A Novel Mechanism of Bacterial Toxin Transfer within Host Blood Cell-Derived Microvesicles

PLoS Pathogens

Volumn 11, Issue 2, 2015, Pages

  Ståhl, Anne lie ^a   Arvidsson, Ida ^a   Johansson, Karl E ^a   Chromek, Milan ^a   Rebetz, Johan ^a   Loos, Sebastian ^a   Kristoffersson, Ann Charlotte ^a   Békássy, Zivile D ^a   Mörgelin, Matthias ^a   Karpman, Diana ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CD38 ANTIGEN; CD45 ANTIGEN; FLUORESCEIN ISOTHIOCYANATE; GLYCOPHORIN A; GLYCOPROTEIN IB ALPHA; IMMUNOGLOBULIN G ANTIBODY; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; SHIGA TOXIN; VIRULENCE FACTOR;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BASEMENT MEMBRANE; BLOOD CELL; CAPILLARY ENDOTHELIAL CELL; CELL DEATH; CELL ULTRASTRUCTURE; CELL VIABILITY ASSAY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; ENDOCYTOSIS; ENDOTHELIAL MICROPARTICLE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI O157; FEMALE; FLOW CYTOMETRY; GENETIC TRANSFECTION; HEMOLYTIC UREMIC SYNDROME; HUMAN; HUMAN TISSUE; IMMORTALIZED CELL LINE; IMMUNE EVASION; IMMUNOELECTRON MICROSCOPY; IMMUNOSTIMULATION; KIDNEY BIOPSY; KIDNEY CORTEX; KIDNEY FAILURE; KIDNEY TUBULE EPITHELIUM; MALE; MICROVESICLE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PODOCYTE; PROTEIN SYNTHESIS INHIBITION; RADIOIMMUNOPRECIPITATION; THROMBOCYTE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; ESCHERICHIA COLI INFECTION; HOST PATHOGEN INTERACTION; INFANT; MEMBRANE MICROPARTICLE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PRESCHOOL CHILD; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MUS;

ADOLESCENT; ADULT; ANIMALS; BACTERIAL TOXINS; BLOOD CELLS; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; INFANT; MALE; MICE; MICE, INBRED BALB C; PROTEIN TRANSPORT;

EID: 84924405786     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004619     Document Type: Article

References (67)

