Besnoitia besnoiti infections activate primary bovine endothelial cells and promote PMN adhesion and NET formation under physiological flow condition

Parasitology Research

Volumn 115, Issue 5, 2016, Pages 1991-2001

  Maksimov, P ^a,b   Hermosilla, C ^a   Kleinertz, S ^a,c   Hirzmann, J ^a   Taubert, A ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Adhesion molecules; Chemokines; Coccidia; NET formation; PMN adhesion

Indexed keywords

CELL ADHESION MOLECULE; CHEMOKINE; CXCL1 CHEMOKINE; CYCLOOXYGENASE 2; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; PADGEM PROTEIN; RANTES;

ANIMAL CELL; ARTICLE; BESNOITIA BESNOITI; BESNOITIOSIS; BOVINE; CELL ADHESION; CELL INTERACTION; CELLULAR IMMUNITY; COCCIDIA; CONTROLLED STUDY; EXTRACELLULAR TRAP; FLOW CYTOMETRY; GENE EXPRESSION; GENE FUNCTION; IN VITRO STUDY; INNATE IMMUNITY; NONHUMAN; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; RECEPTOR UPREGULATION; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; CATTLE DISEASE; COCCIDIOSIS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MONONUCLEAR CELL; NEUTROPHIL; PARASITOLOGY; PHYSIOLOGY; SARCOCYSTIDAE; UPREGULATION; VETERINARY;

ANIMALS; CATTLE; CATTLE DISEASES; CELL ADHESION; CELL ADHESION MOLECULES; COCCIDIOSIS; ENDOTHELIAL CELLS; EXTRACELLULAR TRAPS; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; LEUKOCYTES, MONONUCLEAR; NEUTROPHILS; P-SELECTIN; SARCOCYSTIDAE; UP-REGULATION;

EID: 84957578895     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-016-4941-5     Document Type: Article

References (80)

