Emerging physiological and pathological implications of tunneling nanotubes formation between cells

European Journal of Cell Biology

Volumn 94, Issue 10, 2015, Pages 429-443

  Sisakhtnezhad, Sajjad ^a   Khosravi, Leila ^a  

^a RAZI UNIVERSITY   (Iran)

Author keywords

Apoptosis; Cancer; Embryogenesis and development; Immune response; Intercellular transfer; Micro and nano particles; Neurodegenerative disease; Pathogen; Reprogramming; Signal transduction; Tunneling nanotube

Indexed keywords

APOPTOSIS; BACTERIAL TRANSMISSION; CANCER GROWTH; CARCINOGENESIS; CELL DIFFERENTIATION; CELL STRUCTURE; CELL TRANSFORMATION; DEGENERATIVE DISEASE; DISEASE COURSE; EMBRYO DEVELOPMENT; GAP JUNCTION; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR REPROGRAMMING; PRION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUNNELING NANOTUBE; VIRUS TRANSMISSION; ANIMAL; CELL COMMUNICATION; CELL JUNCTION; CYTOSKELETON; ORGANELLE BIOGENESIS; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

NANOPARTICLE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL COMMUNICATION; CYTOSKELETON; HUMANS; INTERCELLULAR JUNCTIONS; NANOPARTICLES; ORGANELLE BIOGENESIS;

EID: 84946479256     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2015.06.010     Document Type: Review

References (150)

1. Abounit S., Zurzolo C. Wiring through tunneling nanotubes-from electrical signals to organelle transfer. J. Cell Sci. 2012, 125:1089-1098.
2. Acquistapace A., Bru T., Lesault P.F., Figeac F., Coudert A.E., le Coz O., Christov C., Baudin X., Auber F., Yiou R., Dubois-Rande J.L., Rodriguez A.M. Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer. Stem Cells 2011, 29:812-824.
3. Alomari M., Mactier S., Kaufman K.L., Best O.G., Mulligan S.P., Christopherson R.I. Profiling the lipid raft proteome from human mec1 chronic lymphocytic leukemia cells. J. Proteomics Bioinform. 2014, S7:005.
4. Andresen V., Wang X., Ghimire S., Omsland M., Gjertsen B.T., Gerdes H.H. Tunneling nanotube (TNT) formation is independent of p53 expression. Cell Death Differ. 2013, 20:1124.
5. Andrzejewski S., Gravel S.P., Pollak M., St-Pierre J. Metformin directly acts on mitochondria to alter cellular bioenergetics. Cancer Metab. 2014, 2:12.
6. Arkwright P.D., Luchetti F., Tour J., Roberts C., Ayub R., Morales A.P., Rodriguez J.J., Gilmore A., Canonico B., Papa S., Esposti M.D. Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes. Cell Res. 2010, 20:72-88.
7. Austefjord M.W., Gerdes H.H., Wang X. Tunneling nanotubes: diversity in morphology and structure. Commun. Integr. Biol. 2014, 7:e27934.
8. Baselga J., Campone M., Piccart M.A., Rugo B.H., Sahmoud H.S., Noguchi T., Gnant S., Pritchard M., Lebrun K.I., Beck F., Ito J.T., Yardley Y., Deleu D., Perez I., Bachelot A., Vittori T., Xu L., Mukhopadhyay Z., Lebwohl P., Hortobagyi D.G.N. Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N. Engl. J. Med. 2012, 366:520-529.
9. Bayer T.A. Proteinopathies, a core concept for understanding and ultimately treating degenerative disorders?. Eur. Neuropsychopharmacol. 2015, 25:713-724.
10. Bebawy M., Combes V., Lee E., Jaiswal R., Gong J., Bonhoure A., Grau G.E. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia 2009, 23:1643-1649.
11. Boomsma R.A., Geenen D.L. Evidence for transfer of membranes from mesenchymal stem cells to HL-1 cardiac cells. Stem Cells Int. 2014, 2014:653734.
