Protein cross-linking by chlorinated polyamines and transglutamylation stabilizes neutrophil extracellular traps

Cell Death and Disease

Volumn 7, Issue 8, 2016, Pages

  Csomós, Krisztián ^a,b   Kristóf, Endre ^a   Jakob, Bernadett ^a   Csomós, István ^a   Kovács, György ^a,c   Rotem, Omri ^a   Hodrea, Judit ^a,d   Bagoly, Zsuzsa ^a   Muszbek, Laszlo ^a   Balajthy, Zoltán ^a   Csősz, Éva ^a   Fésüs, László ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c Analytical Minds Ltd   (Hungary)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DIAMINE; MONOAMINE; POLYAMINE; CROSS LINKING REAGENT; PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR TRAP; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; MICROORGANISM; MONOCYTE; NEUTROPHIL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; WESTERN BLOTTING; DRUG EFFECTS; HALOGENATION; METABOLISM; PROTEOMICS; STAPHYLOCOCCUS AUREUS;

CROSS-LINKING REAGENTS; EXTRACELLULAR TRAPS; HALOGENATION; HUMANS; NEUTROPHILS; POLYAMINES; PROTEINS; PROTEOMICS; STAPHYLOCOCCUS AUREUS; TRANSGLUTAMINASES;

EID: 85013262896     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.200     Document Type: Article

References (63)

1. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532–1535.
2. Stoiber W, Obermayer A, Steinbacher P, Krautgartner WD. The role of reactive oxygen species (ROS) in the formation of extracellular traps (ETs) in humans. Biomolecules 2015; 5: 702–723.
3. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5: e1000639.
4. Thomas EL, Jefferson MM, Grisham MB. Myeloperoxidase-catalyzed incorporation of amines into proteins: role of hypochlorous acid and dichloramines. Biochemistry 1982; 21: 6299–6308.
5. Babior BM, Kipnes RS. Superoxide-forming enzyme from human neutrophils: evidence for a flavin requirement. Blood 1977; 50: 517–524.
6. Klebanoff SJ. Myeloperoxidase-halide-hydrogen peroxide antibacterial system. J Bacteriol 1968; 95: 2131–2138.
7. Metzler KD, Fuchs TA, Nauseef WM, Reumaux D, Roesler J, Schulze I et al. Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 2011; 117: 953–959.
8. Chung SI, Lewis MS, Folk JE. Relationships of the catalytic properties of human plasma and platelet transglutaminases (activated blood coagulation factor XIII) to their subunit structures. J Biol Chem 1974; 249: 940–950.
9. Muszbek L, Bereczky Z, Bagoly Z, Komaromi I, Katona E. Factor XIII: a coagulation factor with multiple plasmatic and cellular functions. Physiol Rev 2011; 91: 931–972.
10. Mosher DF. Cross-linking of fibronectin to collagenous proteins. Mol Cell Biochem 1984; 58: 63–68.
11. Aeschlimann D, Paulsson M, Mann K. Identification of Gln726 in nidogen as the amine acceptor in transglutaminase-catalyzed cross-linking of laminin-nidogen complexes. J Biol Chem 1992; 267: 11316–11321.
12. Rosenblatt S, Bassuk JA, Alpers CE, Sage EH, Timpl R, Preissner KT. Differential modulation of cell adhesion by interaction between adhesive and counter-adhesive proteins: characterization of the binding of vitronectin to osteonectin (BM40, SPARC). Biochem J 1997; 324: 311–319.
13. Kleman JP, Aeschlimann D, Paulsson M, van der Rest M. Transglutaminase-catalyzed cross-linking of fibrils of collagen V/XI in A204 rhabdomyosarcoma cells. Biochemistry 1995; 34: 13768–13775.
14. Mosher DF, Schad PE. Cross-linking of fibronectin to collagen by blood coagulation Factor XIIIa. J Clin Invest 1979; 64: 781–787.
15. Skorstengaard K, Halkier T, Hojrup P, Mosher D. Sequence location of a putative transglutaminase cross-linking site in human vitronectin. FEBS Lett 1990; 262: 269–274.
16. Usui T, Takagi J, Saito Y. Propolypeptide of von Willebrand factor serves as a substrate for factor XIIIa and is cross-linked to laminin. J Biol Chem 1993; 268: 12311–12316.
17. Takagi J, Aoyama T, Ueki S, Ohba H, Saito Y, Lorand L. Identification of factor-XIIIa-reactive glutaminyl residues in the propolypeptide of bovine von Willebrand factor. Eur J Biochem 1995; 232: 773–777.
18. Matsuka YV, Migliorini MM, Ingham KC. Cross-linking of fibronectin to C-terminal fragments of the fibrinogen alpha-chain by factor XIIIa. J Protein Chem 1997; 16: 739–745.
19. Kim HC, Lewis MS, Gorman JJ, Park SC, Girard JE, Folk JE et al. Protransglutaminase E from guinea pig skin. Isolation and partial characterization. J Biol Chem 1990; 265: 21971–21978.
20. Kim HC, Idler WW, Kim IG, Han JH, Chung SI, Steinert PM. The complete amino acid sequence of the human transglutaminase K enzyme deduced from the nucleic acid sequences of cDNA clones. J Biol Chem 1991; 266: 536–539.
21. Steinert PM, Marekov LN. The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J Biol Chem 1995; 270: 17702–17711.
22. Folk JE. Transglutaminases. Annu Rev Biochem 1980; 49: 517–531.
23. Beninati S, Martinet N, Folk JE. High-performance liquid chromatographic method for the determination of epsilon-(gamma-glutamyl)lysine and mono-and bis-gamma-glutamyl derivatives of putrescine and spermidine. J Chromatogr 1988; 443: 329–335.
24. Davies PJ, Chiocca EA, Basilion JP, Poddar S, Stein JP. Transglutaminases and their regulation: implications for polyamine metabolism. Adv Exp Med Biol 1988; 250: 391–401.
25. Lee KN, Birckbichler PJ, Patterson MK Jr. Colorimetric assay of blood coagulation factor XIII in plasma. Clin Chem 1988; 34: 906–910.
26. Ogata K, Tamura M, Takeshita M. Spermine down-regulates superoxide generation induced by fMet-Leu-Phe in electropermeabilized human neutrophils. Biochem Biophys Res Commun 1992; 182: 20–26.
27. Ogata K, Nishimoto N, Uhlinger DJ, Igarashi K, Takeshita M, Tamura M. Spermine suppresses the activation of human neutrophil NADPH oxidase in cell-free and semi-recombinant systems. Biochem J 1996; 313: 549–554.
28. Gotze M, Pettelkau J, Schaks S, Bosse K, Ihling CH, Krauth F et al. StavroX–a software for analyzing crosslinked products in protein interaction studies. J Am Soc Mass Spectrom 2012; 23: 76–87.
29. Martinet N, Beninati S, Nigra TP, Folk JE. N1N8-bis(gamma-glutamyl)spermidine cross-linking in epidermal-cell envelopes. Comparison of cross-link levels in normal and psoriatic cell envelopes. Biochem J 1990; 271: 305–308.
30. Piacentini M, Farrace MG, Imparato M, Piredda L, Autuori F. Polyamine-dependent post-translational modification of proteins in differentiating mouse epidermal cells. J Invest Dermatol 1990; 94: 694–699.
