Mycoplasma suis infection results endothelial cell damage and activation: New insight into the cell tropism and pathogenicity of hemotrophic mycoplasma

Veterinary Research

Volumn 44, Issue 1, 2013, Pages

  Sokoli, Albina ^a,b   Groebel, Katrin ^b   Hoelzle, Katharina ^b   Amselgruber, Werner M ^a   Mateos, José M ^b   Schneider, Mårten K J ^c   Ziegler, Urs ^b   Felder, Kathrin M ^a   Hoelzle, Ludwig E ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; AORTA; BLOOD; ENDOTHELIUM CELL; ERYTHROCYTE; MICROBIOLOGY; MYCOPLASMA; MYCOPLASMOSIS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; SWINE; SWINE DISEASE; TRANSMISSION ELECTRON MICROSCOPY; TROPISM; VETERINARY; VIRULENCE; ANIMAL DISEASE; ARTICLE;

ANIMALS; AORTA; ENDOTHELIAL CELLS; ERYTHROCYTES; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MYCOPLASMA; MYCOPLASMA INFECTIONS; SUS SCROFA; SWINE; SWINE DISEASES; TROPISM; VIRULENCE;

EID: 84874103235     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/1297-9716-44-6     Document Type: Article

References (63)

1. Mycoplasma suis invades porcine erythrocytes. Groebel K, Hoelzle K, Wittenbrink MM, Ziegler U, Hoelzle LE, Infect Immun 2009 77 576 584 10.1128/IAI.00773-08 19015255
2. Haemotrophic mycoplasmas: recent advances in Mycoplasma suis. Hoelzle LE, Vet Microbiol 2008 130 215 226 10.1016/j.vetmic.2007.12.023 18358641
3. Hemotrophic mycoplasmas (hemoplasmas): a review and new insights into pathogenic potential. Messick JB, Vet Clin Pathol 2004 33 2 13 10.1111/j.1939-165X.2004.tb00342.x 15048620 (Pubitemid 38541516)
4. Hemoplasma infection in HIV-positive patient, Brazil. Dos Santos AP, Dos Santos RP, Biondo AW, Dora JM, Goldani LZ, De Oliveira ST, De Sa Guimaraes AM, Timenetsky J, De Morais HA, Gonzalez FH, Messick JB, Emerg Infect Dis 2008 14 1922 1924 10.3201/eid1412.080964 19046522
5. Human co-infection with Bartonella henselae and two hemotropic mycoplasma variants resembling Mycoplasma ovis. Sykes JE, Lindsay LL, Maggi RG, Breitschwerdt EB, J Clin Microbiol 2010 48 3782 3785 10.1128/JCM.01029-10 20702675
6. Prevalence of Mycoplasma suis (Eperythrozoon suis) infection in swine and swine-farm workers in Shanghai, China. Yuan CL, Liang AB, Yao CB, Yang ZB, Zhu JG, Cui L, Yu F, Zhu NY, Yang XW, Hua XG, Am J Vet Res 2009 70 890 894 10.2460/ajvr.70.7.890 19566474
7. A novel hemotropic Mycoplasma (hemoplasma) in a patient with hemolytic anemia and pyrexia. Steer JA, Tasker S, Barker EN, Jensen J, Mitchell J, Stocki T, Chalker VJ, Hamon M, Clin Infect Dis 2011 53 147 e151 10.1093/cid/cir666 22021921
8. Antibodies to actin in autoimmune haemolytic anaemia. Felder KM, Hoelzle K, Heinritzi K, Ritzmann M, Hoelzle LE, BMC Vet Res 2010 6 18 10.1186/1746-6148-6-18 20353574
9. Ictero-anemia, eperythrozoonosis, or anaplasmosis-like disease of swine proved to be caused by a filtrable virus. Foote LE, Brock WE, Gallaher B, North Am Vet 1951 32 17 23 14807044
10. Protozoan-like body in the blood of swine. Kinsley AT, Vet Med 1932 27 196
11. [A case of eperythrozoonosis suis and its differential diagnostic significance in relation to suspected swine fever]. Korn G, Mussgay M, Zentralbl Veterinarmed B 1968 15 617 630 in German 5693855
