Ukr.Biochem.J. 2013; Том 85, № 6, листопад-грудень, c. 183-196

doi: http://dx.doi.org/10.15407/ubj85.06.183

Загибель клітин має солодкий присмак: роль вуглеводів у системі розпізнавання

Р. Білий, Р. Стойка

Інститут біології клітини НАН України, Львів;
e-mail: r.bilyy@nas.gov.ua; stoika@cellbiol.lviv.ua

У статті описано складний шлях, зав­дяки якому зміни глікоепітопів на поверхні відмираючих клітин дозволили виявити специфічні механізми, що лежать в основі реорганізації клітини за апоптозу. Ці глікоепітопи відіграють важливу роль у забезпеченні видалення фрагментів відмираючих клітин з організму, останні, у свою чергу, здатні спричиняти утворення автоантитіл.

Ключові слова: , , , ,


Посилання:

  1. Lawen A. Apoptosis-an introduction. Bioessays. 2003 Sep;25(9):888-96. Review. PubMed, CrossRef
  2. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol. 1992 Apr 1;148(7):2207-16. PubMed
  3. Hochreiter-Hufford A, Ravichandran KS. Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol. 2013 Jan 1;5(1):a008748. Review. PubMed, PubMedCentral, CrossRef
  4. Gabius HJ, Siebert HC, André S, Jiménez-Barbero J, Rüdiger H. Chemical biology of the sugar code. Chembiochem. 2004 Jun 7;5(6):740-64. Review. PubMed, CrossRef
  5. Sharon N, Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology. 2004 Nov;14(11):53R-62R. Review. PubMed, CrossRef
  6. Antonyuk VO. The lectins and their resources [in Ukrainian]. Lviv: Quart, 2005.
  7. Pittoni V, Valesini G. The clearance of apoptotic cells: implications for autoimmunity. Autoimmun Rev. 2002 May;1(3):154-61. Review. PubMed, CrossRef
  8. Geijtenbeek TB, van Vliet SJ, Engering A, ‘t Hart BA, van Kooyk Y. Self- and nonself-recognition by C-type lectins on dendritic cells. Annu Rev Immunol. 2004;22:33-54. Review. PubMed, CrossRef
  9. Cline AM, Radic MZ. Apoptosis, subcellular particles, and autoimmunity. Clin Immunol. 2004 Aug;112(2):175-82. Review. PubMed, CrossRef
  10. Henson PM, Bratton DL, Fadok VA. Apoptotic cell removal. Curr Biol. 2001 Oct 2;11(19):R795-805. Review. PubMed, CrossRef
  11. Fujita T, Matsushita M, Endo Y. The lectin-complement pathway–its role in innate immunity and evolution. Immunol Rev. 2004 Apr;198(1):185-202. Review. PubMed, CrossRef
  12. Bilyy R, Stoika R. Search for novel cell surface markers of apoptotic cells. Autoimmunity. 2007 Jun;40(4):249-53. Review. PubMed, CrossRef
  13. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972 Aug;26(4):239-57. Review. PubMed, PubMedCentral, CrossRef
  14. Duvall E, Wyllie AH, Morris RG. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology. 1985 Oct;56(2):351-8. PubMed, PubMedCentral
  15. Morris RG, Hargreaves AD, Duvall E, Wyllie AH. Hormone-induced cell death. 2. Surface changes in thymocytes undergoing apoptosis. Am J Pathol. 1984 Jun;115(3):426-36. PubMed, PubMedCentral
  16. Dini L, Autuori F, Lentini A, Oliverio S, Piacentini M. The clearance of apoptotic cells in the liver is mediated by the asialoglycoprotein receptor. FEBS Lett. 1992 Jan 20;296(2):174-8. PubMed, CrossRef
  17. Hall SE, Savill JS, Henson PM, Haslett C. Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin. J Immunol. 1994 Oct 1;153(7):3218-27. PubMed
  18. Dini L, Lentini A, Diez GD, Rocha M, Falasca L, Serafino L, Vidal-Vanaclocha F. Phagocytosis of apoptotic bodies by liver endothelial cells. J Cell Sci. 1995 Mar;108 ( Pt 3):967-73. PubMed
