Participation of Membrane Nanotubes in Intercellular Communication

[1] Abel M, Riese SR, Schlicker O, Bukoreshtliev N, Gerdes H, Spatz JP, Rustom A. Microstructured platforms to study nanotube-mediated long-distance cell-to-cell connections. Biointerphases 2011; 6: 22-31.10.1116/1.356741621428692Search in Google Scholar

[2] Abounit S, Zurzolo Ch. Wiring through tunneling nanotubes -from electrical signals to organelle transfer. J Cell Sci 2012; 125: 1089-1098.10.1242/jcs.08327922399801Search in Google Scholar

[3] Aguzzi A., Calella AM. Pr ions: Protein aggregation and infectious diseases. Physiol Rev 2009; 89: 1105-1152.10.1152/physrev.00006.200919789378Search in Google Scholar

[4] Arkwright PD, Luchetti F, Tour J, Roberts CH, Ayub R, Morales AP, Rodriguez J, Gilmore A, Canonico B, Papa S, Esposti MD. Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes. Cell Res 2010; 20:72-88.10.1038/cr.2009.112282270419770844Search in Google Scholar

[5] Baluska F, Hlavacka A, Volkmann D, Menzel D. Getting connected: actin-based cell-to-cell channels in plants and animals. Trends Cell Biol 2004; 14: 404-408.10.1016/j.tcb.2004.07.00115308205Search in Google Scholar

[6] Belting M, Wittrup A. Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease. J Cell Biol 2008; 183: 1187-1191.10.1083/jcb.200810038260696519103810Search in Google Scholar

[7] Brundin P, Melki R, Kopito R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Mol Cell. Biol 2010: 11: 301-307.10.1038/nrm2873289247920308987Search in Google Scholar

[8] Bukoreshtliev NV, Wang X, Hodneland E, Gurke S, Barroso J, Gerde HH. Selective block of tunneling nanotube (TNTS) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett 2009; 583: 1481-1488.10.1016/j.febslet.2009.03.06519345217Search in Google Scholar

[9] Chauveau A, Aucher A, Eissmann PH, Vivier E, Davis D. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. PNAS 2010; 107: 5545-5550.10.1073/pnas.0910074107285181120212116Search in Google Scholar

[10] Chen P, Hubner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol 2007; 81: 12582-12595.10.1128/JVI.00381-07216900717728240Search in Google Scholar

[11] 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: 5779-5783.10.4049/jimmunol.180.9.5779339217918424694Search in Google Scholar

[12] Cselenyak A, Pankkotai E, Horvath E, 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: 29.10.1186/1471-2121-11-29286933320406471Search in Google Scholar

[13] Daubeuf S, Aucher A, Bordier Ch, Salles A, Serre L, Gaibelet G, Faye J-Ch, Favre G, Joly E, Hudrisier D. Preferential transfer of certain plasma membrane proteins onto T and B cells by trogocytosis. PLoS ONE 2010; 5: e8716.10.1371/journal.pone.0008716280683520090930Search in Google Scholar

[14] Domhan S, Ma L, Tai A, Anaya Z, Beheshti A, Zeier M, Hlatky L, Abdollah I. Intercellular communication by exchange of cytoplasmic material via tunneling nanotube like structures in primary human renal epithelial cells. PLoS ONE 2011; 6: e21283 10.1371/journal.pone.0021283312449321738629Search in Google Scholar

[15] Dubey GP, Ben-Yehuda S. Intercellular nanotubes mediate bacterial communication. Cell 2011; 144: 590-600.10.1016/j.cell.2011.01.01521335240Search in Google Scholar

[16] Eugenin EA, Gaskill PJ, Berman JW. Tunneling nanotubes (TNTS) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell Immunol 2009; 254: 142-148.10.1016/j.cellimm.2008.08.005270134518835599Search in Google Scholar

[17] Gerdes HH, Bukoreshtliev NV, Barroso JF. Tunneling nanotubes: A new route for the exchange of components between animal cells. FEBS Lett 2007; 581: 2194-2201.10.1016/j.febslet.2007.03.07117433307Search in Google Scholar

