Українська Русский English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2019; 65(6): 105-125

CURRENT COMPREHENSION OF VESICULAR INTERCELLULAR SIGNALING

I.M. Prudnikov1, V.M. Tsyvkin1, A.M. Smirnov1, I.V. Pristash1, V.A. Chernyak2, V.M. Selyuk3, P.F. Muzichenko3

  1. O.O. Bogomolets Institute of Physiology, NAS of Ukraine, Kyiv, Ukraine
  2. Taras Shevchenko National University of Kyiv, Ukraine
  3. O.O. Bogomolets National Medical University, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz65.06.105

Abstract

Extracellular vesicles have a lot of different physiological functions: from regulation of gene expression to direct cytotoxic effects. There is a selective mechanism that combines the formation of new vesicles, their receptions, and the complex processing of the content. Vesicle recycling and reception is a versatile process that involves evolutionaryconservative factors. Vesicles and viruses use the same molecular mechanisms to enter and exit cells. The most unusual regulators of cellular physiology mediated by vesicles are many types of vesicular RNA and atypical lipid profile of their membranes. The physiological potential of extracellular vesicles is still unexplored, despite the abundance of new data. It can be assumed that current research brings us closer to understanding of integrative biological events that will allow us to correct physiological functions in various pathological conditions.

Keywords: exosomes, physiology of intercellular signaling

Full text: (PDF, in Ukrainian)

References

  1. Lee HS, Jeong J, Lee KJ. Characterization of vesicles secreted from insulinoma NIT-1 cells. J Proteome Res. 2009 Jun;8(6): 2851-62. CrossRef PubMed
    2.  
  2. Deatherage BL, Cookson BT. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun. 2012;80(6):1948-57. CrossRef PubMed PubMedCentral
    3.  
  3. Choi DS, Kim DK, Kim YK, Gho YS. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics. 2013 May;13 (10-11):1554-71. CrossRef PubMed
    4.  
  4. Sadoul R, Laporte MH, Chassefeyre R, Chi KI, Goldberg Y, Chatellard C, et al. The role of ESCRT during development and functioning of the nervous system. Semin Cell Dev Biol. 2018 Feb;74:40-9. CrossRef PubMed
    5.  
  5. György B, Szabó TG, Pásztói M, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011 Aug; 68(16): 2667-88. CrossRef PubMed PubMedCentral
    6.  
  6. Antonyak MA, Cerione RA. Microvesicles as mediators of intercellular communication in cancer. Methods Mol Biol. 2014;1165:147-73. CrossRef PubMed
    7.  
  7. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol. 2007 Apr 23; 177(2): 329-41. CrossRef PubMed PubMedCentral
    8.  
  8. Simons M, Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009 Aug; 21(4): 575-81. CrossRef PubMed
    9.  
  9. Choi DS, Lee J, Go G, Kim YK, Gho YS. Circulating extracellular vesicles in cancer diagnosis and monitoring: an appraisal of clinical potential. Mol Diagn Ther. 2013 Oct;17(5):265-71. CrossRef PubMed
    10.  
  10. Ratajczak J, Wysoczynski M, Hayek F, JanowskaWieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006 Sep;20(9):1487-95. CrossRef PubMed
    11.  
  11. Kim CW, Lee HM, Lee TH, Kang C, Kleinman HK, Gho YS. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res. 2002 Nov 1; 62(21):6312-7.
    12.  
  12. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, Rak J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008 May;10(5):619-24. CrossRef PubMed
    13.  
  13. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007 Jun;9(6):654-9. CrossRef PubMed
    14.  
  14. Bulgari D, Jha A, Deitcher DL, Levitan ES. Myopic (HD-PTP, PTPN23) selectively regulates synaptic neuropeptide release. Proc Natl Acad Sci USA. 2018 Feb 13;115(7):1617-22. CrossRef PubMed PubMedCentral
    15.  
  15. Christianson HC, Svensson KJ, Belting M. Exosome and microvesicle mediated phene transfer in mammalian cells. Seminars in cancer biology. 2014;28:31-8. CrossRef PubMed
    16.  
  16. van Dongen HM, Masoumi N, Witwer KW, Pegtel DM. Extracellular vesicles exploit viral entry routes for cargo delivery. Microbiology and molecular biology reviews: MMBR 2016;80(2):369-86. CrossRef PubMed PubMedCentral
    17.  
  17. Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M. Sorting it out: Regulation of exosome loading. Seminars in cancer biology 2014;28:3-13. CrossRef PubMed PubMedCentral
    18.  
  18. Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009;284(49):34211-22. CrossRef PubMed PubMedCentral
    19.  
  19. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012;119(3):756-66. CrossRef PubMed PubMedCentral
    20.  