12. Bukoreshtliev N.V., Wang X., Hodneland E., Gurke S., Barroso J.F., Gerdes H.H. Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett. 2009, 583:1481-1488.
13. Caneparo L., Pantazis P., Dempsey W., Fraser S.E. Intercellular bridges in vertebrate gastrulation. PloS One 2011, 6:e20230.
14. Caughey B., Baron G.S. Prions and their partners in crime. Nature 2006, 443:803-810.
15. Chauveau A., Aucher A., Eissmann P., Vivier E., Davis D.M. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5545-5550.
16. Chinnery H.R., Pearlman E., McMenamin P.G. Cutting edge: Membrane nanotubes in vivo: a feature of MHC class II+ cells in the mouse cornea. J. Immunol. 2008, 180:5779-5783.
17. Costanzo M., Abounit S., Marzo L., Danckaert A., Chamoun Z., Roux P., Zurzolo C. Transfer of polyglutamine aggregates in neuronal cells occurs in tunneling nanotubes. J. Cell Sci. 2013, 126:3678-3685.
18. Cselenyak A., Pankotai E., Horvath E.M., Kiss L., Lacza Z. Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections. BMC Cell Biol. 2010, 11:29.
19. Domhan S., Ma L., Tai A., Anaya Z., Beheshti A., Zeier M., Hlatky L., Abdollahi A. Intercellular communication by exchange of cytoplasmic material via tunneling nano-tube like structures in primary human renal epithelial cells. PloS One 2011, 6:e21283.
20. Dubey G.P., Ben-Yehuda S. Intercellular nanotubes mediate bacterial communication. Cell 2011, 144:590-600.
21. Dunning C.J., Reyes J.F., Steiner J.A., Brundin P. Can Parkinson's disease pathology be propagated from one neuron to another?. Prog. Neurobiol. 2012, 97:205-219.
22. Elias L.A., Turmaine M., Parnavelas J.G., Kriegstein A.R. Connexin 43 mediates the tangential to radial migratory switch in ventrally derived cortical interneurons. J. Neurosci. 2010, 30:7072-7077.
23. Elias L.A., Wang D.D., Kriegstein A.R. Gap junction adhesion is necessary for radial migration in the neocortex. Nature 2007, 448:901-907.
24. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
25. Eugenin E.A., Gaskill P.J., Berman J.W. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell. Immunol. 2009, 254:142-148.
26. Ferrati S., Shamsudeen S., Summers H.D., Rees P., Abbey J.V., Schmulen J., Liu X., Wong S.T., Bean A.J., Ferrari M., Serda R.E. Inter-endothelial transport of microvectors using cellular shuttles and tunneling nanotubes. Small 2012, 8:3151-3160.
27. Garden G.A., La Spada A.R. Intercellular (mis)communication in neurodegenerative disease. Neuron 2012, 73:886-901.
28. Gerdes H.H. Prions tunnel between cells. Nat. Cell Biol. 2009, 11:235-236.
29. Gerdes H.H., Bukoreshtliev N.V., Barroso J.F. Tunneling nanotubes: a new route for the exchange of components between animal cells. FEBS Lett. 2007, 581:2194-2201.
30. Gerdes H.H., Carvalho R.N. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 2008, 20:470-475.
31. Sc upon prion conversion on the plasma membrane. J. Cell Sci. 2013, 126:3552-3562.
32. Gordón-Alonso M., Veiga E., Sánchez-Madrid F. Actin dynamics at the immunological synapse. Cell Health Cytoskelet. 2010, 2:33-47.
33. Gousset K., Marzo L., Commere P.H., Zurzolo C. Myo10 is a key regulator of TNT formation in neuronal cells. J. Cell Sci. 2013, 126:4424-4435.
34. Gousset K., Schiff E., Langevin C., Marijanovic Z., Caputo A., Browman D.T., Chenouard N., de Chaumont F., Martino A., Enninga J., Olivo-Marin J.C., Mannel D., Zurzolo C. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 2009, 11:328-336.