[18] Goligorsky MS, Chen J, Patschan S. Stress-induced premature senescence of endothelial cells - a perilous state between recovery and point of no-return. Curr Opin Hematol 2009; 16: 215-219.10.1097/MOH.0b013e32832a07bd19318942Search in Google Scholar

[19] Gordon-Alonso M, Veiga E, Sanchez-Madrid F. Actin dynamics at the immunological synapse. Cell Health Cytoskel 2010; 2: 33-47.Search in Google Scholar

[20] Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT, Chenouard N, De Chaumont F, Martino A, Enninga J, Olivo-Marin JC, Mannel D, Zurzolo C. Prions hijack tunneling nanotubes for intercellular spread. Nat Cell Biol 2009; 11: 328-336.10.1038/ncb184119198598Search in Google Scholar

[21] Guescini M, Leo G, Genedani S, Carone S, Pederzoli F, Ciruela F, Guidolin D, Stocchi V, Mantuano M, Borroto-Escuela Do, Fuxe K, Agnati LF. Microvesicle and tunneling nanotube mediated intercellular transfer of g-protein coupled receptors in cell cultures. Exp Cell Res 2012; 318: 603-613.10.1016/j.yexcr.2012.01.00522266577Search in Google Scholar

[22] Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, Kitamura H, Ito M, Watarai H, Hazelett Cc, Yeaman Ch, Ohno H. M-Sec promotes membrane nanotube formation by interacting with RaI and the exocyst complex. Nat Cell Biol 2009; 11: 1427-1432.10.1038/ncb199019935652Search in Google Scholar

[23] He K, Luo W, Zhang Y, Liu F, Liu D, Xu L, Qin L, Xiong C, Lu Z, Fang X, Zhang Y. Intercellular transportation of quantum dots mediated by membrane nanotubes. ACS Nano 2010; 4: 3015-3022.10.1021/nn100219820524630Search in Google Scholar

[24] He Y, Wu J, Dressman DC, Iacobuzio-Donahue CH, Markowitz SD, Velculescu VE, Diaz LA, Kinzler KW, Vogelstein B, Papadopoulos N. Heteroplasmic mitochondrial DNA mutations in normal and tumor cells. Nature 2010; 464: 610-614.10.1038/nature08802317645120200521Search in Google Scholar

[25] He K, 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: 39-47.10.1093/cvr/cvr18921719573Search in Google Scholar

[26] Hodneland E, Lundervold A, Gurke S, Tai XCh, Rustom A, Gerdes HH. Automated detection of tunneling nanotubes in 3D images. Cytom Part A 2006; 69A: 961-972.10.1002/cyto.a.2030216969816Search in Google Scholar

[27] Hurtig J, Chiu DT, Onfelt B. Intercellular nanotubes: insights from imaging studies and beyond. Wiley Interdiscip Rev Nanomed Nanobiotech 2010; 2: 260-276.10.1002/wnan.80560258220166114Search in Google Scholar

[28] Kabaso D, Lokar M, Kralj-Iglic V, Veranic P, Iglic A. Temperature and cholera toxin B are factors that influence formation of membrane nanotubues in RT4 and T24 urothelial cancer cell lines. Int J NanoMedicine 2011; 6:495-509.10.2147/IJN.S16982306579621468353Search in Google Scholar

[29] Kabaso D, Bobrovska N, Góźdź W, Gov N, Kralj-Iglic V, Veranic P, Iglic A. On the role of membrane anisotropy and BAR proteins in the stability of tubular membrane structures. J Biomech 2012; 45: 231-238.10.1016/j.jbiomech.2011.10.03922138195Search in Google Scholar

[30] Kabaso D, Bobrovska N, Góźdź W, Gongadze E, Kralj-Iglic V, Zorec R, Iglic A. The transport along membrane nanotubes driven by the spontaneous curvature of membrane components. Bioelectrochemistry 2012; 87: 204-210.10.1016/j.bioelechem.2012.02.00922502994Search in Google Scholar

[31] Kadiu I, Gendelman HE. Macrophage bridging conduit trafficking of HIV-1 through the endoplasmic reticulum and Golgi network. J Proteome Res 2011; 10: 3225-3238.10.1021/pr200262q312846321563830Search in Google Scholar

