C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction

Experimental Cell Research

Volumn 316, Issue 12, 2010, Pages 1977-1984

  Guescini, M ^a   Guidolin, D ^b   Vallorani, L ^a   Casadei, L ^a   Gioacchini, A M ^a   Tibollo, P ^a   Battistelli, M ^a   Falcieri, E ^a,c   Battistin, L ^d   Agnati, L F ^d   Stocchi, V ^a  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c CNR   (Italy)

^d IRCCS SAN CAMILLO HOSPITAL   (Italy)

Author keywords

Bioinformatics analysis; Exosomes; Inter cellular communication; Mitochondrial DNA; Myoblasts

Indexed keywords

MITOCHONDRIAL DNA; SOMATOMEDIN C;

APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL STRAIN; EXOSOME; MYOBLAST; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DATABASE; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME OF FLIGHT MASS SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY;

EID: 77953356673     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.04.006     Document Type: Article

References (49)

1. Chan M.H., Carey A.L., Watt M.J., Febbraio M.A. Cytokine gene expression in human skeletal muscle during concentric contraction: evidence that IL-8, like IL-6, is influenced by glycogen availability. Am. J. Physiol. 2004, 287:R322-R327.
2. Cuppini R., Sartini S., Agostini D., Guescini M., Ambrogini P., Betti M., Bertini L., Vallasciani M., Stocchi V. Bdnf expression in rat skeletal muscle after acute or repeated exercise. Arch. Ital. Biol. 2007, 145:99-110.
3. Akerstrom T., Steensberg A., Keller P., Keller C., Penkowa M., Pedersen B.K. Exercise induces interleukin-8 expression in human skeletal muscle. J. Physiol. 2005, 563:507-516.
4. Febbraio M.A., Hiscock N., Sacchetti M., Fischer C.P., Pedersen B.K. Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 2004, 53:1643-1648.
5. Izumiya Y., Bina H.A., Ouchi N., Akasaki Y., Kharitonenkov A., Walsh K. FGF21 is an Akt-regulated myokine. FEBS Lett. 2008, 582:3805-3810.
6. Ouchi N., Oshima Y., Ohashi K., Higuchi A., Ikegami C., Izumiya Y., Walsh K. Follistatin-like 1, a secreted muscle protein, promotes endothelial cell function and revascularization in ischemic tissue through a nitric-oxide synthase-dependent mechanism. J. Biol. Chem. 2008, 283:32802-32811.
7. Pedersen B.K., Febbraio M.A. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev. 2008, 88:1379-1406.
8. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009, 19:43-51.
9. van Niel G., Porto-Carreiro I., Simoes S., Raposo G. Exosomes: a common pathway for a specialized function. J. Biochem. 2006, 140:13-21.
10. Lakkaraju A., Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol. 2008, 18:199-209.
11. Smalheiser N.R. Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol. Direct 2007, 2:35.
12. Faure J., Lachenal G., Court M., Hirrlinger J., Chatellard-Causse C., Blot B., Grange J., Schoehn G., Goldberg Y., Boyer V., Kirchhoff F., Raposo G., Garin J., Sadoul R. Exosomes are released by cultured cortical neurones. Mol. Cell. Neurosci. 2006, 31:642-648.
13. Fevrier B., Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 2004, 16:415-421.
14. Simons M., Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21:575-581.
15. Guescini M., Genedani S., Stocchi V., Agnati L.F. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J. Neural Transm. 2010, 117:1-4.
16. Agnati L.F., Leo G., Genedani S., Andreoli N., Marcellino D., Woods A., Piron L., Guidolin D., Fuxe K. Structural plasticity in G-protein coupled receptors as demonstrated by the allosteric actions of homocysteine and computer-assisted analysis of disordered domains. Brain Res. Rev. 2008, 58:459-474.
17. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. 2005, 6:197-208.
18. Uversky V.N., Oldfield C.J., Dunker A.K. Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu. Rev. Biophys, 2008, 37:215-246.
19. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
20. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
21. Dunker A.K., Brown C.J., Obradovic Z. Identification and functions of usefully disordered proteins. Adv. Protein Chem. 2002, 62:25-49.
22. Linding R., Russell R.B., Neduva V., Gibson T.J. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 2003, 31:3701-3708.