35. Gousset K., Zurzolo C. Tunnelling nanotubes: a highway for prion spreading?. Prion 2009, 3:94-98.
36. Guescini M., Leo G., Genedani S., Carone C., Pederzoli F., Ciruela F., Guidolin D., Stocchi V., Mantuano M., Borroto-Escuela D.O., Fuxe K., Agnati L.F. Microvesicle and tunneling nanotube mediated intercellular transfer of g-protein coupled receptors in cell cultures. Exp. Cell Res. 2012, 318:603-613.
37. Gurke S., Barroso J.F., Gerdes H.H. The art of cellular communication: tunneling nanotubes bridge the divide. Histochem. Cell Biol. 2008, 129:539-550.
38. Hase K., Kimura S., Takatsu H., Ohmae M., Kawano S., Kitamura H., Ito M., Watarai H., Hazelett C.C., Yeaman C., Ohno H. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell Biol. 2009, 11:1427-1432.
39. He K., Luo W., Zhang Y., Liu F., Liu D., Xu L., Qin L., Xiong C., Lu Z., Fang X. Intercellular transportation of quantum dots mediated by membrane nanotubes. ACS Nano 2010, 4:3015-3022.
40. He K., Shi X., Zhang X., Dang S., Ma X., Liu F., Xu M., Lv Z., Han D., Fang X., Zhang Y. Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc. Res. 2011, 92:39-47.
41. Humphries B., Yang C. The microRNA-200 family: small molecules with novel roles in cancer development, progression and therapy. Oncotarget 2015, 6:6472-6498.
42. Hurtig J., Chiu D.T., Onfelt B. Intercellular nanotubes: insights from imaging studies and beyond. Wiley interdisciplinary reviews. Nanomed. Nanobiotechnol. 2010, 2:260-276.
43. Ikeda M., Ishida O., Hinoi T., Kishida S., Kikuchi A. Identification and characterization of a novel protein interacting with Ral-binding protein 1, a putative effector protein of Ral. J. Biol. Chem. 1998, 273:814-821.
44. Incardona J.P., Lee J.H., Robertson C.P., Enga K., Kapur R.P., Roelink H. Receptor-mediated endocytosis of soluble and membrane-tethered Sonic hedgehog by Patched-1. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:12044-12049.
45. Islam M.N., Das S.R., Emin M.T., Wei M., Sun L., Westphalen K., Rowlands D.J., Quadri S.K., Bhattacharya S., Bhattacharya J. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat. Med. 2012, 18:759-765.
46. Kabaso D., Lokar M., Kralj-Iglic V., Veranic P., Iglic A. Temperature and cholera toxin B are factors that influence formation of membrane nanotubes in RT4 and T24 urothelial cancer cell lines. Int. J. Nanomed. 2011, 6:495-509.
47. Kadiu I., Gendelman H.E. Human immunodeficiency virus type 1 endocytic trafficking through macrophage bridging conduits facilitates spread of infection. J. Neuroimmune Pharmacol. NeuroImmune Pharmacol. 2011, 6:658-675.
48. Kadiu I., Gendelman H.E. Macrophage bridging conduit trafficking of HIV-1 through the endoplasmic reticulum and Golgi network. J. Proteome Res. 2011, 10:3225-3238.
49. Kadiu I., Orenstein J.M., Gendelman H.E. HIV-1 hijacks tunneling nanotubes and secretory microvesicles for intercellular spread in monocyte-derived macrophages. Retrovirology 2009, 6:O22.
50. Kaminska K., Szczylik C., Bielecka Z.F., Bartnik E., Porta C., Lian F., Czarnecka A.M. The role of the cell-cell interactions in cancer progression. J. Cell. Mol. Med. 2015, 19:283-296.
51. Kegel K.B., Sapp E., Yoder J., Cuiffo B., Sobin L., Kim Y.J., Qin Z.H., Hayden M.R., Aronin N., Scott D.L., Isenberg G., Goldmann W.H., DiFiglia M. Huntingtin associates with acidic phospholipids at the plasma membrane. J. Biol. Chem. 2005, 280:36464-36473.