  19. Falasca L, Bergamini A, Serafino A, Balabaud C, Dini L. Human Kupffer cell recognition and phagocytosis of apoptotic peripheral blood lymphocytes. Exp Cell Res. 1996 Apr 10;224(1):152-62. PubMed, CrossRef
  20. Verhoven B, Krahling S, Schlegel RA, Williamson P. Regulation of phosphatidylserine exposure and phagocytosis of apoptotic T lymphocytes. Cell Death Differ. 1999 Mar;6(3):262-70. PubMed, CrossRef
  21. Verhoven B, Schlegel RA, Williamson P. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J Exp Med. 1995 Nov 1;182(5):1597-601. PubMed, PubMedCentral, CrossRef
  22. Krahling S, Callahan MK, Williamson P, Schlegel RA. Exposure of phosphatidylserine is a general feature in the phagocytosis of apoptotic lymphocytes by macrophages. Cell Death Differ. 1999 Feb;6(2):183-9. PubMed, CrossRef
  23. Reutelingsperger CP, Christiaan Peter M. (inventors). Method for detecting and/or optionally quantifying and/or separating apoptotic cells in or from a sample. United States patent 5,834,196.
  24. van den Eijnde SM, Luijsterburg AJ, Boshart L, De Zeeuw CI, van Dierendonck JH, Reutelingsperger CP, Vermeij-Keers C. In situ detection of apoptosis during embryogenesis with annexin V: from whole mount to ultrastructure. Cytometry. 1997 Dec 1;29(4):313-20. PubMed, CrossRef
  25. Chaurio RA, Janko C, Muñoz LE, Frey B, Herrmann M, Gaipl US. Phospholipids: key players in apoptosis and immune regulation. Molecules. 2009 Nov 30;14(12):4892-914. Review. PubMed, CrossRef
  26. Li W. Eat-me signals: keys to molecular phagocyte biology and “appetite” control. J Cell Physiol. 2012 Apr; 227(4):1291-1297. PubMed, PubMedCentralCrossRef
  27. Frey B, Munoz LE, Pausch F, Sieber R, Franz S, Brachvogel B, Poschl E, Schneider H, Rödel F, Sauer R, Fietkau R, Herrmann M, Gaipl US. The immune reaction against allogeneic necrotic cells is reduced in Annexin A5 knock out mice whose macrophages display an anti-inflammatory phenotype. J Cell Mol Med. 2009 Jul;13(7):1391-9. PubMed, PubMedCentral, CrossRef
  28. Munoz LE, Frey B, Pausch F, Baum W, Mueller RB, Brachvogel B, Poschl E, Rödel F, von der Mark K, Herrmann M, Gaipl US. The role of annexin A5 in the modulation of the immune response against dying and dead cells. Curr Med Chem. 2007;14(3):271-7. Review. PubMed, CrossRef
  29. Rapoport E, Pendu JL. Glycosylation alterations of cells in late phase apoptosis from colon carcinomas. Glycobiology. 1999 Dec;9(12):1337-45. PubMed, CrossRef
  30. Bilyy RO, Stoika RS. Lectinocytochemical detection of apoptotic murine leukemia L1210 cells. Cytometry A. 2003 Dec;56(2):89-95. PubMed, CrossRef
  31. Heyder P, Gaipl US, Beyer TD, Voll RE, Kern PM, Stach C, Kalden JR, Herrmann M. Early detection of apoptosis by staining of acid-treated apoptotic cells with FITC-labeled lectin from Narcissus pseudonarcissus. Cytometry A. 2003 Oct;55(2):86-93. PubMed, CrossRef
  32. Bilyy RO, Antonyuk VO, Stoika RS. Cytochemical study of role of alpha-d-mannose- and beta-d-galactose-containing glycoproteins in apoptosis. J Mol Histol. 2004 Nov;35(8-9):829-38. PubMed, CrossRef
  33. Azuma Y, Taniguchi A, Matsumoto K. Decrease in cell surface sialic acid in etoposide-treated Jurkat cells and the role of cell surface sialidase. Glycoconj J. 2000 May;17(5):301-6. PubMed, CrossRef