[32] Kadiu I, Gendelman HE. Human Immunodeficiency virus type 1 endocytic trafficking through macrophage bridging conduits facilitates spread of infection. J Neuroimmune Pharmacol 2011; 6: 658-675.10.1007/s11481-011-9298-z323257021789505Search in Google Scholar

[33] Kimura S, Hase K, Ohno H. Tunnel ing nanot ubes: Emerging view of their molecular components and formation mechanisms. Exp Cell Res 2012; 318: 1699-1706.10.1016/j.yexcr.2012.05.01322652450Search in Google Scholar

[34] Langevin CH, Gousset K, Costanzo M, Richard-Le Goff O, Zurzolo C. Characterization of the role of dendritic cells in prion transfer to primary neurons. Biochem J 2010; 431: 189-198. 10.1042/BJ2010069820670217Search in Google Scholar

[35] Lee TH, D`Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J . Microvesicles as mediators of intercellular communication in cancer -the emerging sciene of cellular “debris”. Semin Immunopathol 2011; 33:455-467.10.1007/s00281-011-0250-321318413Search in Google Scholar

[36] Lokar M, Iglic A, Veranic P. Protruding membrane nanotubes: attachment of tubular protrusions to adjacent cells by several anchoring junctions. Protoplasma 2010; 246: 81-87.10.1007/s00709-010-0143-720526853Search in Google Scholar

[37] Lokar M, Kabaso D, Resnik N, Sepcic K, Kralj-Iglic V, Veranic P, Zorec R, Iglic A. The rol e of cholesterol-sphingomyelin membrane nanodomains in the stability of intercellular membrane nanotubes. Int J Nanomed 2012; 7: 1891-1902.Search in Google Scholar

[38] Lou E, Fujisawa S, Morozov A, Barlas A, Romin Y, Dogan Y, Gholami S, Moreira A, Manova- Todorova K, Moore MA. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS ONE 2012; 7: e33093.10.1371/journal.pone.0033093330286822427958Search in Google Scholar

[39] Lou E, Fujisawa S, Barlos A, Romin Y, Manova-Todorova K, Moore MA, Subramanian S. Tunneling nanotubes: A new paradigm for studying intercellular communication and therapeutics in cancer. Commun Integr Biol 2012; 5: 399-403 .10.4161/cib.20569346085023060969Search in Google Scholar

[40] Luchetti F, Canonico B, Arcangeletti M, Guescini M, Cesarini E, Stocchi V, Degli Esposti M, Papa S. Fas signaling promotes intercellular communication in T cells. PLoS ONE 2012; 7: e35766.10.1371/journal.pone.0035766333845722558220Search in Google Scholar

[41] Marzo L, Gousset K, Zurzolo Ch. Multifaceted roles of tunneling nanotubes in intercellular communication. Front Physiol 2012; 3: 1-14.10.3389/fphys.2012.00072332252622514537Search in Google Scholar

[42] Mathivanan S, Ji H, Simpson RJ. Exosomes: Extracellular organelles important in intercellular communication. J Proteomics 2010; 73: 1907-1920.10.1016/j.jprot.2010.06.00620601276Search in Google Scholar

[43] Mcgowan M. Tunnel ing nanot ubes -cr ossing t he br idge. J Cell Mol Biol 2011; 9: 11-18.Search in Google Scholar

[44] Mi L, Xiong R, Zhang Y, Li Z, Yang W, Chen J, Wang P. Microscopic observat ion of t he int er cel lular transport of CdTe quantum dot aggregates through tunneling-nanotubes. J Biomat Nanobiotech 2011; 2: 173-180.10.4236/jbnb.2011.22022Search in Google Scholar

[45] Nakamura K, Nemani VM, Azarbal F, Skibinski G, Levy JM, Egami K, Munishkina L, Zhang J, Gardner B, Wakabayashi J, Sesaki H, Cheng Y, Finkbeiner S, Nussbaum RL, Masliah E, Edwards RH. Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein α-synuclein. J Biol Chem 2011; 286: 20710-20726.10.1074/jbc.M110.213538312147221489994Search in Google Scholar

[46] Niu X, Gupta K, Yang Jt, Shamblott MJ, Levchenko A. Physical transfer of membrane and cytoplasmic components as a general mechanism of cell-cell communication. J. Cell Sci 2008; 122: 600-610.10.1242/jcs.03142719208767Search in Google Scholar