52. Kegel K.B., Schewkunow V., Sapp E., Masso N., Wanker E.E., DiFiglia M., Goldmann W.H. Polyglutamine expansion in huntingtin increases its insertion into lipid bilayers. Biochem. Biophys. Res. Commun. 2009, 387:472-475.
53. Kellner S., Kikyo N. Transcriptional regulation of the Oct4 gene, a master gene for pluripotency. Histol. Histopathol. 2010, 25:405-412.
54. Knopik-skrocka A., Sniegowska A. Participation of membrane nanotubes in intercellular communication. Adv. Cell. Biol. 2014, 4:61-82.
55. Koyanagi M., Brandes R.P., Haendeler J., Zeiher A.M., 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, 96:1039-1041.
56. Kuznetsov I.A., Kuznetsov A.V. A two population model of prion transport through a tunnelling nanotube. Comput. Methods Biomech. Biomed. Eng. 2014, 17:1705-1715.
57. Lee J.Y. New and old roles of plasmodesmata in immunity and parallels to tunneling nanotubes. Plant Sci. 2014, 221-222:13-20.
58. Levin M. Molecular bioelectricity in developmental biology: new tools and recent discoveries: control of cell behavior and pattern formation by transmembrane potential gradients. Bioessays 2012, 34:205-217.
59. Levin M. Molecular bioelectricity: how endogenous voltage potentials control cell behavior and instruct pattern regulation in vivo. Mol. Biol. Cell 2014, 25:3835-3850.
60. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
61. Liras A. Future research and therapeutic applications of human stem cells: general, regulatory, and bioethical aspects. J. Transl. Med. 2010, 8:131.
62. Lo U.G., Yang D., Hsieh J.T. The role of microRNAs in prostate cancer progression. Transl. Androl. Urol. 2013, 2:228-241.
63. Lokar M., Iglic A., Veranic P. Protruding membrane nanotubes: attachment of tubular protrusions to adjacent cells by several anchoring junctions. Protoplasma 2010, 246:81-87.
64. Lou E., Fujisawa S., Barlas A., Romin Y., Manova-Todorova K., Moore M.A., Subramanian S. Tunneling Nanotubes: a new paradigm for studying intercellular communication and therapeutics in cancer. Commun. Integr. Biol. 2012, 5:399-403.
65. Lou E., Fujisawa S., Morozov A., Barlas A., Romin Y., Dogan Y., Gholami S., Moreira A.L., Manova-Todorova K., Moore M.A. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PloS One 2012, 7:e33093.
66. Luchetti F., Canonico B., Arcangeletti M., Guescini M., Cesarini E., Stocchi V., Degli Esposti M., Papa S. Fas signalling promotes intercellular communication in T cells. PloS One 2012, 7:e35766.
67. Luo G., Yi J., Ma C., Xiao Y., Yi F., Yu T., Zhou J. Defective mitochondrial dynamics is an early event in skeletal muscle of an amyotrophic lateral sclerosis mouse model. PloS One 2013, 8:e82112.
68. Luo Q., Hu D., Hu S., Yan M., Sun Z., Chen F. In vitro and in vivo anti-tumor effect of metformin as a novel therapeutic agent in human oral squamous cell carcinoma. BMC Cancer 2012, 12:517.
69. Lutz M., Kapp M., Einsele H., Grigoleit G.U., Mielke S. Improvement of quality of life in patients with steroid-refractory chronic graft-versus-host disease treated with the mTOR inhibitor everolimus. Clin. Transplant. 2014, 28:1410-1415.
70. Ma L., Rohatgi R., Kirschner M.W. The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15362-15367.
71. Mabbott N.A., MacPherson G.G. Prions and their lethal journey to the brain. Nat. Rev. Microbiol. 2006, 4:201-211.
72. Magalhaes A.C., Baron G.S., Lee K.S., Steele-Mortimer O., Dorward D., Prado M.A., Caughey B. Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells. J. Neurosci. 2005, 25:5207-5216.