  34. Batisse C, Marquet J, Greffard A, Fleury-Feith J, Jaurand MC, Pilatte Y. Lectin-based three-color flow cytometric approach for studying cell surface glycosylation changes that occur during apoptosis. Cytometry A. 2004 Dec;62(2):81-8. PubMed, CrossRef
  35. Bilyy R., Tomyn A., Stoika R. Membrane glycoproteins during cell death: how and why they appear on the cell surface? J. Physiol. Sci. 2009;59(S1):155.
  36. Franz S, Frey B, Sheriff A, Gaipl US, Beer A, Voll RE, Kalden JR, Herrmann M. Lectins detect changes of the glycosylation status of plasma membrane constituents during late apoptosis. Cytometry A. 2006 Apr;69(4):230-9. PubMed, CrossRef
  37. Bilyy R, Kit Y, Hellman U, Tryndyak V, Kaminskyy V, Stoika R. In vivo expression and characteristics of novel alpha-D-mannose-rich glycoprotein markers of apoptotic cells. Cell Biol Int. 2005 Nov;29(11):920-8. PubMed, CrossRef
  38. Bilyy R, Kit Y, Hellman U, Stoika R. AMID: new insights on its intracellular localization and expression at apoptosis. Apoptosis. 2008 May;13(5):729-32. PubMed, CrossRef
  39. Bilyy RO, Shkandina T, Tomin A, Muñoz LE, Franz S, Antonyuk V, Kit YY, Zirngibl M, Fürnrohr BG, Janko C, Lauber K, Schiller M, Schett G, Stoika RS, Herrmann M. Macrophages discriminate glycosylation patterns of apoptotic cell-derived microparticles. J Biol Chem. 2012 Jan 2;287(1):496-503. PubMed, PubMedCentral, CrossRef
  40. Miyagi T. Aberrant expression of sialidase and cancer progression. Proc Jpn Acad Ser B Phys Biol Sci. 2008;84(10):407-18. Review. PubMed, PubMedCentral, CrossRef
  41. Achyuthan KE, Achyuthan AM. Comparative enzymology, biochemistry and pathophysiology of human exo-alpha-sialidases (neuraminidases). Comp Biochem Physiol B Biochem Mol Biol. 2001 May;129(1):29-64. Review. PubMed, CrossRef
  42. Nayak DP, Reichl U. Neuraminidase activity assays for monitoring MDCK cell culture derived influenza virus. J Virol Methods. 2004 Dec 1;122(1):9-15. PubMed, CrossRef
  43. Tomin A, Shkandina T, Bilyy R. Novel assay for direct fluorescent imaging of sialidase activity . Proc. SPIE   8087, Clinical and Biomedical Spectroscopy and Imaging II, 80871Z (June 14, 2011).  CrossRef
  44. Bilyy R., Tomin A., Stoika R. (inventors). Method of neuraminidase activity detection in cells and cellular compartments. UA Patent No. 93816 patent.
  45. Shkandina T, Herrmann M, Bilyy R. Sweet kiss of dying cell: sialidase activity on apoptotic cell is able to act toward its neighbors. Autoimmunity. 2012 Dec;45(8):574-8.  PubMed, CrossRef
  46. Herscovics A, Orlean P. Glycoprotein biosynthesis in yeast. FASEB J. 1993 Apr 1;7(6):540-50. Review. PubMed
  47. Kornfeld R, Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54(1):631-64. Review. PubMed, CrossRef
  48. Helenius J, Aebi M. Transmembrane movement of dolichol linked carbohydrates during N-glycoprotein biosynthesis in the endoplasmic reticulum. Semin Cell Dev Biol. 2002 Jun;13(3):171-8. Review. PubMed, CrossRef
  49. Alaimo C, Catrein I, Morf L, Marolda CL, Callewaert N, Valvano MA, Feldman MF, Aebi M. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J. 2006 Mar 8;25(5):967-76. PubMed, PubMedCentral, CrossRef
  50. Hubbard SC, Ivatt RJ. Synthesis and processing of asparagine-linked oligosaccharides. Annu Rev Biochem. 1981;50(1):555-83. Review. PubMed, CrossRef