[47] Ohno H, Hase K, Kimura S. Emerging secrets of tunneling nanotube formation. Commum Integr Biol. 2010; 3: 231-233.10.4161/cib.3.3.11242291876320714400Search in Google Scholar

[48] Onfelt B, Nedvetzki S, Benninger RK, Purbhoo MA, Sowinski S, Hume AN, Seabra MC, Neil MA, French PM, Davis D. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol 2006; 177: 8476-8483.10.4049/jimmunol.177.12.847617142745Search in Google Scholar

[49] 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: 1-18.10.1186/1745-6150-6-5303898821269489Search in Google Scholar

[50] 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: 7374-7387.10.1074/jbc.M111.312157329353722228759Search in Google Scholar

[51] Patschan S, Chen J, Gealekman O, Krupincza K, Wang M, Shu L, Shayman JA, Goligorsky MS. Mechanisms of premature cell senescence: lysosomal dysfunction and ganglioside accumulation in endothelial cells. Am J Physiol Renal Physiol 2008; 294: 100-109.10.1152/ajprenal.00261.200717928415Search in Google Scholar

[52] Plotnikov EY, Khryapenkova TG, Galkina SI, Sukhikh GT, Zorov DB. Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture. Exp Cell Res 2010; 316: 2447-2455.10.1016/j.yexcr.2010.06.00920599955Search in Google Scholar

[53] Rechavi O, Goldstein I, Kloog Y. Intercellular exchange of proteins: The immune cell habit of sharing. FEBS Lett 2009; 583: 1792-1799. 10.1016/j.febslet.2009.03.01419289124Search in Google Scholar

[54] Ridley AJ. Life at the leading edge. Cell 2011; 145: 1012-1022.10.1016/j.cell.2011.06.01021703446Search in Google Scholar

[55] Roda-Navarro P, Reyburn HT. Intercellular protein transfer at the NK cell immune synapse: mechanisms and physiological significance. FASEB J 2007; 21: 1636-1646.10.1096/fj.06-7488rev17314139Search in Google Scholar

[56] Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, Prevost M-Ch, Estaquier J, Haase AT, Sol-Foulon N, Schwartz O. Simultaneous cell-to-cell transmission of Human Immunodeficiency Virus to multiple targets through polysynapses. J Virol 2009; 83: 6234-6246.10.1128/JVI.00282-09268737919369333Search in Google Scholar

[57] Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004; 303:1007-1010.10.1126/science.109313314963329Search in Google Scholar

[58] Rustom A. Hen or Egg? Some thoughts on tunneling nanotubes. Nat Genetic Engin Nat Genome 2009; 1178: 129-136.Search in Google Scholar

[59] Schiller Ch, Huber JE, Diakopoulos KN, Weiss EH. Tunneling nanotubes enable intercellular transfer of MHC class I molecules. Hum Immunol 2013; 74: 412-416.10.1016/j.humimm.2012.11.02623228397Search in Google Scholar

[60] Sharom FJ. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 2008; 9: 105-127.10.2217/14622416.9.1.10518154452Search in Google Scholar

[61] Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz Ch, Pypaert M, Mothes W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol 2007; 9: 310-315.10.1038/ncb1544262897617293854Search in Google Scholar

[62] Sherer NM, Mothes W. Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends Cell Biol 2008; 9: 414-420.Search in Google Scholar

[63] Simons K, Sampaio JL. Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 2011; 3: a004697.10.1101/cshperspect.a004697317933821628426Search in Google Scholar

[64] Singh R, Nalwa HS. Medical applications of nanoparticles in biological imaging, cell labeling, antimicrobial agents and anticancer nanodrugs. J Biomed Nanotechnol 2011; 7: 489-503.10.1166/jbn.2011.132421870454Search in Google Scholar

[65] Smith IF, Shai J, Parker I. Active generation and propagation of Ca2+ signals within tunneling membrane nanotubes. Biophys J 2011; 100: L37-L39.10.1016/j.bpj.2011.03.007307770121504718Search in Google Scholar