1. McKee ML, O'Brien AD, (1995) Investigation of enterohemorrhagic Escherichia coli O157:H7 adherence characteristics and invasion potential reveals a new attachment pattern shared by intestinal E. coli. Infect Immun 63: 2070–2074. 7537254
2. Habib R, Kaplan BS, Trompeter R.S., Moake J.L., (1992) Pathology of the Hemolytic Uremic Syndrome. In: Hemolytic Uremic Syndrome and Thrombotic thrombocytopenic purpura. New York: Marcel Dekker Inc. 1300882
3. Karpman D, Håkansson A, Perez MT, Isaksson C, Carlemalm E, et al. (1998) Apoptosis of renal cortical cells in the hemolytic-uremic syndrome: in vivo and in vitro studies. Infect Immun 66: 636–644. 9453620
4. Wadolkowski EA, Sung LM, Burris JA, Samuel JE, O'Brien AD, (1990) Acute renal tubular necrosis and death of mice orally infected with Escherichia coli strains that produce Shiga-like toxin type II. Infect Immun 58: 3959–3965. 2254023
5. Karpman D, Connell H, Svensson M, Scheutz F, Alm P, et al. (1997) The role of lipopolysaccharide and Shiga-like toxin in a mouse model of Escherichia coli O157:H7 infection. J Infect Dis 175: 611–620. 9041333
6. Chromek M, Arvidsson I, Karpman D, (2012) The antimicrobial peptide cathelicidin protects mice from Escherichia coli O157:H7-mediated disease. PLoS One 7: e46476. doi: 10.1371/journal.pone.0046476 23077510
7. Psotka MA, Obata F, Kolling GL, Gross LK, Saleem MA, et al. (2009) Shiga toxin 2 targets the murine renal collecting duct epithelium. Infect Immun 77: 959–969. doi: 10.1128/IAI.00679-08 19124603
8. Calderon Toledo C, Rogers TJ, Svensson M, Tati R, Fischer H, et al. (2008) Shiga toxin-mediated disease in MyD88-deficient mice infected with Escherichia coli O157:H7. Am J Pathol 173: 1428–1439. doi: 10.2353/ajpath.2008.071218 18832584
9. Békássy ZD, Calderon Toledo C, Leoj G, Kristoffersson A, Leopold SR, et al. (2011) Intestinal damage in enterohemorrhagic Escherichia coli infection. Pediatr Nephrol 26: 2059–2071. doi: 10.1007/s00467-010-1616-9 20809220
10. Lindberg AA, Brown JE, Strömberg N, Westling-Ryd M, Schultz JE, et al. (1987) Identification of the carbohydrate receptor for Shiga toxin produced by Shigella dysenteriae type 1. J Biol Chem 262: 1779–1785. 3543013
11. Sandvig K, Garred O, Prydz K, Kozlov JV, Hansen SH, et al. (1992) Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature 358: 510–512. 1641040
12. Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, et al. (1988) Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem 171: 45–50. 3276522
13. Waddell T, Cohen A, Lingwood CA, (1990) Induction of verotoxin sensitivity in receptor-deficient cell lines using the receptor glycolipid globotriosylceramide. Proc Natl Acad Sci U S A 87: 7898–7901. 2236008
14. Chark D, Nutikka A, Trusevych N, Kuzmina J, Lingwood C, (2004) Differential carbohydrate epitope recognition of globotriaosyl ceramide by verotoxins and a monoclonal antibody. Eur J Biochem 271: 405–417. 14717708
15. Jacewicz MS, Mobassaleh M, Gross SK, Balasubramanian KA, Daniel PF, et al. (1994) Pathogenesis of Shigella diarrhea: XVII. A mammalian cell membrane glycolipid, Gb3, is required but not sufficient to confer sensitivity to Shiga toxin. J Infect Dis 169: 538–546. 8158025
16. Khan F, Proulx F, Lingwood CA, (2009) Detergent-resistant globotriaosyl ceramide may define verotoxin/glomeruli-restricted hemolytic uremic syndrome pathology. Kidney Int 75: 1209–1216. doi: 10.1038/ki.2009.7 19212418
17. Schüller S, Frankel G, Phillips AD, (2004) Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell Microbiol 6: 289–301. 14764112
18. Petruzziello-Pellegrini TN, Yuen DA, Page AV, Patel S, Soltyk AM, et al. (2012) The CXCR4/CXCR7/SDF-1 pathway contributes to the pathogenesis of Shiga toxin-associated hemolytic uremic syndrome in humans and mice. J Clin Invest 122: 759–776. doi: 10.1172/JCI57313 22232208
19. Morigi M, Galbusera M, Gastoldi S, Locatelli M, Buelli S, et al. (2011) Alternative pathway activation of complement by Shiga toxin promotes exuberant C3a formation that triggers microvascular thrombosis. J Immunol 187: 172–180. doi: 10.4049/jimmunol.1100491 21642543
20. Keepers TR, Psotka MA, Gross LK, Obrig TG, (2006) A murine model of HUS: Shiga toxin with lipopolysaccharide mimics the renal damage and physiologic response of human disease. J Am Soc Nephrol 17: 3404–3414. 17082244
21. Brigotti M, Tazzari PL, Ravanelli E, Carnicelli D, Rocchi L, et al. (2011) Clinical relevance of shiga toxin concentrations in the blood of patients with hemolytic uremic syndrome. Pediatr Infect Dis J 30: 486–490. doi: 10.1097/INF.0b013e3182074d22 21164386