  20. Aryani A, Denecke B. Exosomes as a nanodelivery system: a Key to the future of neuromedicine? Mol neurobiol. 2016;53(2):818-21. CrossRef PubMed PubMedCentral
    21.  
  21. Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracellular Vesicles. 2014;3. CrossRef PubMed PubMedCentral
    22.  
  22. Chivet M, Javalet C, Laulagnier K, Blot B, Hemming FJ, Sadoul R. Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons. J Extracellular Vesicles. 2014;3:24722. CrossRef PubMed PubMedCentral
    23.  
  23. Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood. 2005;106(5):1604-11. CrossRef PubMed
    24.  
  24. Alberts B, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell. Garland Science. 2007. CrossRef  
  25. Record M, Carayon K, Poirot M, Silvente-Poirot S. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochimica et Biophysica Acta (BBA) Mol and Cell Biol of Lipids. 2014;1841(1):108-20. CrossRef PubMed
    26.  
  26. Record M. Intercellular communication by exosomes in placenta: A possible role in cell fusion? Placenta. 2014;35(5):297-302. CrossRef PubMed
    27.  
  27. Nakase I, Kobayashi NB, Takatani-Nakase T, Yoshida T. Active macropinocytosis induction by stimulation of epidermal growth factor receptor and oncogenic Ras expression potentiates cellular uptake efficacy of exosomes.  Sci Reports. 2015;5:10300. CrossRef PubMed PubMedCentral
    28.  
  28. Tian T, Zhu YL, Zhou YY, Liang GF, Wang YY, Hu FH, et al. Exosome uptake through clathrinmediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem. 2014;289(32):22258-67. CrossRef PubMed PubMedCentral
    29.  
  29. Fitzner D, Schnaars M, van Rossum D, Krishnamoorthy G, Dibaj P, Bakhti M, et al. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J Cell Sci. 2011;124(Pt 3):447-58. CrossRef PubMed
    30.  
  30. Feng D, Zhao WL, Ye YY, Bai XC, Liu RQ, Chang LF, et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic (Copenhagen, Denmark). 2010;11(5):675-87. CrossRef PubMed
    31.  
  31. Barres C, Blanc L, Bette-Bobillo P, Andre S, Mamoun R, Gabius HJ, et al. Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood. 2010;115(3):696-705. CrossRef PubMed
    32.  
  32. Nanbo A, Kawanishi E, Yoshida R, Yoshiyama H. Exosomes derived from Epstein-Barr virusinfected cells are internalized via caveola-dependent endocytosis and promote phenotypic modulation in target cells. J Virol. 2013;87(18):10334-47. CrossRef PubMed PubMedCentral
    33.  
  33. Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM, et al. Exosome uptake depends on ERK1. 2-heat shock protein 27 signaling and lipid Raft-mediated endocytosis negatively regulated by caveolin-1. J Biol Chem. 2013;288(24):17713-24. CrossRef PubMed PubMedCentral
    34.  
  34. Plebanek MP, Mutharasan RK, Volpert O, Matov A, Gatlin JC, Thaxton CS. Nanoparticle targeting and cholesterol flux through scavenger receptor type B-1 inhibits cellular exosome uptake. Sci Reports. 2015;5:15724. CrossRef PubMed PubMedCentral
    35.  
  35. Hazan-Halevy I, Rosenblum D, Weinstein S, Bairey O, Raanani P, Peer D. Cell-specific uptake of mantle cell lymphoma-derived exosomes by malignant and non-malignant B-lymphocytes. Cancer Lett. 2015;364(1):59-69. CrossRef PubMed PubMedCentral
    36.  
  36. Lim JP, Gleeson PA. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol. 2011;89(8):836-43. CrossRef PubMed
    37.  
  37. Costa Verdera H, Gitz-Francois JJ, Schiffelers RM, Vader P. Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. J Controlled Release. 2017;266:100-8. CrossRef PubMed
    38.  
  38. Nakase I, Noguchi K, Fujii I, Futaki S. Vectorization of biomacromolecules into cells using extracellular vesicles with enhanced internalization induced by macropinocytosis. Sci Reports. 2016;6:34937. CrossRef PubMed PubMedCentral
    39.  
  39. Gordon S. Phagocytosis: An Immunobiologic Process. Immunity. 2016;44(3):463-75. CrossRef PubMed
    40.  
  40. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature. 2003;422(6927):37-44. CrossRef PubMed
    41.  
  41. Fruhbeis C, Frohlich D, Kuo WP, Amphornrat J, Thilemann S, Saab AS, et al. Neurotransmitter triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 2013;11(7): e1001604. CrossRef PubMed PubMedCentral
    42.  
  42. Lanzetti L, Di Fiore PP. Endocytosis and cancer: an 'insider' network with dangerous liaisons. Traffic (Copenhagen, Denmark). 2008;9(12): 2011-21. CrossRef PubMed
    43.  
