Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 13 February 2004:
Vol. 303. no. 5660, pp. 1007 - 1010
DOI: 10.1126/science.1093133
Prev | Table of Contents | Next

Reports

Nanotubular Highways for Intercellular Organelle Transport

Amin Rustom,1 Rainer Saffrich,2 Ivanka Markovic,3 Paul Walther,4 Hans-Hermann Gerdes1,5*

Cell-to-cell communication is a crucial prerequisite for the development and maintenance of multicellular organisms. To date, diverse mechanisms of intercellular exchange of information have been documented, including chemical synapses, gap junctions, and plasmodesmata. Here, we describe highly sensitive nanotubular structures formed de novo between cells that create complex networks. These structures facilitate the selective transfer of membrane vesicles and organelles but seem to impede the flow of small molecules. Accordingly, we propose a novel biological principle of cell-to-cell interaction based on membrane continuity and intercellular transfer of organelles.

1 Interdisciplinary Center of Neuroscience (IZN), Institute of Neurobiology, University of Heidelberg, INF 364, Heidelberg 69120, Germany.
2 Otto-Meyerhoff-Zentrum, University of Heidelberg, INF 350, Heidelberg 69120, Germany.
3 Institute of Biochemistry, Faculty of Medicine, University of Belgrade, Pasterova 2, Belgrade 11000, Yugoslavia.
4 Electron Microscopy Facility, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany.
5 Institute for Biochemistry and Molecular Biology, University of Bergen, Jonas Lies vei 91, Bergen 5009, Norway.

* To whom correspondence should be addressed. E-mail: Hans-Hermann.Gerdes{at}ibmb.uib.no