23. Linding R., Jensen L.J., Diella F., Bork P., Gibson T.J., Russell R.B. Protein disorder prediction: implications for structural proteomics. Structure 2003, 11:1453-1459.
24. Zeev-Ben-Mordehai T., Rydberg E.H., Solomon A., Toker L., Auld V.J., Silman I., Botti S., Sussman J.L. The intracellular domain of the Drosophila cholinesterase-like neural adhesion protein, gliotactin, is natively unfolded. Proteins 2003, 53:758-767.
25. Sanchez de Groot N., Pallares I., Aviles F.X., Vendrell J., Ventura S. Prediction of hot spots of aggregation in disease-linked polypeptides. BMC Struct. Biol. 2005, 5:18.
26. Conchillo-Sole O., de Groot N.S., Aviles F.X., Vendrell J., Daura X., Ventura S. AGGRESCAN: a server for the prediction and evaluation of hot spots of aggregation in polypeptides. BMC Bioinformatics 2007, 8:65.
27. Colquhoun D. Lectures in Biostatistics 1971, Clarendon Press, Oxford.
28. Pedersen B.K., Steensberg A., Fischer C., Keller C., Keller P., Plomgaard P., Febbraio M., Saltin B. Searching for the exercise factor: is IL-6 a candidate?. J. Muscle Res. Cell Motil. 2003, 24:113-119.
29. Febbraio M.A., Pedersen B.K. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J. 2002, 16:1335-1347.
30. Pedersen B.K., Steensberg A., Fischer C., Keller C., Keller P., Plomgaard P., Wolsk-Petersen E., Febbraio M. The metabolic role of IL-6 produced during exercise: is IL-6 an exercise factor?. Proc. Nutr. Soc. 2004, 63:263-267.
31. Nielsen A.R., Mounier R., Plomgaard P., Mortensen O.H., Penkowa M., Speerschneider T., Pilegaard H., Pedersen B.K. Expression of interleukin-15 in human skeletal muscle effect of exercise and muscle fibre type composition. J. Physiol. 2007, 584:305-312.
32. Pedersen B.K., Edward F. Adolph Distinguished Lecture: Muscle as an Endocrine Organ: IL-6 and Other Myokines. J. Appl. Physiol. 2009, 107:1006-1014.
33. 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.
34. Mallegol J., Van Niel G., Lebreton C., Lepelletier Y., Candalh C., Dugave C., Heath J.K., Raposo G., Cerf-Bensussan N., Heyman M. T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 2007, 132:1866-1876.
35. Schorey J.S., Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic (Copenhagen, Denmark) 2008, 9:871-881.
36. Raiborg C., Rusten T.E., Stenmark H. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 2003, 15:446-455.
37. Thery C., Zitvogel L., Amigorena S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2:569-579.
38. Fink A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des. 1998, 3:R9-R23.
39. Duan C. Specifying the cellular responses to IGF signals: roles of IGF-binding proteins. J. Endocrinol. 2002, 175:41-54.
40. Duan C., Xu Q. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen. Comp. Endocrinol. 2005, 142:44-52.
41. Choi Y.S., Ryu B.K., Min H.K., Lee S.W., Pak Y.K. Analysis of proteome bound to D-loop region of mitochondrial DNA by DNA-linked affinity chromatography and reverse-phase liquid chromatography/tandem mass spectrometry. Ann. N. Y. Acad. Sci. 2005, 1042:88-100.
42. Herbst A., Pak J.W., McKenzie D., Bua E., Bassiouni M., Aiken J.M. Accumulation of mitochondrial DNA deletion mutations in aged muscle fibers: evidence for a causal role in muscle fiber loss. J. Gerontol. 2007, 62:235-245.
43. 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.
44. Rustom A., Saffrich R., Markovic I., Walther P., Gerdes H.H. Nanotubular highways for intercellular organelle transport. Science (New York, N.Y) 2004, 303:1007-1010.
45. L.F. Agnati, D. Guidolin, F. Baluska, G. Leo, P.W. Barlow, C. Carone, S. Genedani, A new hypothesis of pathogenesis based on the divorce between mitochondria and their host cells: possible relevances for the Alzheimer's disease., Curr Alzheimer Res. 16 (2009) 307-322.
46. Koulintchenko M., Temperley R.J., Mason P.A., Dietrich A., Lightowlers R.N. Natural competence of mammalian mitochondria allows the molecular investigation of mitochondrial gene expression. Hum. Mol. Genet. 2006, 15:143-154.
47. Khrapko K., Vijg J. Mitochondrial DNA mutations and aging: devils in the details?. Trends Genet. 2009, 25:91-98.
48. Simpson R.J., Lim J.W., Moritz R.L., Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev. Proteomics 2009, 6:267-283.
49. Keller S., Sanderson M.P., Stoeck A., Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol. Lett. 2006, 107:102-108.