  43. El-Sayed A, Harashima H. Endocytosis of gene delivery vectors: from clathrin-dependent to lipid raft-mediated endocytosis. Mol Ther. 2013;21(6):1118-30. CrossRef PubMed PubMedCentral
    44.  
  44. Escrevente C, Keller S, Altevogt P, Costa J. Interaction and uptake of exosomes by ovarian cancer cells. BMC cancer. 2011;11:108. CrossRef PubMed PubMedCentral
    45.  
  45. Koumangoye RB, Sakwe AM, Goodwin JS, Patel T, Ochieng J. Detachment of breast tumor cells induces rapid secretion of exosomes which subsequently mediate cellular adhesion and spreading. PloS One. 2011;6(9):e24234. CrossRef PubMed PubMedCentral
    46.  
  46. Zech D, Rana S, Buchler MW, Zoller M. Tumor-exosomes and leukocyte activation: an ambivalent crosstalk. Cell Comm Signal. 2012;10(1):37. CrossRef PubMed PubMedCentral
    47.  
  47. Calzolari A, Raggi C, Deaglio S, Sposi NM, Stafsnes M, Fecchi K, et al. TfR2 localizes in lipid raft domains and is released in exosomes to activate signal transduction along the MAPK pathway. J Cell Sci. 2006; 119(Pt 21):4486-98. CrossRef PubMed
    48.  
  48. Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood. 1989;74(5):1844-51. CrossRef PubMed
    49.  
  49. Goldstein JL, Brown MS. The LDL receptor. Arterioscler Thromb Vasc Biol. 2009;29(4):431-8. CrossRef PubMed PubMedCentral
    50.  
  50. Rajendran L, Simons K. Lipid rafts and membrane dynamics. J Cell Sci. 2005;118(Pt 6):1099-102. CrossRef PubMed
    51.  
  51. Cureton DK, Harbison CE, Cocucci E, Parrish CR, Kirchhausen T. Limited transferrin receptor clustering allows rapid diffusion of canine parvovirus into clathrin endocytic structures. J Virol. 2012;86(9):5330-40. CrossRef PubMed PubMedCentral
    52.  
  52. Moller-Tank S, Maury W. Phosphatidylserine receptors: enhancers of enveloped virus entry and infection. Virology. 2014;468-70:565-80. CrossRef PubMed PubMedCentral
    53.  
  53. Jeong HS, Na KS, Hwang H, Oh PS, Kim DH, Lim ST, et al. Effect of space length of mannose ligand on uptake of mannosylated liposome in RAW 264.7 cells: In vitro and in vivo studies. J Biomed Materials Res Part A. 2014;102(12):4545-53. CrossRef PubMed
    54.  
  54. Kawauchi Y, Kuroda Y, Kojima N. Preferences for uptake of carbohydrate-coated liposomes by C-type lectin receptors as antigen-uptake receptors. Glycoconjugate J. 2012;29(7):481-90. CrossRef PubMed
    55.  
  55. Watson DC, Bayik D, Srivatsan A, Bergamaschi C, Valentin A, Niu G, et al. Efficient production and enhanced tumor delivery of engineered extracellular vesicles. Biomaterials. 2016;105:195-205. CrossRef PubMed
    56.  
  56. Ritz S, Schottler S, Kotman N, Baier G, Musyanovych A, Kuharev J, et al. Protein corona of nanoparticles: distinct proteins regulate the cellular uptake. Biomacromolecules. 2015;16(4):1311-21. CrossRef PubMed
    57.  
  57. Gonda A, Kabagwira J, Senthil GN, Wall NR. Internalization of exosomes through receptor-mediated endocytosis. Mol Cancer Res. 2019 Feb;17(2):337-47. CrossRef PubMed
    58.  
  58. Carlton J1, Bujny M, Peter BJ, Oorschot VM, Rutherford A, Mellor H, Klumperman J, McMahon HT, Cullen PJ. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr Biol. 2004 Oct  26;14(20):1791-800. CrossRef PubMed
    59.  
  59. van Weering JR, Sessions RB, Traer CJ, et al. Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J. 2012 Nov 28;31(23):4466-80. CrossRef PubMed PubMedCentral
    60.  
  60. Burd C1, Cullen PJ. Retromer: a master conductor of endosome sorting. Cold Spring Harb Perspect Biol. 2014 Feb 1; 6(2). CrossRef PubMed PubMedCentral
    61.  
  61. McGough IJ, Cullen PJ. Recent advances in retromer biology. 2011. Traffic. 12(8):963-71. CrossRef PubMed
    62.  
  62. Zhang Y, Grant B, Hirsh D. RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol Biol Cell. 2001;12(7): 2011-21. CrossRef PubMed PubMedCentral
    63.  