73. Malek M., Aghili R., Emami Z., Khamseh M.E. Risk of cancer in diabetes: the effect of metformin. ISRN Endocrinol. 2013, 2013:636927.
74. Mao-Ying Q.L., Kavelaars A., Krukowski K., Huo X.J., Zhou W., Price T.J., Cleeland C., Heijnen C.J. The anti-diabetic drug metformin protects against chemotherapy-induced peripheral neuropathy in a mouse model. PloS One 2014, 9:e100701.
75. Martin D.A., Zheng L., Siegel R.M., Huang B., Fisher G.H., Wang J., Jackson C.E., Puck J.M., Dale J., Straus S.E., Peter M.E., Krammer P.H., Fesik S., Lenardo M.J. Defective CD95/APO-1/Fas signal complex formation in the human autoimmune lymphoproliferative syndrome, type Ia. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4552-4557.
76. Matin M.M., Walsh J.R., Gokhale P.J., Draper J.S., Bahrami A.R., Morton I., Moore H.D., Andrews P.W. Specific knockdown of Oct4 and beta2-microglobulin expression by RNA interference in human embryonic stem cells and embryonic carcinoma cells. Stem Cells 2004, 22:659-668.
77. McGowan M. Tunneling nanotubes-crossing the bridge. J. Cell. Mol. Biol. 2011, 9:11-28.
78. McKinney M.C., Stark D.A., Teddy J., Kulesa P.M. Neural crest cell communication involves an exchange of cytoplasmic material through cellular bridges revealed by photoconversion of KikGR. Dev. Dyn. 2011, 240:1391-1401.
79. Mi L., Xiong R., Zhang Y., Li Z., Yang W., Chen J.Y., Wang P.N. Microscopic observation of the intercellular transport of cdte quantum dot aggregates through tunneling-nanotubes. J. Biomater. Nanobiotechnol. 2011, 2:173-180.
80. Mielke S., Lutz M., Schmidhuber J., Kapp M., Ditz D., Ammer J., Einsele H., Grigoleit G.U., Holler E., Wolff D. Salvage therapy with everolimus reduces the severity of treatment-refractory chronic GVHD without impairing disease control: a dual center retrospective analysis. Bone Marrow Transplant. 2014, 49:1412-1418.
81. Mukerji J., Olivieri K.C., Misra V., Agopian K.A., Gabuzda D. Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation. Retrovirology 2012, 9:33.
82. Naphade S., Sharma J., Gaide Chevronnay H.P., Shook M.A., Yeagy B.A., Rocca C.J., Ur S.N., Lau A.J., Courtoy P.J., Cherqui S. Brief reports: Lysosomal cross-correction by hematopoietic stem cell-derived macrophages via tunneling nanotubes. Stem Cells 2015, 33:301-309.
83. Ohta Y., Suzuki N., Nakamura S., Hartwig J.H., Stossel T.P. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2122-2128.
84. Okita K., Yamanaka S. Induced pluripotent stem cells: opportunities and challenges. Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 2011, 366:2198-2207.
85. Onfelt B., Nedvetzki S., Benninger R.K., Purbhoo M.A., Sowinski S., Hume A.N., Seabra M.C., Neil M.A., French P.M., Davis D.M. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J. Immunol. 2006, 177:8476-8483.
86. Onfelt B., Nedvetzki S., Yanagi K., Davis D.M. Cutting edge: Membrane nanotubes connect immune cells. J. Immunol. 2004, 173:1511-1513.
87. Parikh A., Lee C., Joseph P., Marchini S., Baccarini A., Kolev V., Romualdi C., Fruscio R., Shah H., Wang F., Mullokandov G., Fishman D., D'Incalci M., Rahaman J., Kalir T., Redline R.W., Brown B.D., Narla G., DiFeo A. microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelial-mesenchymal transition. Nat. Commun. 2014, 5:2977.
88. Pasquier J., Galas L., Boulange-Lecomte C., Rioult D., Bultelle F., Magal P., Webb G., Le Foll F. Different modalities of intercellular membrane exchanges mediate cell-to-cell p-glycoprotein transfers in MCF-7 breast cancer cells. J. Biol. Chem. 2012, 287:7374-7387.