22. Ståhl AL, Sartz L, Nelsson A, Békássy ZD, Karpman D, (2009) Shiga toxin and lipopolysaccharide induce platelet-leukocyte aggregates and tissue factor release, a thrombotic mechanism in hemolytic uremic syndrome. PLoS One 4: e6990. doi: 10.1371/journal.pone.0006990 19750223
23. Brigotti M, Caprioli A, Tozzi AE, Tazzari PL, Ricci F, et al. (2006) Shiga toxins present in the gut and in the polymorphonuclear leukocytes circulating in the blood of children with hemolytic-uremic syndrome. J Clin Microbiol 44: 313–317. 16455876
24. Brigotti M, Tazzari PL, Ravanelli E, Carnicelli D, Barbieri S, et al. (2010) Endothelial damage induced by Shiga toxins delivered by neutrophils during transmigration. J Leukoc Biol 88: 201–210. doi: 10.1189/jlb.0709475 20371598
25. te Loo DM, Monnens LA, van Der Velden TJ, Vermeer MA, Preyers F, et al. (2000) Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome. Blood 95: 3396–3402. 10828021
26. Karpman D, Papadopoulou D, Nilsson K, Sjögren AC, Mikaelsson C, et al. (2001) Platelet activation by Shiga toxin and circulatory factors as a pathogenetic mechanism in the hemolytic uremic syndrome. Blood 97: 3100–3108. 11342436
27. Ståhl AL, Sartz L, Karpman D, (2011) Complement activation on platelet-leukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood 117: 5503–5513. doi: 10.1182/blood-2010-09-309161 21447825
28. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM, (2005) Membrane microparticles: two sides of the coin. Physiology (Bethesda) 20: 22–27.
29. Simak J, Gelderman MP, (2006) Cell membrane microparticles in blood and blood products: potentially pathogenic agents and diagnostic markers. Transfus Med Rev 20: 1–26. 16373184
30. Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, et al. (2000) Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 6: 769–775. 10888925
31. Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, et al. (2003) Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS 17: 33–42. 12478067
32. Mause SF, von Hundelshausen P, Zernecke A, Koenen RR, Weber C, (2005) Platelet microparticles: a transcellular delivery system for RANTES promoting monocyte recruitment on endothelium. Arterioscler Thromb Vasc Biol 25: 1512–1518. 15890969
33. Risitano A, Beaulieu LM, Vitseva O, Freedman JE, (2012) Platelets and platelet-like particles mediate intercellular RNA transfer. Blood 119: 6288–6295. doi: 10.1182/blood-2011-12-396440 22596260
34. Diehl P, Fricke A, Sander L, Stamm J, Bassler N, et al. (2012) Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 93: 633–644. doi: 10.1093/cvr/cvs007 22258631
35. Ge S, Hertel B, Emden SH, Beneke J, Menne J, et al. (2012) Microparticle generation and leucocyte death in Shiga toxin-mediated HUS. Nephrol Dial Transplant 27: 2768–2775. doi: 10.1093/ndt/gfr748 22234918
36. Meckes DG, Jr.Raab-Traub N, (2011) Microvesicles and viral infection. J Virol 85: 12844–12854. doi: 10.1128/JVI.05853-11 21976651
37. Bauwens A, Betz J, Meisen I, Kemper B, Karch H, et al. (2013) Facing glycosphingolipid-Shiga toxin interaction: dire straits for endothelial cells of the human vasculature. Cell Mol Life Sci 70: 425–457. doi: 10.1007/s00018-012-1060-z 22766973
38. Okuda T, Tokuda N, Numata S, Ito M, Ohta M, et al. (2006) Targeted disruption of Gb3/CD77 synthase gene resulted in the complete deletion of globo-series glycosphingolipids and loss of sensitivity to verotoxins. J Biol Chem 281: 10230–10235. 16476743
39. Schüller S, (2011) Shiga toxin interaction with human intestinal epithelium. Toxins (Basel) 3: 626–639. doi: 10.3390/toxins3060626 22069729
40. Malyukova I, Murray KF, Zhu C, Boedeker E, Kane A, et al. (2009) Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis. Am J Physiol Gastrointest Liver Physiol 296: G78–92. doi: 10.1152/ajpgi.90347.2008 18974311
41. Griener TP, Mulvey GL, Marcato P, Armstrong GD, (2007) Differential binding of Shiga toxin 2 to human and murine neutrophils. J Med Microbiol 56: 1423–1430. 17965340
42. Arfilli V, Carnicelli D, Rocchi L, Ricci F, Pagliaro P, et al. (2010) Shiga toxin 1 and ricin A chain bind to human polymorphonuclear leucocytes through a common receptor. Biochem J 432: 173–180. doi: 10.1042/BJ20100455 20809900
43. Cooling LL, Walker KE, Gille T, Koerner TA, (1998) Shiga toxin binds human platelets via globotriaosylceramide (Pk antigen) and a novel platelet glycosphingolipid. Infect Immun 66: 4355–4366. 9712788
44. van Setten PA, Monnens LA, Verstraten RG, van den Heuvel LP, van Hinsbergh VW, (1996) Effects of verocytotoxin-1 on nonadherent human monocytes: binding characteristics, protein synthesis, and induction of cytokine release. Blood 88: 174–183. 8704172
