Українська 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. 2020; 66(5): 73-84


EXTRACELLULAR PROTEASOMES

I. Prudnikov1, V. Tsyvkin1, A. Smirnov1, I. Pristash1, M. Syrko2

  1. Bogomoletz Institute of Physiology of NAS of Ukraine, Kyiv, Ukraine
  2. Taras Shevchenko National University of Kyiv, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz66.05.073


Abstract

Little-known to a wide range of specialists details of the functioning of one of the main participants in cellular metabolism – a complex of neutral proteases with their regulators, which is called “proteasome” – are observed in this paper. The review analyzes the works of recent years devoted to the study of the participation of proteasomes in intercellular signaling and catabolism of regulatory and signaling proteins in the extracellular space.

Keywords: exosome; protease; proteasome; signalization.

References

  1. Maupin-Furlow JA, Humbard MA, Kirkland PA, Li W, Reuter CJ, Wright AJ, Zhou G. Proteasomes from structure to function: perspectives from Archaea. Curr Top Dev Biol. 2006; 75:125-69. CrossRef
  2. Naujokat C, Fuchs D, Berges C. Adaptive modification and flexibility of the proteasome system in response to proteasome inhibition. Biochim Biophys Acta. 2007 Sep;1773(9):1389-97. CrossRef PubMed
  3. Konstantinova IM, Tsimokha AS, Mittenberg AG. Role of proteasomes in cellular regulation. Int Rev Cell Mol Biol. 2008; 267:59-124. CrossRef
  4. Mueller O, Anlasik T, Wiedemann J, Thomassen J, Wohlschlaeger J, Hagel V, Keyvani K, Schwieger I, et al. Circulating extracellular proteasome in the cerebrospinal fluid: a study on concentration and proteolytic activity. J Mol Neurosci. 2012;46:509-15. CrossRef PubMed
  5. Sixt SU, Beiderlinden M, Jennissen HP, Peters J. Extracellular proteasome in the human alveolar space: a new housekeeping enzyme? Am J Physiol-Lung Cell Mol Physiol. 2007;292:L1280-8. CrossRef PubMed
  6. Jakob C, Egerer K, Liebisch P, Türkmen S, Zavrski I, Kuckelkorn U, Heider U, Kaiser M, Fleissner C, Sterz J, et al. Circulating proteasome levels are an independent prognostic factor for survival in multiple myeloma. Blood. 2007;109:2100-5. CrossRef PubMed
  7. Ben-Nissan G and Sharon M. Regulating the 20S proteasome ubiquitin-independent degradation pathway. Biomolecules. 2014;4:862-4. CrossRef PubMed PubMedCentral
  8. Groll M, Ditzel L, Löwe J, Stock D, Bochtler M, Bartunik HD, Huber R. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature. 1997;386:463-71. CrossRef PubMed
  9. Maupin-Furlow J. Proteasomes and protein conjugation across domains of life. Nat Rev Microbiol. 2011;10:100-1. CrossRef PubMed PubMedCentral
  10. Budenholzer L, Cheng CL, Li Y, Hochstrasser M. Proteasome structure and assembly. J Mol Biol. 2017;429:3500-4. CrossRef PubMed PubMedCentral
  11. Kisselev AF, Garcia-Calvo M, Overkleeft HS, Peterson E, Pennington MW, Ploegh HL, Thornberry NA, Goldberg AL. the caspase-like sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J Biol Chem. 2003; 278: 35869-77. CrossRef PubMed
  12. Inobe T, Matouschek A. Paradigms of protein degradation by the proteasome. Curr Opin Struct Biol. 2014;24:156-64. CrossRef PubMed PubMedCentral
  13. Qian M-X, Pang Y, Liu CH, Haratake K, Du B-Y, Ji D-Y, et al. Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis. Cell 2013;153:1012-4. CrossRef PubMed PubMedCentral
  14. Kloetzel P-M. Ubiquitin and proteasomes: Antigen processing by the proteasome. Nat Rev Mol Cell Biol. 2001;2:179-87. CrossRef PubMed
  15. Ravid T, Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol. 2008;9:679-690. CrossRef PubMed PubMedCentral
  16. Daulny A, Tansey WP. Damage control: DNA repair, transcription, and the ubiquitin-proteasome system. DNA Repair 2009;8:444-8. CrossRef PubMed
  17. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol Rev. 2002;82:373-428. CrossRef PubMed
  18. Enam C, Geffen Y, Ravid T, Gardner RG. Protein quality control degradation in the nucleus. Annu Rev Biochem. 2018;87:725-49. CrossRef PubMed
  19. Koch B, Yu HG. Regulation of inner nuclear membrane associated protein degradation. Nucleus. 2019;10:169-80. CrossRef PubMed PubMedCentral