1. Abi Abdallah DS, Lin C, Ball CJ, King MR, Duhamel GE, Denkers EY (2012) Toxoplasma gondii triggers release of human and mouse neutrophil extracellular traps. Infect Immun 80:768–777
2. Akira S, Hirano T, Taga T, Kishimoto T (1990) Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J 4:2860–2867
3. Alvarez-Garcia G, Frey CF, Mora LM, Schares G (2013) A century of bovine besnoitiosis: an unknown disease re-emerging in Europe. Trends Parasitol 29:407–415
4. Alvarez-Garcia G, Garcia-Lunar P, Gutierrez-Exposito D, Shkap V, Ortega-Mora LM (2014) Dynamics of Besnoitia besnoiti infection in cattle. Parasitology 141:1419–1435
5. Baker VS, Imade GE, Molta NB, Tawde P, Pam SD, Obadofin MO, Sagay SA, Egah DZ, Iya D, Afolabi BB, Baker M, Ford K, Ford R, Roux KH, Keller TC III (2008) Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malar J 7:41
6. Basso W, Schares G, Gollnick NS, Rutten M, Deplazes P (2011) Exploring the life cycle of Besnoitia besnoiti—experimental infection of putative definitive and intermediate host species. Vet Parasitol 178:223–234
7. Basso W, Lesser M, Grimm F, Hilbe M, Sydler T, Trosch L, Ochs H, Braun U, Deplazes P (2013) Bovine besnoitiosis in Switzerland: imported cases and local transmission. Vet Parasitol 198:265–273
8. Behrendt JH, Hermosilla C, Hardt M, Failing K, Zahner H, Taubert A (2008) PMN-mediated immune reactions against Eimeria bovis. Vet Parasitol 151:97–109
9. Behrendt JH, Ruiz A, Zahner H, Taubert A, Hermosilla C (2010) Neutrophil extracellular trap formation as innate immune reactions against the apicomplexan parasite Eimeria bovis. Vet Immunol Immunopathol 133:1–8
10. Bigalke RD (1968) New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. Onderstepoort J Vet Res 35:3–137
11. Bischoff J, Brasel C (1995) Regulation of P-selectin by tumor necrosis factor-alpha. Biochem Biophys Res Commun 210:174–180
12. Bonfanti R, Furie BC, Furie B, Wagner DD (1989) PADGEM (GMP140) is a component of Weibel-Palade bodies of human endothelial cells. Blood 73:1109–1112
13. Branzk N, Papayannopoulos V (2013) Molecular mechanisms regulating NETosis in infection and disease. Semin Immunopathol 35:513–530
14. Brinkmann V, Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198:773–783
15. Carmona-Rivera C, Zhao W, Yalavarthi S, Kaplan MJ (2015) Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2. Ann Rheum Dis 74:1417–1424
16. Cedervall J, Zhang Y, Huang H, Zhang L, Femel J, Dimberg A, Olsson AK (2015) Neutrophil extracellular traps accumulate in peripheral blood vessels and compromise organ function in tumor-bearing animals. Cancer Res 75:2653–2662
17. Cortes HC, Reis Y, Gottstein B, Hemphill A, Leitao A, Muller N (2007) Application of conventional and real-time fluorescent ITS1 rDNA PCR for detection of Besnoitia besnoiti infections in bovine skin biopsies. Vet Parasitol 146:352–356
18. Cortes H, Leitao A, Gottstein B, Hemphill A (2014) A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges,). Parasitology 141:1406–1417
19. D’Haese J, Mehlhorn H, Peters W (1977) Comparative electron microscope study of pellicular structures in coccidia (Sarcocystis, Besnoitia and Eimeria). Int J Parasitol 7:505–518
20. Deckert-Schlüter M, Schlüter D, Hof H, Wiestler OD, Lassmann H (1994) Differential expression of ICAM-1, VCAM-1 and their ligands LFA-1, Mac-1, CD43, VLA-4, and MHC class II antigens in murine Toxoplasma encephalitis: a light microscopic and ultrastructural immunohistochemical study. J Neuropathol Exp Neurol 53:457–468
21. Delemarre FG, Stevenhagen A, Van FR (1995) Granulocyte-macrophage colony-stimulating factor (GM-CSF) reduces toxoplasmastatic activity of human monocytes via induction of prostaglandin E2 (PGE2). Clin Exp Immunol 102:425–429
22. Diesing L, Heydorn AO, Matuschka FR, Bauer C, Pipano E, de Waal DT, Potgieter FT (1988) Besnoitia besnoiti: studies on the definitive host and experimental infections in cattle. Parasitol Res 75:114–117
23. Dubey JP, Shkap V, Pipano E, Fish L, Fritz DL (2003) Ultrastructure of Besnoitia besnoiti tissue cysts and bradyzoites. J Eukaryot Microbiol 50:240–244
24. Ebnet K, Vestweber D (1999) Molecular mechanisms that control leukocyte extravasation: the selectins and the chemokines. Histochem Cell Biol 112:1–23
25. Etulain J, Martinod K, Wong SL, Cifuni SM, Schattner M, Wagner DD (2015) P-selectin promotes neutrophil extracellular trap formation in mice. Blood 126:242–246
26. European Food Safety Authority (2010) Bovine besnoitiosis: an emerging disease in Europe. EFSA Journal 8:1499
27. Fernandez-Garcia A, Risco-Castillo V, Pedraza-Diaz S, Guado-Martinez A, Varez-Garcia G, Gomez-Bautista M, Collantes-Fernandez E, Ortega-Mora LM (2009) First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. J Parasitol 95:474–476
