private. Trends Cell Biol. 2016;26(7):526–34.PubMedPubMedCentralCrossRef

LOEWENSTEIN WR, KANNO Y. Intercellular Communication and the Control of Tissue Growth: Lack of Communication between Cancer Cells. Nature 1966; 209(5029):1248–9. Available from: URL: https://www.nature.com/articles/2091248a0.pdf.PubMedCrossRef

Borek C, Higashino S, LOEWENSTEIN WR. Intercellular communication and tissue growth. The Journal of Membrane Biology 1969; 1(1):274–93. Available from: URL: https://doi.org/10.1007/BF01869786 .PubMedCrossRef

Wang X, Gerdes H-H. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ. 2015;22(7):1181–91.PubMedPubMedCentralCrossRef

Guo R, Davis D, Fang Y. Intercellular transfer of mitochondria rescues virus-induced cell death but facilitates cell-to-cell spreading of porcine reproductive and respiratory syndrome virus. Virology. 2018;517:122–34.PubMedCrossRef

Rodriguez A-M, Nakhle J, Griessinger E, Vignais M-L. Intercellular mitochondria trafficking highlighting the dual role of mesenchymal stem cells as both sensors and rescuers of tissue injury. Cell Cycle. 2018;17(6):712–21.PubMedPubMedCentralCrossRef

Torralba D, Baixauli F, Sánchez-Madrid F. Mitochondria know no boundaries: mechanisms and functions of intercellular mitochondrial transfer. Front Cell Dev Biol. 2016;4:107.PubMedPubMedCentralCrossRef

Ariazi J, Benowitz A, de Biasi V, Den Boer ML, Cherqui S, Cui H, et al. Tunneling nanotubes and gap junctions-their role in long-range intercellular communication during development, health, and disease conditions. Front Mol Neurosci. 2017;10:333.PubMedPubMedCentralCrossRef

Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A. Browman DT et al. Prions hijack tunnelling nanotubes for intercellular spread ncb. 2009;11(3):328–36.

10.

Gousset K, Zurzolo C. Tunnelling nanotubes: a highway for prion spreading? Prion. 2009;3(2):94–8.PubMedPubMedCentralCrossRef

11.

Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Köhler K, et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Ncb 2008; 10(2):211–9. Available from: URL. https://www.nature.com/articles/ncb1682.pdf.PubMedCrossRef

12.

Onfelt B, Nedvetzki S, Benninger RKP, Purbhoo MA, Sowinski S, Hume AN, et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol. 2006;177(12):8476–83.PubMedCrossRef

13.

Hurtig J, Orwar O. Injection and transport of bacteria in nanotube–vesicle networks. Soft Matter. 2008;4(7):1515.CrossRefPubMed

14.

Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol. 2007;9(3):310–5.PubMedPubMedCentralCrossRef

15.

Abounit S, Wu JW, Duff K, Victoria GS, Zurzolo C. Tunneling nanotubes: a possible highway in the spreading of tau and other prion-like proteins in neurodegenerative diseases. Prion. 2016;10(5):344–51.PubMedPubMedCentralCrossRef

16.

Lu J, Zheng X, Li F, Yu Y, Chen Z, Liu Z, et al. Tunneling nanotubes promote intercellular mitochondria transfer followed by increased invasiveness in bladder cancer cells. Oncotarget. 2017;8(9):15539–52.PubMedPubMedCentral

17.

Levchenko A, Mehta BM, Niu X, Kang G, Villafania L, Way D, et al. Intercellular transfer of P-glycoprotein mediates acquired multidrug resistance in tumor cells. Proc Natl Acad Sci U S A. 2005;102(6):1933–8.PubMedPubMedCentralCrossRef

18.

Desouky O, Ding N, Zhou G. Targeted and non-targeted effects of ionizing radiation. Journal of Radiation Research and Applied Sciences. 2015;8(2):247–54.CrossRef

19.

Prise KM, O'Sullivan JM. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer. 2009;9(5):351–60.PubMedPubMedCentralCrossRef

20.

Yahyapour R, Motevaseli E, Rezaeyan A, Abdollahi H, Farhood B, Cheki M, et al. Mechanisms of radiation bystander and non-targeted effects: implications to radiation carcinogenesis and radiotherapy. Curr Radiopharm. 2018;11(1):34–45.PubMedCrossRef

21.