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Physical transfer of membrane and cytoplasmic components as a general mechanism of cell-cell communication.
X. Niu, K. Gupta, J. T. Yang, M. J. Shamblott, and A. Levchenko (2009)
J. Cell Sci. 122, 600-610
   Abstract »    Full Text »    PDF »
Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease.
M. Belting and A. Wittrup (2008)
J. Cell Biol. 183, 1187-1191
   Abstract »    Full Text »    PDF »
Extensive and bidirectional transfer of major histocompatibility complex class II molecules between donor and recipient cells in vivo following solid organ transplantation.
K. Brown, S. H. Sacks, and W. Wong (2008)
FASEB J 22, 3776-3784
   Abstract »    Full Text »    PDF »
Schwann Cell to Axon Transfer of Ribosomes: Toward a Novel Understanding of the Role of Glia in the Nervous System.
F. A. Court, W. T. J. Hendriks, H. D. MacGillavry, J. Alvarez, and J. van Minnen (2008)
J. Neurosci. 28, 11024-11029
   Abstract »    Full Text »    PDF »
Cutting Edge: Membrane Nanotubes In Vivo: A Feature of MHC Class II+ Cells in the Mouse Cornea.
H. R. Chinnery, E. Pearlman, and P. G. McMenamin (2008)
J. Immunol. 180, 5779-5783
   Abstract »    Full Text »    PDF »
RNAs as extracellular signaling molecules.
M. E Dinger, T. R Mercer, and J. S Mattick (2008)
J. Mol. Endocrinol. 40, 151-159
   Abstract »    Full Text »    PDF »
Local Gene Expression in Axons and Nerve Endings: The Glia-Neuron Unit.
A. Giuditta, J. Tai Chun, M. Eyman, C. Cefaliello, A. P. Bruno, and M. Crispino (2008)
Physiol Rev 88, 515-555
   Abstract »    Full Text »    PDF »
Bystander B cells rapidly acquire antigen receptors from activated B cells by membrane transfer.
B. J. C. Quah, V. P. Barlow, V. McPhun, K. I. Matthaei, M. D. Hulett, and C. R. Parish (2008)
PNAS 105, 4259-4264
   Abstract »    Full Text »    PDF »
Horizontal gene transfer from human endothelial cells to rat cardiomyocytes after intracoronary transplantation.
S. Burghoff, Z. Ding, S. Godecke, A. Assmann, A. Wirrwar, D. Buchholz, O. Sergeeva, C. Leurs, H. Hanenberg, H.-W. Muller, et al. (2008)
Cardiovasc Res 77, 534-543
   Abstract »    Full Text »    PDF »
Nonspecific CD4+ T cells with uptake of antigen-specific dendritic cell-released exosomes stimulate antigen-specific CD8+ CTL responses and long-term T cell memory.
S. Hao, J. Yuan, and J. Xiang (2007)
J. Leukoc. Biol. 82, 829-838
   Abstract »    Full Text »    PDF »
Antigen Transmission by Replicating Antigen-Bearing Dendritic Cells.
J. Diao, E. Winter, W. Chen, F. Xu, and M. S. Cattral (2007)
J. Immunol. 179, 2713-2721
   Abstract »    Full Text »    PDF »
The effect of cellular cholesterol on membrane-cytoskeleton adhesion.
M. Sun, N. Northup, F. Marga, T. Huber, F. J. Byfield, I. Levitan, and G. Forgacs (2007)
J. Cell Sci. 120, 2223-2231
   Abstract »    Full Text »    PDF »
Intercellular protein transfer at the NK cell immune synapse: mechanisms and physiological significance.
P. Roda-Navarro and H. T. Reyburn (2007)
FASEB J 21, 1636-1646
   Abstract »    Full Text »    PDF »
Plasma Membrane Sterol Distribution Resembles the Surface Topography of Living Cells.
D. Wustner (2007)
Mol. Biol. Cell 18, 211-228
   Abstract »    Full Text »    PDF »
Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria.
B. Onfelt, S. Nedvetzki, R. K. P. Benninger, M. A. Purbhoo, S. Sowinski, A. N. Hume, M. C. Seabra, M. A. A. Neil, P. M. W. French, and D. M. Davis (2006)
J. Immunol. 177, 8476-8483
   Abstract »    Full Text »    PDF »
The physiological roles of extracellular metallothionein..
M. A. Lynes, K. Zaffuto, D. W. Unfricht, G. Marusov, J. S. Samson, and X. Yin (2006)
Experimental Biology and Medicine 231, 1548-1554
   Abstract »    Full Text »    PDF »
The Spread of Rice Dwarf Virus among Cells of Its Insect Vector Exploits Virus-Induced Tubular Structures..
T. Wei, A. Kikuchi, Y. Moriyasu, N. Suzuki, T. Shimizu, K. Hagiwara, H. Chen, M. Takahashi, T. Ichiki-Uehara, and T. Omura (2006)
J. Virol. 80, 8593-8602
   Abstract »    Full Text »    PDF »
Transfer of NKG2D and MICB at the cytotoxic NK cell immune synapse correlates with a reduction in NK cell cytotoxic function.
P. Roda-Navarro, M. Vales-Gomez, S. E. Chisholm, and H. T. Reyburn (2006)
PNAS 103, 11258-11263
   Abstract »    Full Text »    PDF »
Hydrodynamic narrowing of tubes extruded from cells.