[66] Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Kohler K, Oddos S, Eissmann PH, Brodsky FM, Hopkins C, Onfelt B, Sattentau Q, Davis D. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nature Cell Biol 2008; 10: 211-219.10.1038/ncb168218193035Search in Google Scholar

[67] Sowinski S, Alakoskela JM, Jolly C, Davis D. Optimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1. Methods 2011; 53: 27-33.10.1016/j.ymeth.2010.04.00220382227Search in Google Scholar

[68] Stinchcombe JC, Salio M, Cerundolo V, Pende D, Arico M, Griffiths GM. Centriole polarization to the immunological synapse direct secretion from cytolytic cells of both the innate and adaptive immune systems. BMC Biol 2011; 9: 45-52.10.1186/1741-7007-9-45314959721711522Search in Google Scholar

[69] Su B, Wang X, Nunomura A, Moreira PI, Lee HG, Perry G, Smith Ma, Zhu X. Oxidat ive st r ess signaling in Alzheimer`s disease. Curr Alzheimer Res 2008; 5: 525-532.10.2174/156720508786898451278001519075578Search in Google Scholar

[70] Takahashi A, Kukita A, Zhang J, Nomiyama H, Yamaza T, Ayukawa Y, Koyano K, Kukita T. Tunneling nanotube formation is essential for the regulation of osteoclastogenesis. J Cell Biochem 2012 /doi/ 10.1002/jcb.24433.10.1002/jcb.2443323129562Search in Google Scholar

[71] Veranic P, Lokar M, Schutz Gj, Weghuber J, Wieser S, Hagerstrand H. Different types of cell-tocell connections mediated by nanotubular structures. Biophys J 2008; 95:4416-4425.10.1529/biophysj.108.131375256792418658210Search in Google Scholar

[72] Wang X, Veruki ML, Bukoreshtliev NV, Hartveit E, Gerdes HH. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. PNAS 2010; 107: 17194-17199.10.1073/pnas.1006785107295145720855598Search in Google Scholar

[73] Wang Y, Cui J, Sun X, Zhang Y. Tunneling nanotube development in astrocytes depends on p53 activation. Cell Death Differ 2011; 18: 732-742.10.1038/cdd.2010.147313190421113142Search in Google Scholar

[74] Wang ZG, Liu SL, Tian ZQ, Zhang ZL, Tang HW, Pang DW. Myosin-driven intercellular transportation of wheat germ agglutinin mediated by membrane nanotubes between human lung cancer cells. ACS Nano 2012; 6: 10033-10041.10.1021/nn303729r23102457Search in Google Scholar

[75] Wittig D, Wang X, Walter C, Gerdes HH, Funk RH, Roehlecke C. Multi-level communication of human retinal pigment epithelial cells via tunneling nanotubes. PLoS ONE 2012; 7: e33195. 10.1371/journal.pone.0033195331086522457742Search in Google Scholar

[76] Yao J, Oite T, Kitamura M. Gap junctional intercellular communication in the juxtaglomerular apparatus. Am J Physiol Renal Physiol 2009; 296: F939-F946.10.1152/ajprenal.90612.200819073638Search in Google Scholar

[77] Yasuda K, Park HCh, Ratliff B, Addabbo F, Hatzopoulos K, Chander P, Goligorsky MS. Adr iamycin nephropathy. A failure of endothelial progenitor cell-induced repair. Am J Pathol 2010; 176: 1685-1695.10.2353/ajpath.2010.091071284346020167859Search in Google Scholar

[78] Yasuda K, Khandare A, Burianovskyy L, Maruyama S, Zhan F, Nasjletti A, Goligorsky MS. Tunneling nanotubes mediate rescue of prematurely senescent endothelial cells by endothelial progenitors: exchange of lysosomal pool. Aging 2011; 3: 597-608.10.18632/aging.100341316436821705809Search in Google Scholar

[79] Zani BG, Indofli L, Edelman ER. Tubular bridges for bronchial epithelial cell migration and communication. PLoS ONE 2010; 5: e8930.10.1371/journal.pone.0008930281249320126618Search in Google Scholar

[80] Zhao H, Pykalainen A, Lappalainen P. I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr Opin Cell Biol 2011; 23: 14-21. 10.1016/j.ceb.2010.10.00521093245Search in Google Scholar