89. Pasquier J., Magal P., Boulange-Lecomte C., Webb G., Le Foll F. Consequences of cell-to-cell P-glycoprotein transfer on acquired multidrug resistance in breast cancer: a cell population dynamics model. Biol. Direct 2011, 6:5.
90. Peralta B., Gil-Carton D., Castano-Diez D., Bertin A., Boulogne C., Oksanen H.M., Bamford D.H., Abrescia N.G. Mechanism of membranous tunnelling nanotube formation in viral genome delivery. PLoS Biol. 2013, 11:e1001667.
91. Plotnikov E.Y., Khryapenkova T.G., Galkina S.I., Sukhikh G.T., Zorov D.B. Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture. Exp. Cell Res. 2010, 316:2447-2455.
92. Politis M., Lindvall O. Clinical application of stem cell therapy in Parkinson's disease. BMC Med. 2012, 10:1.
93. Quail D.F., Joyce J.A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 2013, 19:1423-1437.
94. Ramanan V.K., Saykin A.J. Pathways to neurodegeneration: mechanistic insights from GWAS in Alzheimer's disease, Parkinson's disease, and related disorders. Am. J. Neurodegener. Dis. 2013, 2:145-175.
95. Ratajczak J., Miekus K., Kucia M., Zhang J., Reca R., Dvorak P., Ratajczak M.Z. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006, 20:847-856.
96. Rego A.C., Oliveira C.R. Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochem. Res. 2003, 28:1563-1574.
97. Roberts K.L., Manicassamy B., Lamb R.A. Influenza A virus uses intercellular connections to spread to neighboring cells. J. Virol. 2015, 89:1537-1549.
98. Rojas-Rios P., Guerrero I., Gonzalez-Reyes A. Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila. PLoS Biol. 2012, 10:e1001298.
99. Rolf H.J., Niebert S., Niebert M., Gaus L., Schliephake H., Wiese K.G. Intercellular transport of Oct4 in mammalian cells: a basic principle to expand a stem cell niche?. PloS One 2012, 7:e32287.
100. Roma-Rodrigues C., Fernandes A.R., Baptista P.V. Exosome in tumour microenvironment: overview of the crosstalk between normal and cancer cells. BioMed Res. Int. 2014, 2014:179486.
101. Rosich L., Montraveta A., Xargay-Torrent S., Lopez-Guerra M., Roldan J., Aymerich M., Salaverria I., Bea S., Campo E., Perez-Galan P., Roue G., Colomer D. Dual PI3K/mTOR inhibition is required to effectively impair microenvironment survival signals in mantle cell lymphoma. Oncotarget 2014, 5:6788-6800.
102. Rozental R., Srinivas M., Gokhan S., Urban M., Dermietzel R., Kessler J.A., Spray D.C., Mehler M.F. Temporal expression of neuronal connexins during hippocampal ontogeny. Brain Res. Brain Res. Rev. 2000, 32:57-71.
103. Ruckes T., Saul D., Van Snick J., Hermine O., Grassmann R. Autocrine antiapoptotic stimulation of cultured adult T-cell leukemia cells by overexpression of the chemokine I-309. Blood 2001, 98:1150-1159.
104. Rustom A., Saffrich R., Markovic I., Walther P., Gerdes H.H. Nanotubular highways for intercellular organelle transport. Science 2004, 303:1007-1010.
105. Sarkar S., Horn G., Moulton K., Oza A., Byler S., Kokolus S., Longacre M. Cancer development, progression, and therapy: an epigenetic overview. Int. J. Mol. Sci. 2013, 14:21087-21113.
106. Schiller C., Diakopoulos K.N., Rohwedder I., Kremmer E., von Toerne C., Ueffing M., Weidle U.H., Ohno H., Weiss E.H. LST1 promotes the assembly of a molecular machinery responsible for tunneling nanotube formation. J. Cell Sci. 2013, 126:767-777.