45. Bitzan M, Richardson S, Huang C, Boyd B, Petric M, et al. (1994) Evidence that verotoxins (Shiga-like toxins) from Escherichia coli bind to P blood group antigens of human erythrocytes in vitro. Infect Immun 62: 3337–3347. 8039905
46. Fontaine A, Arondel J, Sansonetti PJ, (1988) Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a Tox- mutant of Shigella dysenteriae 1. Infect Immun 56: 3099–3109. 3053452
47. Ståhl AL, Svensson M, Mörgelin M, Svanborg C, Tarr PI, et al. (2006) Lipopolysaccharide from enterohemorrhagic Escherichia coli binds to platelets through TLR4 and CD62 and is detected on circulating platelets in patients with hemolytic uremic syndrome. Blood 108: 167–176. 16514062
48. te Loo DM, Heuvelink AE, de Boer E, Nauta J, van der Walle J, et al. (2001) Vero cytotoxin binding to polymorphonuclear leukocytes among households with children with hemolytic uremic syndrome. J Infect Dis 184: 446–450. 11471102
49. te Loo DM, van Hinsbergh VW, van den Heuvel LP, Monnens LA, (2001) Detection of verocytotoxin bound to circulating polymorphonuclear leukocytes of patients with hemolytic uremic syndrome. J Am Soc Nephrol 12: 800–806. 11274241
50. Brigotti M, Carnicelli D, Arfilli V, Tamassia N, Borsetti F, et al. (2013) Identification of TLR4 as the receptor that recognizes Shiga toxins in human neutrophils. J Immunol 191: 4748–4758. doi: 10.4049/jimmunol.1300122 24068665
51. Falguieres T, Mallard F, Baron C, Hanau D, Lingwood C, et al. (2001) Targeting of Shiga toxin B-subunit to retrograde transport route in association with detergent-resistant membranes. Mol Biol Cell 12: 2453–2468. 11514628
52. Morel O, Jesel L, Freyssinet JM, Toti F, (2011) Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 31: 15–26. doi: 10.1161/ATVBAHA.109.200956 21160064
53. Karmali MA, Petric M, Lim C, Fleming PC, Arbus GS, et al. (1985) The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis 151: 775–782. 3886804
54. Caprioli A, Luzzi I, Rosmini F, Pasquini P, Cirrincione R, et al. (1992) Hemolytic-uremic syndrome and Vero cytotoxin-producing Escherichia coli infection in Italy. The HUS Italian Study Group. J Infect Dis 166: 154–158. 1607689
55. Porubsky S, Federico G, Muthing J, Jennemann R, Gretz N, et al. (2014) Direct acute tubular damage contributes to Shiga toxin-mediated kidney failure. J Pathol 234: 120–133. doi: 10.1002/path.4388 24909663
56. Owens AP, 3rdMackman N, (2011) Microparticles in hemostasis and thrombosis. Circ Res 108: 1284–1297. doi: 10.1161/CIRCRESAHA.110.233056 21566224
57. Müller I, Klocke A, Alex M, Kotzsch M, Luther T, et al. (2003) Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 17: 476–478. 12514112
58. Galli M, Grassi A, Barbui T, (1996) Platelet-derived microvesicles in thrombotic thrombocytopenic purpura and hemolytic uremic syndrome. Thromb Haemost 75: 427–431. 8701402
59. Karpman D, Manea M, Vaziri-Sani F, Ståhl AL, Kristoffersson AC, (2006) Platelet activation in hemolytic uremic syndrome. Semin Thromb Hemost 32: 128–145. 16575688
60. Calderon Toledo C, Arvidsson I, Karpman D, (2011) Cross-reactive protection against enterohemorrhagic Escherichia coli infection by enteropathogenic E. coli in a mouse model. Infect Immun 79: 2224–2233. doi: 10.1128/IAI.01024-10 21402761
61. Gagnon M, Kheadr EE, Dabour N, Richard D, Fliss I, (2006) Effect of Bifidobacterium thermacidophilum probiotic feeding on enterohemorrhagic Escherichia coli O157:H7 infection in BALB/c mice. Int J Food Microbiol 111: 26–33. 16822570
62. Palermo M, Alves-Rosa F, Rubel C, Fernandez GC, Fernandez-Alonso G, et al. (2000) Pretreatment of mice with lipopolysaccharide (LPS) or IL-1beta exerts dose-dependent opposite effects on Shiga toxin-2 lethality. Clin Exp Immunol 119: 77–83. 10606967
63. Stirling JW, Graff PS, (1995) Antigen unmasking for immunoelectron microscopy: labeling is improved by treating with sodium ethoxide or sodium metaperiodate, then heating on retrieval medium. J Histochem Cytochem 43: 115–123. 7529784
64. Stone SM, Thorpe CM, Ahluwalia A, Rogers AB, Obata F, et al. (2012) Shiga toxin 2-induced intestinal pathology in infant rabbits is A-subunit dependent and responsive to the tyrosine kinase and potential ZAK inhibitor imatinib. Front Cell Infect Microbiol 135: 1–11.
65. Satchell SC, Tasman CH, Singh A, Ni L, Geelen J, et al. (2006) Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF. Kidney Int 69: 1633–1640. 16557232
66. Petric M, Karmali MA, Arbus GS, Roscoe M, Louie S, et al. (1987) Effects of cycloheximide and puromycin on cytotoxic activity of Escherichia coli verocytotoxin (Shiga-like toxin). J Clin Microbiol 25: 1265–1268. 3301891
67. Gentry MK, Dalrymple JM, (1980) Quantitative microtiter cytotoxicity assay for Shigella toxin. J Clin Microbiol 12: 361–366. 7012172