Marín A, Martín M, Liñán O, Alvarenga F, López M, Fernández L, et al. Bystander effects and radiotherapy. Reports of Practical Oncology & Radiotherapy 2015; 20(1):12–21. Available from: URL. http://www.sciencedirect.com/science/article/pii/S1507136714001424.

22.

Ariyoshi K, Miura T, Kasai K, Fujishima Y, Nakata A, Yoshida M. Radiation-induced bystander effect is mediated by mitochondrial DNA in exosome-like vesicles. Sci rep; 9(1):1–14. Available from: URL. https://www.nature.com/articles/s41598-019-45669-z.pdf.

23.

Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H-H. Nanotubular highways for intercellular organelle transport. Science. 2004;303(5660):1007–10.PubMedCrossRef

24.

Austefjord MW, Gerdes H-H, Wang X. Tunneling nanotubes: diversity in morphology and structure. Commun Integr Biol. 2014;7(1):e27934.PubMedPubMedCentralCrossRef

25.

Seyed-Razavi Y, Hickey MJ, Kuffová L, McMenamin PG, Chinnery HR. Membrane nanotubes in myeloid cells in the adult mouse cornea represent a novel mode of immune cell interaction. Immunol Cell Biol. 2013;91(1):89–95.PubMedCrossRef

26.

Gurke S, Barroso JFV, Gerdes H-H. The art of cellular communication: tunneling nanotubes bridge the divide. Histochem Cell Biol. 2008;129(5):539–50.PubMedPubMedCentralCrossRef

27.

Gerdes H-H, Bukoreshtliev NV, Barroso JFV. Tunneling nanotubes: a new route for the exchange of components between animal cells. FEBS Lett. 2007;581(11):2194–201.PubMedCrossRef

28.

Marzo L, Gousset K, Zurzolo C. Multifaceted roles of tunneling nanotubes in intercellular communication. Front Physiol. 2012;3:72.PubMedPubMedCentralCrossRef

29.

He K, Shi X, Zhang X, Dang S, Ma X, Liu F, et al. Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc Res. 2011;92(1):39–47.PubMedCrossRef

30.

Islam MN, Das SR, Emin MT, Wei M, Sun L, Westphalen K, et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med. 2012;18(5):759–65.PubMedPubMedCentralCrossRef

31.

Sisakhtnezhad S, Khosravi L. Emerging physiological and pathological implications of tunneling nanotubes formation between cells. Eur J Cell Biol. 2015;94(10):429–43.PubMedCrossRef

32.

McCoy-Simandle K, Hanna SJ, Cox D. Exosomes and nanotubes: control of immune cell communication. Int J Biochem Cell Biol. 2016;71:44–54.PubMedCrossRef

33.

Zaccard CR, Rinaldo CR, Mailliard RB. Linked in: immunologic membrane nanotube networks. J Leukoc Biol. 2016;100(1):81–94.PubMedPubMedCentralCrossRef

34.

Drab M, Stopar D, Kralj-Iglič V, Iglič A. Inception Mechanisms of Tunneling Nanotubes. Cells 2019; 8(6).PubMedCentralCrossRef

35.

Murray LMA, Krasnodembskaya AD. Concise review: intercellular communication via organelle transfer in the biology and therapeutic applications of stem cells. Stem Cells 2019; 37(1):14–25.PubMedCrossRef

36.

Chinnery HR, Pearlman E, McMenamin PG. Cutting edge: membrane nanotubes in vivo: a feature of MHC class II+ cells in the mouse cornea. J Immunol. 2008;180(9):5779–83.PubMedCrossRef

37.

Veranic P, Lokar M, Schütz GJ, Weghuber J, Wieser S, Hägerstrand H, et al. Different types of cell-to-cell connections mediated by nanotubular structures. Biophys J. 2008;95(9):4416–25.PubMedPubMedCentralCrossRef

38.

Bukoreshtliev NV, Wang X, Hodneland E, Gurke S, Barroso JFV, Gerdes H-H. Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett. 2009;583(9):1481–8.PubMedCrossRef

39.