28. Fischer HG, Nitzgen B, Reichmann G, Hadding U (1997) Cytokine responses induced by Toxoplasma gondii in astrocytes and microglial cells. Eur J Immunol 27:1539–1548
29. Gentile A, Militerno G, Schares G, Nanni A, Testoni S, Bassi P, Gollnick NS (2011) Evidence for bovine besnoitiosis being endemic in Italy—first in vitro isolation of Besnoitia besnoiti from cattle born in Italy. Vet Parasitol
30. Gollnick NS, Gentile A, Schares G (2010) Diagnosis of bovine besnoitiosis in a bull born in Italy. Vet Rec 166:599
31. Gollnick NS, Scharr JC, Schares G, Langenmayer MC (2015) Natural Besnoitia besnoiti infections in cattle: chronology of disease progression. BMC Vet Res 11:35
32. Gupta AK, Joshi MB, Philippova M, Erne P, Hasler P, Hahn S, Resink TJ (2010) Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett 584:3193–3197
33. Hermosilla C, Zahner H, Taubert A (2006) Eimeria bovis modulates adhesion molecule gene transcription in and PMN adhesion to infected bovine endothelial cells. Int J Parasitol 36:423–431
34. Hermosilla C, Caro TM, Silva LM, Ruiz A, Taubert A (2014) The intriguing host innate immune response: novel anti-parasitic defence by neutrophil extracellular traps. Parasitology 141:1489–1498
35. Heydorn AO, Senaud J, Mehlhorn H, Heinonen R (1984) Besnoitia sp. from goats in Kenya. Z Parasitenkd 70:709–713
36. Hornok S, Fedak A, Baska F, Hofmann-Lehmann R, Basso W (2014) Bovine besnoitiosis emerging in Central-Eastern Europe, Hungary. Parasit Vectors 7:20
37. Jaffe EA, Nachman RL, Becker CG, Minick CR (1973) Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 52:2745–2756
38. Kaplan MJ, Radic M (2012) Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 189:2689–2695
39. Knight BC, Brunton CL, Modi NC, Wallace GR, Stanford MR (2005) The effect of Toxoplasma gondii infection on expression of chemokines by rat retinal vascular endothelial cells. J Neuroimmunol 160:41–47
40. Lachenmaier SM, Deli MA, Meissner M, Liesenfeld O (2011) Intracellular transport of Toxoplasma gondii through the blood-brain barrier. J Neuroimmunol 232:119–130
41. Lawrence MB, Springer TA (1991) Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65:859–873
42. Leutenegger CM, Alluwaimi AM, Smith WL, Perani L, Cullor JS (2000) Quantitation of bovine cytokine mRNA in milk cells of healthy cattle by real-time TaqMan polymerase chain reaction. Vet Immunol Immunopathol 77:275–287
43. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-delta-delta-CT method. Methods 25:402–408
44. Locati M, Otero K, Schioppa T, Signorelli P, Perrier P, Baviera S, Sozzani S, Mantovani A (2002) The chemokine system: tuning and shaping by regulation of receptor expression and coupling in polarized responses. Allergy 57:972–982
45. Marki A, Esko JD, Pries AR, Ley K (2015) Role of the endothelial surface layer in neutrophil recruitment. J Leukoc Biol 98:503–515
46. McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF (1989) GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest 84:92–99
47. Mehlhorn H, Klimpel S, Schein E, Heydorn AO, Al-Quraishy S, Selmair J (2009) Another African disease in Central Europa: besnoitiosis of cattle. I. Light and electron microscopical study. Parasitol Res 104:861–868
48. Munoz-Caro T, Hermosilla C, Silva LM, Cortes H, Taubert A (2014a) Neutrophil extracellular traps as innate immune reaction against the emerging apicomplexan parasite Besnoitia besnoiti. PLoS One 9:e91415
49. Munoz-Caro T, Silva LM, Ritter C, Taubert A, Hermosilla C (2014b) Besnoitia besnoiti tachyzoites induce monocyte extracellular trap formation. Parasitol Res 113:4189–4197
50. Munoz-Caro T, Lendner M, Daugschies A, Hermosilla C, Taubert A (2015a) NADPH oxidase, MPO, NE, ERK1/2, p38 MAPK and Ca2+ influx are essential for Cryptosporidium parvum-induced NET formation. Dev Comp Immunol 52:245–254
51. Munoz-Caro T, Mena Huertas SJ, Conejeros I, Alarcon P, Hidalgo MA, Burgos RA, Hermosilla C, Taubert A (2015b) Eimeria bovis-triggered neutrophil extracellular trap formation is CD11b-, ERK 1/2-, p38 MAP kinase- and SOCE-dependent. Vet Res 46:23
52. Nagineni CN, Detrick B, Hooks JJ (2000) Toxoplasma gondii infection induces gene expression and secretion of interleukin 1 (IL-1), IL-6, granulocyte-macrophage colony-stimulating factor, and intercellular adhesion molecule 1 by human retinal pigment epithelial cells. Infect Immun 68:407–410
53. Njenga JM, Bwangamoi O, Kangethe EK, Mugera GM, Mutiga ER (1995) Comparative ultrastructural studies on Besnoitia besnoiti and Besnoitia caprae. Vet Res Commun 19:295–308
54. Olias P, Schade B, Mehlhorn H (2011) Molecular pathology, taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae). Infect Genet Evol 11:1564–1576
55. Pate M, Damarla V, Chi DS, Negi S, Krishnaswamy G (2010) Endothelial cell biology: role in the inflammatory response. Adv Clin Chem 52:109–130