107. Schneider A., Simons M. Exosomes: vesicular carriers for intercellular communication in neurodegenerative disorders. Cell Tissue Res. 2013, 352:33-47.
108. Seyed-Razavi Y., Hickey M.J., Kuffova L., McMenamin P.G., Chinnery H.R. Membrane nanotubes in myeloid cells in the adult mouse cornea represent a novel mode of immune cell interaction. Immunol. Cell Biol. 2013, 91:89-95.
109. Sherer N.M., Lehmann M.J., Jimenez-Soto L.F., Horensavitz C., Pypaert M., Mothes W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 2007, 9:310-315.
110. Simons K., Sampaio J.L. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 2011, 3:a004697.
111. Singh R., Nalwa H.S. Medical applications of nanoparticles in biological imaging, cell labeling, antimicrobial agents, and anticancer nanodrugs. J. Biomed. Nanotechnol. 2011, 7:489-503.
112. Sisakhtnezhad S., Matin M.M. Transdifferentiation: a cell and molecular reprogramming process. Cell Tissue Res. 2012, 348:379-396.
113. 2+ signals within tunneling membrane nanotubes. Biophys. J. 2011, 100:L37-L39.
114. Soltanian S., Matin M.M. Cancer stem cells and cancer therapy. Tumour Biol.: J. Int. Soc. Oncodev. Biol. Med. 2011, 32:425-440.
115. Sowinski S., Alakoskela J.M., Jolly C., Davis D.M. Optimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1. Methods 2011, 53:27-33.
116. Sowinski S., Jolly C., Berninghausen O., Purbhoo M.A., Chauveau A., Kohler K., Oddos S., Eissmann P., Brodsky F.M., Hopkins C., Onfelt B., Sattentau Q., Davis D.M. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 2008, 10:211-219.
117. Sun X., Wang Y., Zhang J., Tu J., Wang X.J., Su X.D., Wang L., Zhang Y. Tunneling-nanotube direction determination in neurons and astrocytes. Cell Death Dis. 2012, 3:e438.
118. Sweeney D., Raymer M.L., Lockwood T.D. Antidiabetic and antimalarial biguanide drugs are metal-interactive antiproteolytic agents. Biochem. Pharmacol. 2003, 66:663-677.
119. Takahashi A., Kukita A., Li Y.J., Zhang J.Q., Nomiyama H., Yamaza T., Ayukawa Y., Koyano K., Kukita T. Tunneling nanotube formation is essential for the regulation of osteoclastogenesis. J. Cell. Biochem. 2013, 114:1238-1247.
120. Tassew N.G., Mothe A.J., Shabanzadeh A.P., Banerjee P., Koeberle P.D., Bremner R., Tator C.H., Monnier P.P. Modifying lipid rafts promotes regeneration and functional recovery. Cell Rep. 2014, 8:1146-1159.
121. Teddy J.M., Kulesa P.M. In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 2004, 131:6141-6151.
122. Thayanithy V., Dickson E.L., Steer C., Subramanian S., Lou E. Tumor-stromal cross talk: direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes. Transl. Res. 2014, 164:359-365.
123. Tilney L.G., Portnoy D.A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 1989, 109:1597-1608.
124. Vallabhaneni K.C., Haller H., Dumler I. Vascular smooth muscle cells initiate proliferation of mesenchymal stem cells by mitochondrial transfer via tunneling nanotubes. Stem Cells Dev. 2012, 21:3104-3113.
125. van Dam E.M., Robinson P.J. Ral: mediator of membrane trafficking. Int. J. Biochem. Cell Biol. 2006, 38:1841-1847.
126. Van Prooyen N., Gold H., Andresen V., Schwartz O., Jones K., Ruscetti F., Lockett S., Gudla P., Venzon D., Franchini G. Human T-cell leukemia virus type 1 p8 protein increases cellular conduits and virus transmission. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20738-20743.
127. van Rooijen B.D., Claessens M.M., Subramaniam V. Membrane binding of oligomeric alpha-synuclein depends on bilayer charge and packing. FEBS Lett. 2008, 582:3788-3792.