  63. Walsh P, Bursa D, Law YC, Cyr D, Lithgow T. The J-protein family: Modulating protein assembly, disassembly and translocation. EMBO Rep. 2004;5(6):567-71. CrossRef PubMed PubMedCentral
    64.  
  64. Ungewickell E, Ungewickell H, Holstein SE, Lindner R, Prasad K, Barouch W, et al. Role of auxilin in uncoating clathrin-coated vesicles. Nature. 1995 Dec 7;378(6557):632-5. CrossRef PubMed
    65.  
  65. Greener T, Grant B, Zhang Y, Wu X, Greene LE, Hirsh D, Eisenberg E. Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat Cell Biol. 2001 Feb;3(2):215-9. CrossRef PubMed
    66.  
  66. Shi A, Sun L, Banerjee R, Tobin M, Zhang Y, Grant BD. Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. EMBO J. 2009 Nov 4;28(21):3290-302. CrossRef PubMed PubMedCentral
    67.  
  67. Popoff V, Mardones GA, Bai SK, Chambon V, Tenza D, Burgos PV, et al. Analysis of articulation between clathrin and retromer in retrograde sorting on early endosomes. Traffic. 2009 Dec;10(12):1868-80. CrossRef PubMed
    68.  
  68. Xhabija B, Vacratsis PO. Receptor-mediated endocytosis 8 utilizes an N-terminal phosphoinositide-binding motif to regulate endosomal clathrin dynamics. J Biol Chem. 2015;290(35):21676-89. CrossRef PubMed PubMedCentral
    69.  
  69. Fujibayashi A1, Taguchi T, Misaki R, Ohtani M, Dohmae N, Takio K, et al. Human RME-8 is involved in membrane trafficking through early endosomes. Cell Struct Funct. 2008;33(1):35-50. CrossRef PubMed
    70.  
  70. Freeman CL, Hesketh G, Seaman MN. RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J Cell Sci. 2014, 127(pt 9):2053-70. CrossRef PubMed PubMedCentral
    71.  
  71. Hurley JH. The ESCRT complexes. Crit Rev Biochem Mol Biol. 2010;45(6):463-87. CrossRef PubMed PubMedCentral
    72.  
  72. Babst M. MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr Opin Cell Biol. 2011 Aug; 23(4):452-7. CrossRef PubMed PubMedCentral
    73.  
  73. Henne WM, Buchkovich NJ, Emr SD. The ESCRT pathway. Dev Cell. 2011;21(1):77-91. CrossRef PubMed
    74.  
  74. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature. 2002 Mar 28;416(6879):451-5. CrossRef PubMed
    75.  
  75. Bishop N, Horman A, Woodman P. Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol. 2002; 157(1):91-101. CrossRef PubMed PubMedCentral
    76.  
  76. Hofmann K, Falquet L. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem Sci. 2001;26(6):347-50. CrossRef  
  77. Raiborg C, Stenmark H. Hrs and endocytic sorting of ubiquitinated membrane proteins. Cell Struct Funct. 2002;27(6):403-8. CrossRef PubMed
    78.  
  78. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol. 2002 May;4(5):394-8. CrossRef PubMed
    79.  
  79. Raiborg C, Bremnes B, Mehlum A, Gillooly DJ, D'Arrigo A, Stang E, Stenmark H. FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J Cell Sci. 2001 Jun;114(Pt 12):2255-63.
    80.  
  80. Sönnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol. 2000; 149(4):901-14. CrossRef PubMed PubMedCentral
    81.  
  81. Sachse M, Urbé S, Oorschot V, Strous GJ, Klumperman J. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell. 2002;13(4):1313-28. CrossRef PubMed PubMedCentral
    82.  
  82. Norris A, Tammineni P, Wang S, Gerdes J, Murr A, Kwan KY3, Cai Q, Grant BD. SNX-1 and RME-8 oppose the assembly of HGRS-1. ESCRT-0 degradative microdomains on endosomes. Proc Natl Acad Sci USA. 2017 Jan 17;114(3):E307-E316. CrossRef PubMed PubMedCentral
    83.  
  83. Teis D, Saksena S, Emr SD. Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev Cell. 2008,15(4):578-89. CrossRef PubMed
    84.  
  84. Sadoul R. Do Alix and ALG-2 really control endosomes for better or for worse? Biol Cell. 2006 Jan; 98(1):69-77. CrossRef PubMed
    85.  
  85. Bissig C, Gruenberg J. ALIX and the multivesicular endosome: ALIX in Wonderland, Trends Cell Biol. 2014;24(1):19-25. CrossRef PubMed
    86.  
  86. Doyotte A, Mironov A, McKenzie E, Woodman P. The Bro1-related protein HDPTP. PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis, Proc Natl Acad Sci USA. 2008; 105(17):6308-13. CrossRef PubMed PubMedCentral
    87.  