  51. Franz S, Herrmann K, Fürnrohr BG, Sheriff A, Frey B, Gaipl US, Voll RE, Kalden JR, Jäck HM, Herrmann M. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ. 2007 Apr;14(4):733-42. PubMed, CrossRef
  52. Grieve AG, Rabouille C. Golgi bypass: skirting around the heart of classical secretion. Cold Spring Harb Perspect Biol. 2011 Apr 1;3(4). pii: a005298. Review. PubMed, PubMedCentral, CrossRef
  53. Marie M, Sannerud R, Avsnes Dale H, Saraste J. Take the ‘A’ train: on fast tracks to the cell surface. Cell Mol Life Sci. 2008 Sep;65(18):2859-74. Review. PubMed, CrossRef
  54. Casciola-Rosen LA, Anhalt G, Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med. 1994 Apr 1;179(4):1317-30. PubMed, PubMedCentral, CrossRef
  55. Munoz LE, Herrmann M, Gaipl US. An impaired detection and clearance of dying cells can lead to the development of chronic autoimmunity. Z Rheumatol. 2005 Sep;64(6):370-6. German. PubMed, CrossRef
  56. Michlewska S, McColl A, Rossi AG, Megson IL, Dransfield I. Clearance of dying cells and autoimmunity. Autoimmunity. 2007 Jun;40(4):267-73. Review. PubMed, CrossRef
  57. Schulze C, Sarter K, Herrmann M. Do we already understand all aspects connecting clearance and autoimmunity? Autoimmunity. 2007 Jun;40(4):239-43. PubMed, CrossRef
  58. Muñoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol. 2010 May;6(5):280-9. Review. PubMed, CrossRef
  59. Gaipl US, Munoz LE, Grossmayer G, Lauber K, Franz S, Sarter K, Voll RE, Winkler T, Kuhn A, Kalden J, Kern P, Herrmann M. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun. 2007 Mar-May;28(2-3):114-21. PubMed, CrossRef
  60. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, Métivier D, Larochette N, van Endert P, Ciccosanti F, Piacentini M, Zitvogel L, Kroemer G. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007 Jan;13(1):54-61. PubMed, CrossRef
  61. Meesmann HM, Fehr EM, Kierschke S, Herrmann M, Bilyy R, Heyder P, Blank N, Krienke S, Lorenz HM, Schiller M. Decrease of sialic acid residues as an eat-me signal on the surface of apoptotic lymphocytes. J Cell Sci. 2010 Oct 1;123(Pt 19):3347-56. PubMed, CrossRef
  62. Köttgen E, Reutter W, Tauber R. Human lectins and their correspondent glycans in cell biology and clinical medicine. Med Klin (Munich). 2003 Dec 15;98(12):717-38. Review. German. PubMed, CrossRef
  63. Crocker PR, Paulson JC, Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol. 2007 Apr;7(4):255-66. Review. PubMed, CrossRef
  64. Gouin SG, Wellens A, Bouckaert J, Kovensky J. Synthetic multimeric heptyl mannosides as potent antiadhesives of uropathogenic Escherichia coli. Chem Med Chem. 2009 May;4(5):749-55. PubMed, CrossRef
  65. Beer A, André S, Kaltner H, Lensch M, Franz S, Sarter K, Schulze C, Gaipl US, Kern P, Herrmann M, Gabius HJ. Human galectins as sensors for apoptosis/necrosis-associated surface changes of granulocytes and lymphocytes. Cytometry A. 2008 Feb;73(2):139-47. PubMed, CrossRef
  66. Pavlovic M, Kats A, Cavallo M, Chen R, Hartmann JX, Shoenfeld Y. Pathogenic and Epiphenomenal Anti-DNA Antibodies in SLE. Autoimmune Dis. 2010 Jul 20;2011:462841.  PubMed, PubMedCentralCrossRef
  67. Schiller M, Heyder P, Ziegler S, Niessen A, Claßen L, Lauffer A, Lorenz HM. During apoptosis HMGB1 is translocated into apoptotic cell-derived membranous vesicles. Autoimmunity. 2013 Aug;46(5):342-6. PubMed, CrossRef

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.