128. Wang H., Duan L., Zou Z., Li H., Yuan S., Chen X., Zhang Y., Li X., Sun H., Zha H., Zhou L. Activation of the PI3K/Akt/mTOR/p70S6K pathway is involved in S100A4-induced viability and migration in colorectal cancer cells. Int. J. Med. Sci. 2014, 11:841-849.
129. Wang S., Qu X., Zhao R.C. Clinical applications of mesenchymal stem cells. J. Hematol. Oncol. 2012, 5:19.
130. Wang T., Xu Z., Jiang W., Ma A. Cell-to-cell contact induces mesenchymal stem cell to differentiate into cardiomyocyte and smooth muscle cell. Int. J. Cardiol. 2006, 109:74-81.
131. Wang X., Bukoreshtliev N.V., Gerdes H.H. Developing neurons form transient nanotubes facilitating electrical coupling and calcium signaling with distant astrocytes. PloS One 2012, 7:e47429.
132. Wang X., Gerdes H.H. Long-distance electrical coupling via tunneling nanotubes. Biochim. Biophys. Acta 2012, 1818:2082-2086.
133. Wang X., Gerdes H.H. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ. 2015, 22:1181-1191.
134. Wang X., Veruki M.L., Bukoreshtliev N.V., 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, 107:17194-17199.
135. Wang Y., Cui J., Sun X., Zhang Y. Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death Differ. 2011, 18:732-742.
136. 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, 6:10033-10041.
137. Watkins S.C., Salter R.D. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005, 23:309-318.
138. Wheaton W.W., Weinberg S.E., Hamanaka R.B., Soberanes S., Sullivan L.B., Anso E., Glasauer A., Dufour E., Mutlu G.M., Budigner G.S., Chandel N.S. Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis. eLife 2014, 3:e02242.
139. Winner B., Kohl Z., Gage F.H. Neurodegenerative disease and adult neurogenesis. Eur. J. Neurosci. 2011, 33:1139-1151.
140. Winner B., Winkler J. Adult neurogenesis in neurodegenerative diseases. Cold Spring Harb. Perspect. Biol. 2015, 7:a021287.
141. Wittig D., Wang X., Walter C., Gerdes H.H., Funk R.H., Roehlecke C. Multi-level communication of human retinal pigment epithelial cells via tunneling nanotubes. PloS One 2012, 7:e33195.
142. Xue G., Hemmings B.A. PKB/Akt-dependent regulation of cell motility. J. Natl. Cancer Instit. 2013, 105:393-404.
143. Yamanaka S. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 2012, 10:678-684.
144. Yasuda K., Khandare A., Burianovskyy L., Maruyama S., Zhang F., Nasjletti A., Goligorsky M.S. Tunneling nanotubes mediate rescue of prematurely senescent endothelial cells by endothelial progenitors: exchange of lysosomal pool. Aging 2011, 3:597-608.
145. You R., Li X., Xu Y., Liu Y., Lu S., Li M. The micropillar structure on silk fibroin film influence intercellular connection mediated by nanotubular structures. Materials 2014, 7:4628-4639.
146. Zhang J., Zhang Y. Membrane nanotubes: novel communication between distant cells. Sci. China Life Sci. 2013, 56:994-999.
147. Zhao H., Pykalainen A., Lappalainen P. I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr. Opin. Cell Biol. 2011, 23:14-21.
148. Zhao M., Song B., Pu J., Wada T., Reid B., Tai G., Wang F., Guo A., Walczysko P., Gu Y., Sasaki T., Suzuki A., Forrester J.V., Bourne H.R., Devreotes P.N., McCaig C.D., Penninger J.M. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 2006, 442:457-460.
149. Zhou H., Wu S., Joo J.Y., Zhu S., Han D.W., Lin T., Trauger S., Bien G., Yao S., Zhu Y., Siuzdak G., Scholer H.R., Duan L., Ding S. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009, 4:381-384.
150. Zhou S.F. Structure, function and regulation of P-glycoprotein and its clinical relevance in drug disposition. Xenobiot. 2008, 38:802-832.