  87. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, et al. Tsg101 and thevacuolar protein sorting pathway are essential for HIV-1 budding. Cell. 2001;107(1):55-65. CrossRef  
  88. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG. AIP1. ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding, Cell. 2003;114(6):689-99. CrossRef  
  89. Martin-Serrano J, Yarovoy A, Perez-Caballero D, Bieniasz PD, Divergent retroviral latebudding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci USA. 2003;100(21):12414-9. CrossRef PubMed PubMedCentral
    90.  
  90. Segura-Morales C, Pescia C, Chatellard-Causse C, Sadoul R, Bertrand E, Basyuk E. Tsg101 and Alix interact with murine leukemia virus Gag and cooperate with Nedd4 ubiquitin ligases during budding. J Biol Chem. 2005; 280(29):27004-12. CrossRef PubMed
    91.  
  91. Morita E, Sandrin V, McCullough J, Katsuyama A, Baci Hamilton I, Sundquist WI. ESCRTIII Protein Requirements for HIV-1 Budding, Cell Host Microbe. 2011;9(3):235-42. CrossRef PubMed PubMedCentral
    92.  
  92. Sandrin V, Sundquist WI. ESCRT requirements for EIAV budding, Retrovirology. 2013;10, 104. CrossRef PubMed PubMedCentral
    93.  
  93. Bartusch C, Prange R. ESCRT Requirements for Murine Leukemia Virus Release. Viruses. 2016;8(4):103. CrossRef PubMed PubMedCentral
    94.  
  94. Carlton JG, Martin-Serrano J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science. 2007; 316(5833):1908-12. CrossRef PubMed
    95.  
  95. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, Rodesch CK, et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. Embo J. 2007;26(19):4215-27. CrossRef PubMed PubMedCentral
    96.  
  96. Guizetti J, Schermelleh L, Mäntler J, Maar S, Poser I, Leonhardt H, et al. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science. 2011 Mar 25;331(6024):1616-20. CrossRef PubMed
    97.  
  97. Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, Perez F. ESCRT machinery is required for plasma membrane repair. Science. 2014 Feb 28;343(6174):1247-136. CrossRef PubMed
    98.  
  98. Scheffer LL, Sreetama SC, Sharma N, Medikayala S, Brown KJ, Defour A, Jaiswal JK. Mechanism of Ca²⁺- triggered ESCRT assembly and regulation of cell membrane repair. Nat Commun. 2014 Dec;23(5):5646. CrossRef PubMed PubMedCentral
    99.  
  99. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci USA. 2012 Mar 13;109(11):4146-51. CrossRef PubMed PubMedCentral
    100.  
  100. Matusek T, Wendler F, Polès S, Pizette S, D'Angelo G, Fürthauer M, Thérond PP. The ESCRT machinery regulates the secretion and long-range activity of Hedgehog. Nature. 2014 Dec 4; 516(7529):99-103. CrossRef PubMed
    101.  
  101. Webster BM, Colombi P, Jäger J, Lusk CP. Surveillance of nuclear pore complex assembly by ESCRT-III. Vps4. Cell. 2014 Oct 9;159(2):388-401. CrossRef PubMed PubMedCentral
    102.  
  102. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG. ESCRT-III controls nuclear envelope reformation. Nature. 2015 Jun 11;522(7555):236-9. CrossRef PubMed PubMedCentral
    103.  
  103. Vietri M, Schink KO, Campsteijn C, Wegner CS, Schultz SW, Christ L, et al. Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature. 2015 Jun 11;522(7555):231-5. CrossRef PubMed
    104.  
  104. Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M, Weigelin B, et al. Nuclear envelope rupture and repair during cancer cell migration. Science. 2016 Apr 15;352(6283):353-8. CrossRef PubMed PubMedCentral
    105.  
  105. Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, et al. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science. 2016 Apr 15;352(6283):359-62. CrossRef PubMed
    106.  
  106. Sadoul R, Laporte MH, Chassefeyre R, Chi KI, Goldberg Y, Chatellard C, et al. The role of ESCRT during development and functioning of the nervous system. Semin Cell Dev Biol. 2018 Feb; 74:40-9. CrossRef PubMed
    107.  
  107. Hanyaloglu, AC, and von Zastrow M. A novel sorting sequence in the beta2-adrenergic receptor switches recycling from default to the Hrs-dependent mechanism. J Biol Chem. 2007, 282:3095-104. CrossRef PubMed
    108.  
  108. Huang SH, Zhao L, Sun ZP, Li XZ, Geng Z, Zhang KD, et al. Essential role of Hrs in endocytic recycling of fulllength TrkB receptor but not its isoform TrkB.T1. J Biol Chem. 2009, 284:15126-36. CrossRef PubMed PubMedCentral
    109.  