Ranzinger J, Rustom A, Abel M, Leyh J, Kihm L, Witkowski M, et al. Nanotube action between human mesothelial cells reveals novel aspects of inflammatory responses. PLoS One. 2011;6(12):e29537.PubMedPubMedCentralCrossRef

40.

Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity. 2005;23(3):309–18.PubMedCrossRef

41.

Wang X, Gerdes H-H. Long-distance electrical coupling via tunneling nanotubes. Biochim Biophys Acta. 2012;1818(8):2082–6.PubMedCrossRef

42.

Wang X, Veruki ML, Bukoreshtliev NV, Hartveit E, Gerdes H-H. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proc Natl Acad Sci U S A. 2010;107(40):17194–9.PubMedPubMedCentralCrossRef

43.

Chauveau A, Aucher A, Eissmann P, Vivier E, Davis DM. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc Natl Acad Sci U S A. 2010;107(12):5545–50.PubMedPubMedCentralCrossRef

44.

Ramírez-Weber F-A, Kornberg TB. Cytonemes: cellular processes that project to the principal signaling Center in Drosophila Imaginal Discs. Cell 1999; 97(5):599–607. Available from: URL. http://www.sciencedirect.com/science/article/pii/S0092867400807710.PubMedCrossRef

45.

Gradilla A-C, Guerrero I. Cytoneme-mediated cell-to-cell signaling during development. Cell Tissue Res. 2013;352(1):59–66.PubMedCrossRef

46.

Mattila PK, Lappalainen P. Filopodia: molecular architecture and cellular functions. nrm 2008; 9(6):446–54. Available from: URL: https://www.nature.com/articles/nrm2406.pdf.PubMedCrossRef

47.

Hervé J-C, Derangeon M. Gap-junction-mediated cell-to-cell communication. Cell Tissue Res. 2013;352(1):21–31.PubMedCrossRef

48.

Zani BG, Edelman ER. Cellular bridges: routes for intercellular communication and cell migration. Commun Integr Biol. 2010;3(3):215–20.PubMedPubMedCentralCrossRef

49.

Abounit S, Zurzolo C. Wiring through tunneling nanotubes--from electrical signals to organelle transfer. J Cell Sci. 2012;125(Pt 5):1089–98.PubMedCrossRef

50.

Davis DM, Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. nrm. 9(6):431–6. URL: Available from; 2008. https://www.nature.com/articles/nrm2399.pdf

51.

Arkwright PD, Luchetti F, Tour J, Roberts C, Ayub R, Morales AP, et al. Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes. Cell Res. 2010;20(1):72–88.PubMedCrossRef

52.

Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, Kitamura H, et al. M-sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat Cell Biol. 2009;11(12):1427–32.PubMedCrossRef

53.

Schiller C, Diakopoulos KN, Rohwedder I, Kremmer E. Toerne cv, Ueffing M et al. LST1 promotes the assembly of a molecular machinery responsible for tunneling nanotube formation. J cell Sci 2013; 126(3):767–77. Available from: URL. https://jcs.biologists.org/content/joces/126/3/767.full.pdf.PubMedCrossRef

54.

Kabaso D, Lokar M, Kralj-Iglič V, Veranič P, Iglič A. Temperature and cholera toxin B are factors that influence formation of membrane nanotubes in RT4 and T24 urothelial cancer cell lines. Int J Nanomedicine. 2011;6:495–509.PubMedPubMedCentralCrossRef

55.

Lokar M, Iglič A, Veranič P. Protruding membrane nanotubes: attachment of tubular protrusions to adjacent cells by several anchoring junctions. Protoplasma 2010; 246(1):81–7. Available from: URL: https://doi.org/10.1007/s00709-010-0143-7 .PubMedCrossRef

56.

Kimura S, Hase K, Ohno H. The molecular basis of induction and formation of tunneling nanotubes. Cell Tissue Res. 2013;352(1):67–76.PubMedCrossRef

57.

Pasquier J, Guerrouahen BS, Thawadi HA, Ghiabi P, Maleki M, Abu-Kaoud N, et al. Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl med 2013; 11(1):1–14. Available from: URL. https://translational-medicine.biomedcentral.com/track/pdf/10.1186/1479-5876-11-94 .PubMedPubMedCentralCrossRef

58.