  20. von Mikecz A, Chen M, Rockel T, Scharf A. The nuclear ubiquitin-proteasome system: visualization of proteasomes, protein aggregates, and proteolysis in the cell nucleus. Methods Mol Biol. 2008;463:191-202. CrossRef PubMed
  21. Smoyer CJ, Jaspersen SL. Patrolling the nucleus: inner nuclear membrane-associated degradation. Curr Genet. 2019;65:1099-106. CrossRef PubMed PubMedCentral
  22. Reits EA, Benham AM, Plougastel B, Neefjes J, Trowsdale J. Dynamics of proteasome distribution in living cells. EMBO J. 1997;16:6087-94. CrossRef PubMed PubMedCentral
  23. Enenkel C, Lehmann A, Kloetzel PM. Subcellular distribution of proteasomes implicates a major location of protein degradation in the nuclear envelope-ER network in yeast. EMBO J. 1998;17:6144-54. CrossRef PubMed PubMedCentral
  24. Takeda K, Yanagida M. Regulation of nuclear proteasome by Rhp6/Ubc2 through ubiquitination and destruction of the sensor and anchor Cut8. Cell. 2005; 122:393-405. CrossRef PubMed
  25. Albert S, Schaffer M, Beck F, Mosalaganti S, Asano S, Thomas HF, Plitzko JM, Beck M, Baumeister W, Engel BD. Proteasomes tether to two distinct sites at the nuclear pore complex. Proc Natl Acad Sci USA. 2017;114:13726-31. CrossRef PubMed PubMedCentral
  26. Wójcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol. 2003;35:579-89. CrossRef
  27. Sixt SU, Dahlmann B. Extracellular, circulating proteasomes and ubiquitin - incidence and relevance. Biochim Biophys Acta. 2008;1782:817-23. CrossRef PubMed
  28. Kulichkova VA, Mittenberg AG, Ermolaeva YB, Tsimokha AS, Volkova IV, Evteeva IN, Kozyukharova IV, Gauze LN, Konstantinova IM. Specificity of the proteasome population secreted from cells into the culture medium. Dokl Biol Sci Proc Acad Sci USSR Biol Sci. 2004;399;503-6. CrossRef PubMed
  29. Lavabre-Bertrand T, Henry L, Carillo S, Guiraud I, Ouali A, Dutaud D, Aubry L, Rossi JF, Bureau JP. Plasma proteasome level is a potential marker in patients with solid tumors and hemopoietic malignancies. Cancer. 2001; 92:2493-500. CrossRef
  30. Egerer K, Kuckelkorn U, Rudolph PE, Rückert JC, Dörner T, Burmester G-R, Kloetzel P-M, Feist E. Circulating proteasomes are markers of cell damage and immunologic activity in autoimmune diseases. J Rheumatol. 2002; 29:2045-52.
  31. Deatherage BL, Cookson BT. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun. 2012; 80:1948-57. CrossRef PubMed PubMedCentral
  32. 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; 68:2667-88. CrossRef PubMed PubMedCentral
  33. Hayashi T, Hoffman MP. Exosomal microRNA communication between tissues during organogenesis. RNA Biol. 2017;14:1683-9. CrossRef PubMed PubMedCentral
  34. Giacomini E, Alleva E, Fornelli G, Quartucci A, Privitera L, Vanni VS, Viganò P. Embryonic extracellular vesicles as informers to the immune cells at the maternal-fetal interface. Clin Exp Immunol. 2019;198:15-23 CrossRef PubMed PubMedCentral
  35. Choi DS, Kim DK, Kim YK, Gho YS. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics. 2013;13:1554-71. CrossRef PubMed
  36. Simons M, Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21:575-81. CrossRef PubMed
  37. 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;62:6312-7.
  38. Bulgari D, Jha A, Deitcher DL, Levitan ES. Myopic (HDPTP, PTPN23) selectively regulates synaptic neuropeptide release. Proc Natl Acad Sci USA. 2018;115:1617-22. CrossRef PubMed PubMedCentral
  39. Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M. Sorting it out: Regulation of exosome loading. Semin Cancer Biol. 2014;28:3-13. CrossRef PubMed PubMedCentral
  40. Aryani A, Denecke B. Exosomes as a nanodelivery system: a key to the future of neuromedicine? Mol Neurobiol. 2016;53:818-21. CrossRef PubMed PubMedCentral
  41. Record M, Carayon K, Poirot M, 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
  42. 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 Rep. 2015;5:10300. CrossRef PubMed PubMedCentral
  43. Nakase I, Noguchi K, Fujii I, Futaki S. Vectorization of biomacromolecules into cells using extracellular vesicles with enhanced internalization induced by macropinocytosis. Sci Rep. 2016;6:34937. CrossRef PubMed PubMedCentral
  44. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature. 2003;422:37-44. CrossRef PubMed