  109. MacDonald, Brown E, Selvais L, Liu A , Waring H, Newman T, et al. HRS-WASH axis governs actin-mediated endosomal recycling and cell invasion. J Cell Biol. 2018 Jul 2; 217(7):2549-64. CrossRef PubMed PubMedCentral
    110.  
  110. Zech, T, Calaminus SD, Caswell P, Spence HJ, Carnell M, Insall RH, et al. The Arp2. 3 activator WASH regulates α5β1-integrin-mediated invasive migration. J Cell Sci. 2011;124:3753-59. CrossRef PubMed PubMedCentral
    111.  
  111. Dozynkiewicz MA, Jamieson NB, Macpherson I, Grindlay J, van den Berghe PV, von Thun A, et al. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes. lysosomes and drive cancer progression. Dev Cell. 2012;22:131-45. CrossRef PubMed PubMedCentral
    112.  
  112. Macpherson IR, Rainero E, Mitchell LE, van den Berghe PV, Speirs C, Dozynkiewicz MA, et al. CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer. J Cell Sci. 2014;127:3893-901. CrossRef PubMed
    113.  
  113. Harbour ME, Breusegem SY, Antrobus R. Freeman C, Reid E, Seaman MN. The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J Cell Sci. 2010;123:3703-17. CrossRef PubMed PubMedCentral
    114.  
  114. Harbour ME, Breusegem SY, and Seaman MN. Recruitment of the endosomal WASH complex is mediated by the extended 'tail' of Fam21 binding to the retromer protein Vps35. Biochem J. 2012;442:209-20. CrossRef PubMed
    115.  
  115. Jia D, Gomez TS, Billadeau DD, and Rosen MK. Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer. Mol Biol Cell. 2012;23:2352-61. CrossRef PubMed PubMedCentral
    116.  
  116. Pons V, Luyet PP, Morel E, Abrami L, van der Goot FG, Parton RG, and Gruenberg J. Hrs and SNX3 functions in sorting and membrane invagination within multivesicular bodies. PLoS Biol. 2008;6:e214. CrossRef PubMed PubMedCentral
    117.  
  117. Urbé S, Mills IG, Stenmark H, Kitamura N, and Clague MJ. Endosomal localization and receptor dynamics determine tyrosine phosphorylation of hepatocyte growth factor-regulated tyrosine kinase substrate. Mol Cell Biol. 2000;20:7685-92. CrossRef PubMed PubMedCentral
    118.  
  118. Mao Y, Nickitenko A, Duan X, Lloyd TE, Wu MN, Bellen H, and Quiocho FA. Crystal structure of the VHS and FYVE tandem domains of Hrs, a protein involved  in membrane trafficking and signal transduction. Cell. 2000;100:447-56. CrossRef  
  119. Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, and Bonifacino JS. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science. 2001,292:1712-16. CrossRef PubMed
    120.  
  120. Misra S, Puertollano R, Kato Y, Bonifacino JS, and Hurley JH. Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature. 2002;415:933-37. CrossRef PubMed
    121.  
  121. Ren X, and Hurley JH. VHS domains of ESC RT-0 cooperate in high-avidity binding to polyubiquitinated cargo. EMBO J. 2010;29:1045-54. CrossRef PubMed PubMedCentral
    122.  
  122. Calderwood DA, Shattil SJ, and Ginsberg MH. Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J Biol Chem. 2000;275:22607-10. CrossRef PubMed
    123.  
  123. Jiang G, Giannone G, Critchley D, Fukumoto R, and Sheetz MP. Two-piconewton slip bond between fibronectin and the E. Cytoskeleton depends on talin. Nature. 2003;424:334-7. CrossRef PubMed
    124.  
  124. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K et al. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell. 2010;143:761-73. CrossRef PubMed PubMedCentral
    125.  
  125. Zech T, Calaminus SD, and Machesky LM. Actin on trafficking: could actin guide directed receptor transport? Cell Adhes. Migr. 2012;6:476-81. CrossRef PubMed PubMedCentral
    126.  
  126. Huang F, Kirkpatrick D, Jiang X, Gygi S, and Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell. 2006;21:737-48. CrossRef PubMed
    127.  
  127. Row PE, Clague MJ, and Urbé S. Growth factors induce differential phosphorylation profiles of the Hrs-STAM complex: a common node in signalling networks with signal-specific properties. Biochem J. 2005;389:629-636. CrossRef PubMed PubMedCentral
    128.  
  128. Ratajczak J, Miekus K, Kucia, M, Zhang J, Reca R, Dvorak P, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006; 20:847-856. CrossRef PubMed
    129.  
  129. Skog, J, Wurdinger T, van Rijin S, Meijer DH, Gainche L, Curry WT, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumor growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470-6. CrossRef PubMed PubMedCentral
    130.  