Lou E, Fujisawa S, Barlas A, Romin Y, Manova-Todorova K, Moore MAS, et al. Tunneling nanotubes: a new paradigm for studying intercellular communication and therapeutics in cancer. Commun Integr Biol. 2012;5(4):399–403.PubMedPubMedCentralCrossRef

59.

Lou E, Fujisawa S, Morozov A, Barlas A, Romin Y, Dogan Y, et al. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One. 2012;7(3):e33093.PubMedPubMedCentralCrossRef

60.

Koyanagi M, Brandes RP, Haendeler J, Zeiher AM, Dimmeler S. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes? Circ Res. 2005;96(10):1039–41.PubMedCrossRef

61.

He K, Luo W, Zhang Y, Liu F, Liu D, Xu L, et al. Intercellular transportation of quantum dots mediated by membrane nanotubes. ACS Nano. 2010;4(6):3015–22.PubMedCrossRef

62.

Wang Z-G, Liu S-L, Tian Z-Q, Zhang Z-L, Tang H-W, Pang D-W. Myosin-driven intercellular transportation of wheat germ agglutinin mediated by membrane nanotubes between human lung cancer cells. ACS Nano. 2012;6(11):10033–41.PubMedCrossRef

63.

Mi L, Xiong R, Zhang Y, Yang W, Chen J-Y, Wang P-N. Microscopic observation of the intercellular transport of CdTe quantum dot aggregates through tunneling-nanotubes. JBNB. 2011;02(02):172–9.CrossRef

64.

Rehberg M, Nekolla K, Sellner S, Praetner M, Mildner K, Zeuschner D, et al. Intercellular transport of Nanomaterials is mediated by membrane nanotubes in vivo. Small. 2016;12(14):1882–90.PubMedCrossRef

65.

Haimovich G, Ecker CM, Dunagin MC, Eggan E, Raj A, Gerst JE et al. Intercellular mRNA trafficking via membrane nanotubes in mammalian cells; 2017. ( vol 11).

66.

Smith IF, Shuai J, Parker I. Active generation and propagation of Ca2+ signals within tunneling membrane nanotubes. Biophys J. 2011;100(8):L37–9.PubMedPubMedCentralCrossRef

67.

Bittins M, Wang X. TNT-induced phagocytosis: tunneling nanotubes mediate the transfer of pro-phagocytic signals from apoptotic to viable cells. Journal of cellular physiology 2017; 232(9):2271–9. Available from: URL. https://onlinelibrary.wiley.com/doi/pdf/10.1002/jcp.25584 .PubMedPubMedCentralCrossRef

68.

Gerdes H-H, Carvalho RN. Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol. 2008;20(4):470–5.PubMedCrossRef

69.

Hurtig J, Chiu DT, Onfelt B. Intercellular nanotubes: insights from imaging studies and beyond. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2010;2(3):260–76.PubMedPubMedCentralCrossRef

70.

Zhu D, Tan KS, Zhang X, Sun AY, Sun GY, Lee JC-M. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci. 2005;118(Pt 16):3695–703.PubMedCrossRef

71.

Desir S, Dickson EL, Vogel RI, Thayanithy V, Wong P, Teoh D, et al. Tunneling nanotube formation is stimulated by hypoxia in ovarian cancer cells. Oncotarget. 2016;7(28):43150–61.PubMedPubMedCentralCrossRef

72.

Osswald M, Jung E, Sahm F, Solecki G, Venkataramani V, Blaes J, et al. Brain tumour cells interconnect to a functional and resistant network. Nature. 2015;528(7580):93–8.PubMedCrossRef

73.

Reindl J, Shevtsov M, Dollinger G, Stangl S, Multhoff G. Membrane Hsp70-supported cell-to-cell connections via tunneling nanotubes revealed by live-cell STED nanoscopy. Cell Stress Chaperones. 2019;24(1):213–21.PubMedPubMedCentralCrossRef

74.

Eugenin EA, Gaskill PJ, Berman JW. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell Immunol. 2009;254(2):142–8.PubMedCrossRef

75.

Rustom A. The missing link: does tunnelling nanotube-based supercellularity provide a new understanding of chronic and lifestyle diseases? Open Biol 2016; 6(6).PubMedPubMedCentralCrossRef

76.

Wang Y, Cui J, Sun X, Zhang Y. Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death Differ. 2011;18(4):732–42.PubMedCrossRef

77.

Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol. 2008;9(5):402–12.PubMedCrossRef

78.

Pontes B, Viana NB, Campanati L, Farina M, Neto VM, Nussenzveig HM. Structure and elastic properties of tunneling nanotubes. Eur Biophys J. 2008;37(2):121–9.PubMedCrossRef

79.

Venkatesh VS, Lou E. Tunnelling nanotubes: a bridge for heterogeneity in glioblastoma and a new therapeutic target? Cancer Reports. 2019;74(13):e1185.CrossRef

80.

Osswald M, Jung E, Wick W, Winkler F. Tunneling nanotube-like structures in brain tumors. Cancer Reports. 2019;6(6):1124.

81.

Desir S, O’Hare P, Vogel RI, Sperduto W, Sarkari A, Dickson EL, et al. Chemotherapy-induced tunneling nanotubes mediate intercellular drug efflux in pancreatic Cancer. Sci rep 2018; 8(1):1–13. Available from: URL. https://www.nature.com/articles/s41598-018-27649-x.pdf.

82.

Pasquier J, Galas L, Boulangé-Lecomte C, Rioult D, Bultelle F, Magal P, et al. Different modalities of intercellular membrane exchanges mediate cell-to-cell p-glycoprotein transfers in MCF-7 breast cancer cells. J Biol Chem. 2012;287(10):7374–87.PubMedPubMedCentralCrossRef

83.

Thayanithy V, Dickson EL, Steer C, Subramanian S, Lou E. Tumor-stromal cross talk: direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes. Transl Res. 2014;164(5):359–65.PubMedPubMedCentralCrossRef

84.

Antanavičiūtė I, Rysevaitė K, Liutkevičius V, Marandykina A, Rimkutė L, Sveikatienė R, et al. Long-distance communication between laryngeal carcinoma cells. PLoS One. 2014;9(6):e99196.PubMedCentralCrossRefPubMed

85.

Ady JW, Desir S, Thayanithy V, Vogel RI, Moreira AL, Downey RJ, et al. Intercellular communication in malignant pleural mesothelioma: properties of tunneling nanotubes. Front Physiol. 2014;5:400.PubMedCentralCrossRefPubMed

86.

Ady J, Thayanithy V, Mojica K, Wong P, Carson J, Rao P, et al. Tunneling nanotubes: an alternate route for propagation of the bystander effect following oncolytic viral infection. Mol Ther Oncolytics. 2016;3:16029.PubMedPubMedCentralCrossRef

87.

Thayanithy V, Babatunde V, Dickson EL, Wong P, Oh S, Ke X, et al. Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells. Exp Cell Res. 2014;323(1):178–88.PubMedCentralCrossRefPubMed

88.

Bao L, Hazari S, Mehra S, Kaushal D, Moroz K, Dash S. Increased expression of P-glycoprotein and doxorubicin chemoresistance of metastatic breast cancer is regulated by miR-298. Am J Pathol. 2012;180(6):2490–503.PubMedPubMedCentralCrossRef

89.

Munoz JL, Bliss SA, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P. Delivery of functional anti-miR-9 by Mesenchymal stem cell-derived Exosomes to Glioblastoma Multiforme cells conferred Chemosensitivity. Mol Ther Nucleic Acids. 2013;2:e126.PubMedPubMedCentralCrossRef

90.

Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 2005;104(6):1129–37.PubMedCrossRef

91.

Baskar R, Lee KA, Yeo R, Yeoh K-W. Cancer and radiation therapy: current advances and future directions. Int J Med Sci. 2012;9(3):193–9.PubMedCentralCrossRefPubMed

92.

Raychaudhuri B, Vogelbaum MA. IL-8 is a mediator of NF-κB induced invasion by gliomas. J Neuro-Oncol. 2011;101(2):227–35.CrossRef

93.

Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M, et al. Long-term survival with glioblastoma multiforme. Brain. 2007;130(Pt 10):2596–606.PubMedCrossRef

94.

Curran WJ, Scott CB, Weinstein AS, Martin LA, Nelson JS, Phillips TL, et al. Survival comparison of radiosurgery-eligible and -ineligible malignant glioma patients treated with hyperfractionated radiation therapy and carmustine: a report of radiation therapy oncology group 83-02. J Clin Oncol. 1993;11(5):857–62.CrossRefPubMed

95.