F. Brochard-Wyart, N. Borghi, D. Cuvelier, and P. Nassoy (2006)
PNAS 103, 7660-7663
   Abstract »    Full Text »    PDF »
FUS1 Regulates the Opening and Expansion of Fusion Pores between Mating Yeast.
S. Nolan, A. E. Cowan, D. E. Koppel, H. Jin, and E. Grote (2006)
Mol. Biol. Cell 17, 2439-2450
   Abstract »    Full Text »    PDF »
Cell-Cell Communication Beyond Connexins: The Pannexin Channels.
M. T. Barbe, H. Monyer, and R. Bruzzone (2006)
Physiology 21, 103-114
   Abstract »    Full Text »    PDF »
Intercellular communication in plants. Annual Plant Reviews Vol 16 * Fleming AJ. (ed). 2005. Oxford/Boca Raton: Blackwell Publishing/CRC Press. {pound}105.00 (hardback). 280 pp.
F. Baluska (2006)
Ann. Bot. 97, 675-676
   Full Text »    PDF »
Stable and robust polymer nanotubes stretched from polymersomes.
J. E. Reiner, J. M. Wells, R. B. Kishore, C. Pfefferkorn, and K. Helmerson (2006)
PNAS 103, 1173-1177
   Abstract »    Full Text »    PDF »
Mitochondrial transfer between cells can rescue aerobic respiration.
J. L. Spees, S. D. Olson, M. J. Whitney, and D. J. Prockop (2006)
PNAS 103, 1283-1288
   Abstract »    Full Text »    PDF »
Long-Distance Calls Between Cells Connected by Tunneling Nanotubules.
B. Onfelt, M. A. Purbhoo, S. Nedvetzki, S. Sowinski, and D. M. Davis (2005)
Sci. STKE 2005, pe55
   Abstract »    Full Text »    PDF »
Actin Cytoskeleton Is Involved in Targeting of a Viral Hsp70 Homolog to the Cell Periphery.
A. I. Prokhnevsky, V. V. Peremyslov, and V. V. Dolja (2005)
J. Virol. 79, 14421-14428
   Abstract »    Full Text »    PDF »
Cardiac Stem Cells and Mechanisms of Myocardial Regeneration.
A. Leri, J. Kajstura, and P. Anversa (2005)
Physiol Rev 85, 1373-1416
   Abstract »    Full Text »    PDF »
Partial cell fusion: A newly recognized type of communication between dedifferentiating cardiomyocytes and fibroblasts.
R. B. Driesen, G. D. Dispersyn, F. K. Verheyen, S. M. van den Eijnde, L. Hofstra, F. Thone, P. Dijkstra, W. Debie, M. Borgers, and F. C.S. Ramaekers (2005)
Cardiovasc Res 68, 37-46
   Abstract »    Full Text »    PDF »
GLUT1CBP(TIP2/GIPC1) Interactions with GLUT1 and Myosin VI: Evidence Supporting an Adapter Function for GLUT1CBP.
B. C. Reed, C. Cefalu, B. H. Bellaire, J. A. Cardelli, T. Louis, J. Salamon, M. A. Bloecher, and R. C. Bunn (2005)
Mol. Biol. Cell 16, 4183-4201
   Abstract »    Full Text »    PDF »
Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes.
D. Zhu, K. S. Tan, X. Zhang, A. Y. Sun, G. Y. Sun, and J. C.-M. Lee (2005)
J. Cell Sci. 118, 3695-3703
   Abstract »    Full Text »    PDF »
Single-file electrophoretic transport and counting of individual DNA molecules in surfactant nanotubes.
M. Tokarz, B. Akerman, J. Olofsson, J.-F. Joanny, P. Dommersnes, and O. Orwar (2005)
PNAS 102, 9127-9132
   Abstract »    Full Text »    PDF »
Cell-to-Cell Connection of Endothelial Progenitor Cells With Cardiac Myocytes by Nanotubes: A Novel Mechanism for Cell Fate Changes?.
M. Koyanagi, R. P. Brandes, J. Haendeler, A. M. Zeiher, and S. Dimmeler (2005)
Circ. Res. 96, 1039-1041
   Abstract »    Full Text »    PDF »
Uptake and Neuritic Transport of Scrapie Prion Protein Coincident with Infection of Neuronal Cells.
A. C. Magalhaes, G. S. Baron, K. S. Lee, O. Steele-Mortimer, D. Dorward, M. A. M. Prado, and B. Caughey (2005)
J. Neurosci. 25, 5207-5216
   Abstract »    Full Text »    PDF »
Evolution of gap junction proteins - the pannexin alternative.
Y. V. Panchin (2005)
J. Exp. Biol. 208, 1415-1419
   Abstract »    Full Text »    PDF »
Not just another hole in the wall: understanding intercellular protein trafficking.
K. L. Gallagher and P. N. Benfey (2005)
Genes & Dev. 19, 189-195
   Abstract »    Full Text »    PDF »
Cutting Edge: Membrane Nanotubes Connect Immune Cells.
B. Onfelt, S. Nedvetzki, K. Yanagi, and D. M. Davis (2004)
J. Immunol. 173, 1511-1513
   Abstract »    Full Text »    PDF »
Eukaryotic Cells and their Cell Bodies: Cell Theory Revised.
F. BALUSKA, D. VOLKMANN, and P. W. BARLOW (2004)
Ann. Bot. 94, 9-32
   Abstract »    Full Text »    PDF »
Mechanical tweezer action by self-tightening knots in surfactant nanotubes.
T. Lobovkina, P. Dommersnes, J.-F. Joanny, P. Bassereau, M. Karlsson, and O. Orwar (2004)
PNAS 101, 7949-7953
   Abstract »    Full Text »    PDF »
A dynamite intercellular highway.
N. LeBrasseur (2004)
J. Cell Biol. 164, 795
   Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)