  130. Tsatsaronis JA, Franch-Arroyo S, Resch U, Charpentier E. Extracellular vesicle RNA: A universal mediator of microbial communication? Trends Microbiol. 201;26:401-10. CrossRef PubMed
    131.  
  131. Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol. 2016;36:301-12. CrossRef PubMed PubMedCentral
    132.  
  132. Nolte-'t Hoen EN, Buermans HP, Waasdorp M, Stoorvogel W, Wauben MH, Hoen PA. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res. 2012;40:9272-85. CrossRef PubMed PubMedCentral
    133.  
  133. Batagov AO, Kurochkin IV. Exosomes secreted by human cells transport largely mRNA fragments that are enriched in the 3'-untranslated regions. Biol Direct. 2013;8:12. CrossRef PubMed PubMedCentral
    134.  
  134. Lefebvre FA, Benoit Bouvrette LP, Perras L, BlanchetCohen A, Garnier D, Rak J, et al. Comparative transcriptomic analysis of human and Drosophila extracellular vesicles. Sci Rep. 2016;6:27680. CrossRef PubMed PubMedCentral
    135.  
  135. Wei Z, Batagov AO, Schinelli S, Wang J, Wang Y, El Fatimy R, et al. Coding and noncoding landscape of extracellular RNA released by human glioma stem cells. Nat Commun. 2017;8:1145. CrossRef PubMed PubMedCentral
    136.  
  136. Bolukbasi MF, Mizrak A, Ozdener GB, Madlener S, Strobel T, Erkan EP, et al. miR-1289 and "zipcode"-like sequence enrich mRNA in microvesicles. J Extracell. Vesicles. 2012;1:2. CrossRef PubMed PubMedCentral
    137.  
  137. Cha DJ, Franklin JL, Dou Y, Liu Q, Higginbotham JN, Demory Beckler, et al. KRAS-dependent sorting of miRNA to exosomes. eLife. 2015,4:e07197. CrossRef PubMed PubMedCentral
    138.  
  138. Melo SA, Sugimoto H, O'Connell JT, Kato N, Villanueva A, Vidal A, et al. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell. 2014;26:707-21. CrossRef PubMed PubMedCentral
    139.  
  139. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009;11:1143-9. CrossRef PubMed
    140.  
  140. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980. CrossRef PubMed PubMedCentral
    141.  
  141. Shurtleff MJ, Temoche-Diaz MM, Karfilis KV, Ri S, Schekman R. Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction. eLife. 2016;5. CrossRef PubMed PubMedCentral
    142.  
  142. Faury D, Nantel A, Dunn SE, Guiot MC, Haque T, Hauser P, et al. Molecular profiling identifies prognostic subgroups of pediatric glioblastoma and shows increased YB-1 expression in tumors. J Clin Oncol. 2007;25:1196-208. CrossRef PubMed
    143.  
  143. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E, Jacob K, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 2012;482:226-31. CrossRef PubMed
    144.  
  144. Santangelo L, Giurato G, Cicchini C, Montaldo C, Mancone C, Tarallo R, et al. The RNA-binding protein SYNCRIP is a component of the hepatocyte exosomal machinery controlling microRNA sorting. Cell Rep. 2016;17:799-808. CrossRef PubMed
    145.  
  145. Koppers-Lalic D, Hackenberg M, Bijnsdorp IV, van Eijndhoven MAJ, Sadek P, Sie D, et al. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014; 8:1649-58. CrossRef PubMed
    146.  
  146. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285:17442-52. CrossRef PubMed PubMedCentral
    147.  
  147. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science (New York NY). 2008;319:1244-7. CrossRef PubMed
    148.  
  148. Chevillet JR, Kang Q, Ruf IK, Briggs HA, Vojtech LN, Hughes SM, et al. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA. 2014;111:14888-93. CrossRef PubMed PubMedCentral
    149.  
  149. Qin Y, Yao J, Wu DC, Nottingham RM, Mohr S, HunickeSmith S, Lambowitz AM. High-throughput sequencing of human plasma RNA by using thermostable group II intron reverse transcriptases. RNA. 2016 Jan;22(1):111-28. CrossRef PubMed PubMedCentral
    150.  
  150. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 2011 Mar 22;108(12):5003-8. CrossRef PubMed PubMedCentral
    151.  
  151. Cha DJ, Franklin JL, Dou Y, Liu Q, Higginbotham JN, Demory Beckler M, et al. KRAS-dependent sorting of miRNA to exosomes. Elife. 2015 Jul,1;4:e07197. CrossRef PubMed PubMedCentral
    152.  
  152. Shurtleff MJ, Temoche-Diaz MM, Karfilis KV, Ri S, Schekman R. Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction. Elife. 2016 Aug 25;5. pii: e19276. CrossRef PubMed PubMedCentral
    153.  
