Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Waldenström, Anders ^a,b   Gennebäck, Nina ^a   Hellman, Urban ^a,b   Ronquist, Gunnar ^c  

^a UMEÅ UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY HOSPITAL   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 3; COMPLEMENTARY DNA; DNA; FLOTILLIN 1; RNA; CLATHRIN; FLOTILLINS; LIPOCORTIN 2; MEMBRANE PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSOL; DNA SEQUENCE; DNA TRANSFER; DOWN REGULATION; ELECTRON MICROSCOPY; EXOSOME; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HEART MUSCLE CELL; MEMBRANE VESICLE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; TARGET CELL; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION; UPREGULATION; ANIMAL; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; CELL STRAIN 3T3; METABOLISM; METHODOLOGY; SECRETORY VESICLE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ANNEXIN A2; BIOLOGICAL TRANSPORT; CAVEOLIN 3; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; CLATHRIN; CYTOSOL; DNA; EXOSOMES; FIBROBLASTS; MEMBRANE PROTEINS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MYOCYTES, CARDIAC; NIH 3T3 CELLS; RNA; RNA, MESSENGER; SECRETORY VESICLES;

EID: 84859608013     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034653     Document Type: Article

References (44)

1. Ronquist G, Brody I, Gottfries A, Stegmayr B, (1978) An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid-part II. Andrologia 10: 427-433.
2. Ronquist G, Brody I, Gottfries A, Stegmayr B, (1978) An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part I. Andrologia 10: 261-272.
3. Ronquist G, Hedstrom M, (1977) Restoration of detergent-inactivated adenosine triphosphatase activity of human prostatic fluid with concanavalin A. Biochim Biophys Acta 483: 483-486.
4. Ronquist G, Brody I, (1985) The prostasome: its secretion and function in man. Biochim Biophys Acta 822: 203-218.
5. Sahlen GE, Egevad L, Ahlander A, Norlen BJ, Ronquist G, et al. (2002) Ultrastructure of the secretion of prostasomes from benign and malignant epithelial cells in the prostate. Prostate 53: 192-199.
6. Arvidson G, Ronquist G, Wikander G, Ojteg AC, (1989) Human prostasome membranes exhibit very high cholesterol/phospholipid ratios yielding high molecular ordering. Biochim Biophys Acta 984: 167-173.
7. Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA, (2009) Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 69: 159-167.
8. Ronquist G, Nilsson O, (2001) Prostasomes, proceedings from a symposium held at the Wenner-Gren Centre, Stockholm, Sweden, Vol 81, 2001 Portland Press, London, U K.
9. Ronquist G, (2011) Prostasomes are mediators of intercellular communication: from basic research to clinical implications. J Intern Med.
10. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C, (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262: 9412-9420.
11. Pan BT, Teng K, Wu C, Adam M, Johnstone RM, (1985) Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 101: 942-948.
12. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, et al. (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183: 1161-1172.
13. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, et al. (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 4: 594-600.
14. Skokos D, Le Panse S, Villa I, Rousselle JC, Peronet R, et al. (2001) Mast cell-dependent B and T lymphocyte activation is mediated by the secretion of immunologically active exosomes. J Immunol 166: 868-876.
15. Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, et al. (2002) TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol 168: 3235-3241.
16. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ, (1999) Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94: 3791-3799.
17. van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, et al. (2001) Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 121: 337-349.
18. Fevrier B, Vilette D, Archer F, Loew D, Faigle W, et al. (2004) Cells release prions in association with exosomes. Proc Natl Acad Sci U S A 101: 9683-9688.
19. Faure J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, et al. (2006) Exosomes are released by cultured cortical neurones. Mol Cell Neurosci 31: 642-648.
20. Koga K, Matsumoto K, Akiyoshi T, Kubo M, Yamanaka N, et al. (2005) Purification, characterization and biological significance of tumor-derived exosomes. Anticancer Res 25: 3703-3707.
21. Llorente A, de Marco MC, Alonso MA, (2004) Caveolin-1 and MAL are located on prostasomes secreted by the prostate cancer PC-3 cell line. J Cell Sci 117: 5343-5351.
22. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, et al. (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7: 297-303.
23. Arienti G, Carlini E, Palmerini CA, (1997) Fusion of human sperm to prostasomes at acidic pH. J Membr Biol 155: 89-94.
24. Minelli A, Allegrucci C, Mezzasoma I, Ronquist G, Lluis C, et al. (1999) CD26 and adenosine deaminase interaction: its role in the fusion between horse membrane vesicles and spermatozoa. Biol Reprod 61: 802-808.
25. Ronquist G, Nilsson BO, Hjerten S, (1990) Interaction between prostasomes and spermatozoa from human semen. Arch Androl 24: 147-157.
26. Fabiani R, Johansson L, Lundkvist O, Ronquist G, (1994) Enhanced recruitment of motile spermatozoa by prostasome inclusion in swim-up medium. Hum Reprod 9: 1485-1489.
27. Kelly RW, Holland P, Skibinski G, Harrison C, McMillan L, et al. (1991) Extracellular organelles (prostasomes) are immunosuppressive components of human semen. Clin Exp Immunol 86: 550-556.
28. Rooney IA, Atkinson JP, Krul ES, Schonfeld G, Polakoski K, et al. (1993) Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J Exp Med 177: 1409-1420.
29. Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, et al. (2007) Exosomes with immune modulatory features are present in human breast milk. J Immunol 179: 1969-1978.
30. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659.
31. Ronquist KG, Ronquist G, Carlsson L, Larsson A, (2009) Human prostasomes contain chromosomal DNA. Prostate 69: 737-743.
32. Miranda KC, Bond DT, McKee M, Skog J, Paunescu TG, et al. (2010) Nucleic acids within urinary exosomes/microvesicles are potential biomarkers for renal disease. Kidney Int 78: 191-199.
33. Al-Nedawi K, Meehan B, Rak J, (2009) Microvesicles: messengers and mediators of tumor progression. Cell Cycle 8: 2014-2018.
34. Callahan KP, Butler JS, (2010) TRAMP complex enhances RNA degradation by the nuclear exosome component Rrp6. J Biol Chem 285: 3540-3547.
35. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH, (2009) Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 10: 42-46.
36. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, et al. (1998) HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 95: 2979-2984.
37. Goldoni D, Zhao Y, Green BD, McDermott BJ, Collins A, (2010) Inward rectifier potassium channels in the HL-1 cardiomyocyte-derived cell line. J Cell Physiol 225: 751-756.
38. Todaro GJ, Green H, (1963) Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 17: 299-313.
39. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society 57: 289-300.
40. Reiner A, Yekutieli D, Benjamini Y, (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368-375.
41. Ronquist GK, Larsson A, Ronquist G, Isaksson A, Hreinsson J, et al. (2011) Prostasomal DNA characterization and transfer into human sperm. Mol Reprod Dev 78: 467-476.
42. Gupta S, Knowlton AA, (2007) HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Heart Circ Physiol 292: H3052-3056.
43. Hayashi YK, Matsuda C, Ogawa M, Goto K, Tominaga K, et al. (2009) Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. J Clin Invest 119: 2623-2633.
44. Gazzerro E, Sotgia F, Bruno C, Lisanti MP, Minetti C, (2010) Caveolinopathies: from the biology of caveolin-3 to human diseases. Eur J Hum Genet 18: 137-145.