Wank M, Schilling D, Reindl J, Meyer B, Gempt J, Motov S, et al. Evaluation of radiation-related invasion in primary patient-derived glioma cells and validation with established cell lines: impact of different radiation qualities with differing LET. J Neuro-Oncol. 2018;139(3):583–90.CrossRef

96.

Rieken S, Habermehl D, Mohr A, Wuerth L, Lindel K, Weber K, et al. Targeting ανβ3 and ανβ5 inhibits photon-induced hypermigration of malignant glioma cells. Radiat Oncol. 2011;6:132.PubMedPubMedCentralCrossRef

97.

Pouget JP, Mather SJ. General aspects of the cellular response to low- and high-LET radiation. Eur J Nucl Med. 2001;28(4):541–61.PubMedCrossRef

98.

Baker M. How the internet of cells has biologists buzzing. Nature. 2017;549(7672):322–4.PubMedCrossRef

99.

Winkler F, Wick W. Harmful networks in the brain and beyond. Science. 2018;359(6380):1100–1.PubMedCrossRef

100.

Lou E, Zhai E, Sarkari A, Desir S, Wong P, Iizuka Y, et al. Cellular and molecular networking within the ecosystem of Cancer cell communication via tunneling nanotubes. Front Cell Dev Biol. 2018;6:95.PubMedPubMedCentralCrossRef

101.

Takei H, Inaniwa T. Effect of irradiation time on biological effectiveness and tumor control probability in proton therapy. Int J Radiat Oncol Biol Phys. 2019;105(1):222–9.PubMedCrossRef

102.

Schulz-Ertner D, Nikoghosyan A, Thilmann C, Haberer T, Jäkel O, Karger C, et al. Results of carbon ion radiotherapy in 152 patients. International journal of radiation oncology*biology*physics 2004; 58(2):631–40. Available from: URL. http://www.sciencedirect.com/science/article/pii/S0360301603019801.CrossRefPubMed

103.

Levin WP, Kooy H, Loeffler JS, DeLaney TF. Proton beam therapy. Br J Cancer 2005; 93(8):849–54. Available from: URL: https://www.nature.com/articles/6602754.pdf.PubMedCentralCrossRefPubMed

104.

Makishima H, Yasuda S, Isozaki Y, Kasuya G, Okada N, Miyazaki M, et al. Single fraction carbon ion radiotherapy for colorectal cancer liver metastasis: a dose escalation study. Cancer Sci. 2019;110(1):303–9.PubMed

105.

Fukumitsu N, Sugahara S, Nakayama H, Fukuda K, Mizumoto M, Abei M et al. A Prospective Study of Hypofractionated Proton Beam Therapy for Patients With Hepatocellular Carcinoma. International Journal of Radiation Oncology*Biology*Physics 2009; 74(3):831–6. Available from: URL: http://www.sciencedirect.com/science/article/pii/S0360301608038625.CrossRefPubMed

106.

Sahu P, Jena SR, Samanta L. Tunneling nanotubes: a versatile target for Cancer therapy. Curr Cancer Drug Targets. 2018;18(6):514–21.PubMedCrossRef

107.

Osswald M, Solecki G, Wick W, Winkler F. A malignant cellular network in gliomas: potential clinical implications. Neuro-oncology. 2016;18(4):479–85.PubMedPubMedCentralCrossRef

108.

Vignais M-L, Caicedo A, Brondello J-M, Jorgensen C. Cell connections by tunneling nanotubes: effects of mitochondrial trafficking on target cell metabolism, homeostasis, and response to therapy. Stem Cells Int. 2017;2017:6917941.PubMedPubMedCentralCrossRef

Title: Perspectives of cellular communication through tunneling nanotubes in cancer cells and the connection to radiation effects
Authors: Nicole Matejka
Judith Reindl
Publication date: 01-12-2019
Publisher: BioMed Central
Published in: Radiation Oncology / Issue 1/2019
Electronic ISSN: 1748-717X
DOI: https://doi.org/10.1186/s13014-019-1416-8

At a glance: The STEP trials

Springer Medicine

Perspectives of cellular communication through tunneling nanotubes in cancer cells and the connection to radiation effects

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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