  45. Fruhbeis C, Frohlich D, Kuo WP, Amphornrat J, Thilemann S, Saab AS, Kirchhoff F, et al. Neurotransmitter triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 2013;11:e1001604. CrossRef PubMed PubMedCentral
  46. El-Sayed A, Harashima H. Endocytosis of gene delivery vectors: from clathrin-dependent to lipid raft-mediated endocytosis. Mol Ther. 2013;21:1118-30. CrossRef PubMed PubMedCentral
  47. Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containi exosomes shows multiple plasma membrane functions. Blood. 1989;74:1844-51. CrossRef PubMed
  48. Hurley JH. The ESCRT complexes. Crit Rev Biochem Mol Biol. 2010;45:463-87. CrossRef PubMed PubMedCentral
  49. Haraszti RA, Didiot M-C, Sapp E, Leszyk J, Shaffer SA, Rockwell HE, Gao F, Narain NR, DiFiglia M, Kiebish MA, Aronin N, Khvorova A. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 2016;5:32570. CrossRef PubMed PubMedCentral
  50. Haraszti RA, Miller R, Dubuke ML, Rockwell HE, Coles AH, Sapp E, Didiot M-C, et al. Serum deprivation of mesenchymal stem cells improves exosome activity and alters lipid and protein composition. Science. 2019;16:230-41. CrossRef PubMed PubMedCentral
  51. Lai RC, Tan SS, Teh BJ, Sze SK, Arslan F, de Kleijn DP, Choo A, Lim SK. Proteolytic potential of the MSC exosome proteome: implications for an exosomemediated delivery of therapeutic proteasome. Int J Proteomics. 2012;2012:971907. CrossRef PubMed PubMedCentral
  52. Zoeger A, Blau M, Egerer K, Feist E, Dahlmann B. Circulating proteasomes are functional and have a subtype pattern distinct from 20S proteasomes in major blood cells. Clin Chem. 2006;52:2079-86. CrossRef PubMed
  53. Sixt SU and Dahlmann B. Extracellular, circulating proteasomes and ubiquitin - incidence and relevance. Biochim Biophys Acta. 2008;1782(12):817-23. CrossRef PubMed
  54. Sixt SU and Peters J. Extracellular alveolar proteasome: possible role in lung injury and repair. Proc Am Thorac Soc. 2010;7(1):91-6. CrossRef PubMed
  55. Bec N, Bonhoure A, Henry L, Berry L, Larroque C, Coux O, Stoebner P-E, Vidal M. Proteasome 19S RP and translation preinitiation complexes are secreted within exosomes upon serum starvation. Traffic. 2019;20(7):516-36. CrossRef PubMed
  56. Tsimokha AS, Zaykova JJ, Bottrill A, Barlev NA. Extracellular proteasomes are deficient in 19S subunits as revealed by iTRAQ quantitative proteomics. J Cell Physiol. 2017; 232(4): 842-51. CrossRef PubMed
  57. Kulichkova VA, Artamonova TO, Lyublinskaya OG, Khodorkovskii MA, Tomilin AN, Tsimokha AS. Proteomic analysis of affinity-purified extracellular proteasomes reveals exclusively 20S complexes. Oncotarget. 2017;8(60):102134-49. CrossRef PubMed PubMedCentral
  58. Dieudé M, Bell C, Turgeon J, Beillevaire D, Pomerleau L, Yang B, Hamelin K, Qi S, et al. The 20S proteasome core, active within apoptotic exosome-like vesicles, induces autoantibody production and accelerates rejection. Sci Transl Med. 2015;7(318): 318ra200. CrossRef PubMed
  59. De Paoli SH, Tegegn TZ, Elhelu QK, Strader MB, Patel M, Diduch LL, Tarandovskiy ID, Wu Y, et al. Dissecting the biochemical architecture and morphological release pathways of the human platelet extracellular vesiculome. Cell Mol Life Sci. 2018;75(20): 3781-801. CrossRef PubMed
  60. Ramachandran KV, Fu JM, Schaffer TB, Na CH, Delannoy M, Margolis SS. Activity-dependent degradation of the nascentome by the neuronal membrane proteasome. Mol Cell. 2018;71:169-77. CrossRef PubMed PubMedCentral
  61. Ramachandran KV and Margolis SS. A mammalian nervous-system-specific plasma membrane proteasome complex that modulates neuronal function. Nat Struct Mol Biol. 2017;24:419-30. CrossRef PubMed PubMedCentral
  62. Sixt SU, Beiderlinden M, Jennissen HP, Peters J. Extracellular proteasome in the human alveolar space: a new housekeeping enzyme? Am J Physiol Lung Cell Mol Physiol. 2007;292(5):L1280-8. CrossRef PubMed
  63. Dianzani C, Bellavista E, Liepe J, Verderio C, Martucci M, Santoro A, Chiocchetti A, Gigliotti CL, et al. Extracellular proteasome-osteopontin circuit regulates cell migration with implications in multiple sclerosis. Sci Rep. 2017;7:43718. CrossRef PubMed PubMedCentral

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2024.