31. Steinert PM, Chung SI, Kim SY. Inactive zymogen and highly active proteolytically processed membrane-bound forms of the transglutaminase 1 enzyme in human epidermal keratinocytes. Biochem Biophys Res Commun 1996; 221: 101–106.
32. Lorand L, Campbell-Wilkes LK, Cooperstein L. A filter paper assay for transamidating enzymes using radioactive amine substrates. Anal Biochem 1972; 50: 623–631.
33. Al-Jallad HF, Myneni VD, Piercy-Kotb SA, Chabot N, Mulani A, Keillor JW et al. Plasma membrane factor XIIIA transglutaminase activity regulates osteoblast matrix secretion and deposition by affecting microtubule dynamics. PLoS One 2011; 6: e15893.
34. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 2012; 198: 773–783.
35. Obermayer A, Stoiber W, Krautgartner WD, Klappacher M, Kofler B, Steinbacher P et al. New aspects on the structure of neutrophil extracellular traps from chronic obstructive pulmonary disease and in vitro generation. PLoS One 2014; 9: e97784.
36. Brooks WH. Increased polyamines alter chromatin and stabilize autoantigens in autoimmune diseases. Front Immunol 2013; 4: 91.
37. Thomas EL, Grisham MB, Jefferson MM. Myeloperoxidase-dependent effect of amines on functions of isolated neutrophils. J Clin Invest 1983; 72: 441–454.
38. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010; 191: 677–691.
39. Masuda M, Betancourt L, Matsuzawa T, Kashimoto T, Takao T, Shimonishi Y et al. Activation of rho through a cross-link with polyamines catalyzed by Bordetella dermonecrotizing toxin. EMBO J 2000; 19: 521–530.
40. Lentini A, Tabolacci C, Mattioli P, Provenzano B, Beninati S. Spermidine delays eye lens opacification in vitro by suppressing transglutaminase-catalyzed crystallin cross-linking. Protein J 2011; 30: 109–114.
41. Song Y, Kirkpatrick LL, Schilling AB, Helseth DL, Chabot N, Keillor JW et al. Transglutaminase and polyamination of tubulin: posttranslational modification for stabilizing axonal microtubules. Neuron 2013; 78: 109–123.
42. Yu CH, Chou CC, Lee YJ, Khoo KH, Chang GD. Uncovering protein polyamination by the spermine-specific antiserum and mass spectrometric analysis. Amino Acids 2015; 47: 469–481.
43. Candi E, Schmidt R, Melino G. The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol 2005; 6: 328–340.
44. Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008; 180: 1895–1902.
45. Tarcsa E, Marekov LN, Mei G, Melino G, Lee SC, Steinert PM. Protein unfolding by peptidylarginine deiminase. Substrate specificity and structural relationships of the natural substrates trichohyalin and filaggrin. J Biol Chem 1996; 271: 30709–30716.
46. Saunders DN, Buttigieg KM, Gould A, McPhun V, Baker MS. Immunological detection of conformational neoepitopes associated with the serpin activity of plasminogen activator inhibitor type-2. J Biol Chem 1998; 273: 10965–10971.
47. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318–1321.
48. Allam R, Scherbaum CR, Darisipudi MN, Mulay SR, Hagele H, Lichtnekert J et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 2012; 23: 1375–1388.
49. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 2012; 7: e32366.
50. Allam R, Darisipudi MN, Tschopp J, Anders HJ. Histones trigger sterile inflammation by activating the NLRP3 inflammasome. Eur J Immunol 2013; 43: 3336–3342.
51. Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 2011; 187: 2626–2631.
52. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood 2011; 118: 3708–3714.
53. Martinod K, Demers M, Fuchs TA, Wong SL, Brill A, Gallant M et al. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proc Natl Acad Sci USA 2013; 110: 8674–8679.
54. Lam FW, Cruz MA, Leung HC, Parikh KS, Smith CW, Rumbaut RE. Histone induced platelet aggregation is inhibited by normal albumin. Thromb Res 2013; 132: 69–76.
55. Dwivedi N, Upadhyay J, Neeli I, Khan S, Pattanaik D, Myers L et al. Felty's syndrome autoantibodies bind to deiminated histones and neutrophil extracellular chromatin traps. Arthritis Rheum 2012; 64: 982–992.
56. Pratesi F, Dioni I, Tommasi C, Alcaro MC, Paolini I, Barbetti F et al. Antibodies from patients with rheumatoid arthritis target citrullinated histone 4 contained in neutrophils extracellular traps. Ann Rheum Dis 2014; 73: 1414–1422.
57. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA 2010; 107: 9813–9818.
58. Bosch X. Systemic lupus erythematosus and the neutrophil. N Engl J Med 2011; 365: 758–760.
59. Leffler J, Martin M, Gullstrand B, Tyden H, Lood C, Truedsson L et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol 2012; 188: 3522–3531.
60. Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 2002; 27: 534–539.
61. Szondy Z, Sarang Z, Molnar P, Nemeth T, Piacentini M, Mastroberardino PG et al. Transglutaminase 2-/-mice reveal a phagocytosis-associated crosstalk between macrophages and apoptotic cells. Proc Natl Acad Sci USA 2003; 100: 7812–7817.
62. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248–254.
63. Hitomi K, Kitamura M, Alea MP, Ceylan I, Thomas V, El Alaoui S. A specific colorimetric assay for measuring transglutaminase 1 and factor XIII activities. Anal Biochem 2009; 394: 281–283.