56. Perez D, Ruiz A, Munoz MC, Molina JM, Hermosilla C, Lopez AM, Matos L, Ortega L, Martin S, Taubert A (2015) Modulation of the pro-inflammatory molecules E-selectin and TNF-alpha gene transcription in Eimeria ninakohlyakimovae-infected primary caprine host endothelial cells. Parasitol Int 64:471–477
57. Phipps RP, Stein SH, Roper RL (1991) A new view of prostaglandin E regulation of the immune response. Immunol Today 12:349–352
58. Raza A, Ghanchi NK, Sarwar ZA, Raheem A, Nizami S, Beg MA (2013) Tumor necrosis factor-alpha, interleukin-10, intercellular and vascular adhesion molecules are possible biomarkers of disease severity in complicated Plasmodium vivax isolates from Pakistan. PLoS One 8:e81363
59. Reichel M, Munoz-Caro T, Sanchez CG, Rubio GA, Magdowski G, Gartner U, Taubert A, Hermosilla C (2015) Harbour seal (Phoca vitulina) PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gondii. Dev Comp Immunol 50:106–115
60. Schares G, Basso W, Majzoub M, Cortes HC, Rostaher A, Selmair J, Hermanns W, Conraths FJ, Gollnick NS (2009) First in vitro isolation of Besnoitia besnoiti from chronically infected cattle in Germany. Vet Parasitol 163:315–322
61. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108
62. Scholtyseck E, Mehlhorn H, Muller BE (1973) Identification of merozoites of 4 cyst-forming Coccidia (Sarcocystis, Toxoplasma, Besnoitia, Frenkelia) by means of electron microscopy. Z Parasitenkd 42:185–206
63. Silva NM, Manzan RM, Carneiro WP, Milanezi CM, Silva JS, Ferro EA, Mineo JR (2010) Toxoplasma gondii: the severity of toxoplasmic encephalitis in C57BL/6 mice is associated with increased ALCAM and VCAM-1 expression in the central nervous system and higher blood-brain barrier permeability. Exp Parasitol 126:167–177
64. Silva LM, Munoz-Caro T, Gerstberger R, Vila-Vicosa MJ, Cortes HC, Hermosilla C, Taubert A (2014) The apicomplexan parasite Eimeria arloingi induces caprine neutrophil extracellular traps. Parasitol Res 113:2797–2807
65. Silva LM, Vila-Vicosa MJ, Cortes HC, Taubert A, Hermosilla C (2015) Suitable in vitro Eimeria arloingi macromeront formation in host endothelial cells and modulation of adhesion molecule, cytokine and chemokine gene transcription. Parasitol Res 114:113–124
66. Stein JV, Nombela-Arrieta C (2005) Chemokine control of lymphocyte trafficking: a general overview. Immunology 116:1–12
67. Suzuki Y, Sa Q, Gehman M, Ochiai E (2011) Interferon-gamma- and perforin-mediated immune responses for resistance against Toxoplasma gondii in the brain. Expert Rev Mol Med 13:e31
68. Tanaka K, Koike Y, Shimura T, Okigami M, Ide S, Toiyama Y, Okugawa Y, Inoue Y, Araki T, Uchida K, Mohri Y, Mizoguchi A, Kusunoki M (2014) In vivo characterization of neutrophil extracellular traps in various organs of a murine sepsis model. PLoS One 9, e111888
69. Taubert A, Hermosilla C (2008) Bovine recombinant IFNgamma induces endothelial cell gene transcription of immunoregulatory molecules and upregulates PMN and PBMC adhesion on bovine endothelial cells. Vet Res Commun 32:35–47
70. Taubert A, Krüll M, Zahner H, Hermosilla C (2006a) Toxoplasma gondii and Neospora caninum infections of bovine endothelial cells induce endothelial adhesion molecule gene transcription and subsequent PMN adhesion. Vet Immunol Immunopathol 112:272–283
71. Taubert A, Zahner H, Hermosilla C (2006b) Dynamics of transcription of immunomodulatory genes in endothelial cells infected with different coccidian parasites. Vet Parasitol 142:214–222
72. Taubert A, Wimmers K, Ponsuksili S, Jimenez CA, Zahner H, Hermosilla C (2010) Microarray-based transcriptional profiling of Eimeria bovis-infected bovine endothelial host cells. Vet Res 41:70
73. Tomasik J, Schultz TL, Kluge W, Yolken RH, Bahn S, Carruthers VB (2015) Shared immune and repair markers during experimental Toxoplasma chronic brain infection and schizophrenia. Schizophr Bull
74. Vorobjeva NV, Pinegin BV (2014) Neutrophil extracellular traps: mechanisms of formation and role in health and disease. Biochemistry (Mosc) 79:1286–1296
75. Wagner JG, Roth RA (2000) Neutrophil migration mechanisms, with an emphasis on the pulmonary vasculature. Pharmacol Rev 52:349–374
76. Wang X, Michie SA, Xu B, Suzuki Y (2007) Importance of IFN-gamma-mediated expression of endothelial VCAM-1 on recruitment of CD8+ T cells into the brain during chronic infection with Toxoplasma gondii. J Interferon Cytokine Res 27:329–338
77. Yuan JS, Reed A, Chen F, Stewart CN Jr (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7:85
78. Zawrotniak M, Rapala-Kozik M (2013) Neutrophil extracellular traps (NETs)—formation and implications. Acta Biochim Pol 60:277–284
79. Zhang J, Rivest S (2001) Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J Neurochem 76:855–864
80. Zlotnik A, Yoshie O (2000) Chemokines: a new classification system and their role in immunity. Immunity 12:121–127