  153. Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, Pérez-Hernández D, Vázquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980. CrossRef PubMed PubMedCentral
    154.  
  154. Santangelo L, Giurato G, Cicchini C, Montaldo C, Mancone C, Tarallo R, et al. The RNA-binding protein SYNCRIP is a component of the Hepatocyte exosomal machinery controlling microRNA sorting. Cell Rep. 2016 Oct 11; 17(3):799-808. CrossRef PubMed
    155.  
  155. Mukherjee K, Ghoshal B, Ghosh S, Chakrabarty Y, Shwetha S, Das S, et al. Reversible HuR-microRNA binding controls extracellular export of miR-122 and augments stress response. EMBO Rep. 2016 Aug;17(8):1184-203. CrossRef PubMed PubMedCentral
    156.  
  156. Shurtleff MJ, Yao J, Qin Y, Nottingham RM, TemocheDiaz MM, Schekman R, et al. Broad role for YBX1 in defining the small noncoding RNA composition of exosomes. Proc Natl Acad Sci USA. 2017 Oct 24;114(43):E8987-E995. CrossRef PubMed PubMedCentral
    157.  
  157. Janas T, Janas MM, Sapoń K, Janas T. Mechanisms of RNA loading into exosomes. FEBS Lett. 2015 Jun 4;589(13):1391-8. CrossRef PubMed
    158.  
  158. Wu BX, Clarke CJ, Matmati N, Montefusco D, Bartke N, and Hannun YA. Identification of novel anionic phospholipid binding domains in neutral sphingomyelinase 2 with selective binding preference. J Biol Chem. 2011;286,22362-71. CrossRef PubMed PubMedCentral
    159.  
  159. Rappa G, Mercapide J, Fabio Anzanello, Pope F, Lorico A. Biochemical and biological characterization of exosomes containing prominin-1. CD133. Mol Cancer 2013;12:62. CrossRef PubMed PubMedCentral
    160.  
  160. Record M, Carayon K, Poirot M, and Silvente-Poirot S. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochim Biophys Acta. 2014;1841,108-20. CrossRef PubMed
    161.  
  161. Kajimoto T, Okada T, Miya S, Lifang Zhang L, and Nakamura S. Ongoing activation of sphingosine 1-phosphate receptors mediates maturation of exosomal multivesicular endosomes. Nat Commun. 2013;4,2712. CrossRef PubMed
    162.  
  162. Gulbins E and Kolesnick R. Raft ceramide in molecular medicine. Oncogene. 2003;22,7070-77. CrossRef PubMed
    163.  
  163. Chiantia S, Kahya N, Ries J and Schwille P. Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys J. 2006;90,4500-8. CrossRef PubMed PubMedCentral
    164.  
  164. Johnston I and Johnston LJ. Ceramide promotes restructuring of model raft membranes. Langmuir. 2006;22,11284-9. CrossRef PubMed
    165.  
  165. Nurminen TA, Holopainen JM, Zhao H and Kinnunen PKJ. Observation of topical catalysis by sphingomyelinase coupled to microspheres. J Am Chem Soc. 2002;124,12129-34. CrossRef PubMed
    166.  
  166. Vyas P, Balakier H, Librach CL. Ultrastructural identification of CD9 positive extracellular vesicles released from human embryos and transported through the zona pellucida. Syst Biol Reprod Med. 2019 Aug;65(4):273-80. CrossRef PubMed
    167.  
  167. Hayashi T, Hoffman MP. Exosomal microRNA communication between tissues during organogenesis. RNA Biol. 2017 Dec 2;14(12):1683-9. CrossRef PubMed PubMedCentral
    168.  
  168. Giacomini E, Alleva E, Fornelli G, Quartucci A, Privitera L, Vanni VS, et al. Embryonic extracellular vesicles as informers to the immune cells at the maternal-fetal interface. Clin Exp Immunol. 2019 Apr 22. CrossRef PubMed
    169.  
  169. Choi D, Lee TH, Spinelli C, Chennakrishnaiah S, D'Asti E, Rak J. Extracellular vesicle communication pathways as regulatory targets of oncogenic transformation. Semin Cell Dev Biol. 2017 Jul;67:11-22. CrossRef PubMed
    170.  
  170. Hong SB, Yang H, Manaenko A, Lu J, Mei Q, Hu Q. Potential of Exosomes for the Treatment of Stroke. Cell Transplant. 2018 Dec 6:963-8. CrossRef PubMed PubMedCentral
    171.  
  171. Zhu L, Kalimuthu S, Gangadaran P, Oh JM, Lee HW, Baek SH, et al. Exosomes derived from natural killer cells exert therapeutic effect in melanoma. Theranostics. 2017 Jul 7;7(10):2732-45. CrossRef PubMed PubMedCentral
    172.  

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2021.