12. [Disseminated intravascular coagulation in eperythrozoonosis of swine]. Plank G, Heinritzi K, Berl Munch Tierarztl Wochenschr 1990 103 13 18 (in German) 2302156
13. Experimental porcine eperythrozoonosis: T-lymphocyte suppression and misdirected immune responses. Zachary JF, Smith AR, Am J Vet Res 1985 46 821 830 3874572
14. Hemotrophic mycoplasmas induce programmed cell death in red blood cells. Felder KM, Hoelzle K, Ritzmann M, Kilchling T, Schiele D, Heinritzi K, Groebel K, Hoelzle LE, Cell Physiol Biochem 2011 27 557 564 10.1159/000329957 21691073
15. Histology, immunohistochemistry, and ultrastructure of the verruga in Carrion's disease. Arias-Stella J, Lieberman PH, Erlandson RA, Arias-Stella J Jr, Am J Surg Pathol 1986 10 595 610 10.1097/00000478-198609000-00002 2428261 (Pubitemid 16011865)
16. Breaking the wall: targeting of the endothelium by pathogenic bacteria. Lemichez E, Lecuit M, Nassif X, Bourdoulous S, Nat Rev Microbiol 2010 8 93 104 20040916
17. Occlusion of brain capillaries by endothelial swelling in mycoplasma infections. Manuelidis EE, Thomas L, Proc Natl Acad Sci U S A 1973 70 706 709 10.1073/pnas.70.3.706 4514983
18. Pathogenetic mechanisms of Mycoplasma mycoides subsp. mycoides septicemia in goats. Rosendal S, Isr J Med Sci 1984 20 970 971 6511321 (Pubitemid 15175842)
19. Expression analysis of the T-cell-targeting chemokines CXCL9 and CXCL10 in mice and humans with endothelial infections caused by rickettsiae of the spotted fever group. Valbuena G, Bradford W, Walker DH, Am J Pathol 2003 163 1357 1369 10.1016/S0002-9440(10)63494-3 14507644 (Pubitemid 37175084)
20. Adherence of Mycoplasma mycoides subspecies mycoides to cultured endothelial cells. Valdivieso-Garcia A, Rosendal S, Serebrin S, Zentralbl Bakteriol 1989 272 210 215 10.1016/S0934-8840(89)80009-X 2698627 (Pubitemid 20131218)
21. [A contribution on splenectomy in swine]. Heinritzi K, Tierarztl Prax 1984 12 451 454 (in German) 6528324
22. Development of a diagnostic PCR assay based on novel DNA sequences for the detection of Mycoplasma suis (Eperythrozoon suis) in porcine blood. Hoelzle LE, Adelt D, Hoelzle K, Heinritzi K, Wittenbrink MM, Vet Microbiol 2003 93 185 196 10.1016/S0378-1135(03)00040-3 12695043 (Pubitemid 36416618)
23. Mycoplasma suis antigens recognized during humoral immune response in experimentally infected pigs. Hoelzle LE, Hoelzle K, Ritzmann M, Heinritzi K, Wittenbrink MM, Clin Vaccine Immunol 2006 13 116 122 10.1128/CVI.13.1.116-122. 2006 16426008
24. First LightCycler real-time PCR assay for the quantitative detection of Mycoplasma suis in clinical samples. Hoelzle LE, Helbling M, Hoelzle K, Ritzmann M, Heinritzi K, Wittenbrink MM, J Microbiol Methods 2007 70 346 354 10.1016/j.mimet.2007.05.009 17586075 (Pubitemid 47198141)
25. [Eperythrozoon infection in swine: effect on the acid-base balance and the glucose, lactate and pyruvate content of venous blood]. Heinritzi K, Peteranderl W, Plank G, Dtsch Tierarztl Wochenschr 1990 97 31 34 (in German) 2311527
26. Vaccination with the Mycoplasma suis recombinant adhesion protein MSG1 elicits a strong immune response but fails to induce protection in pigs. Hoelzle K, Doser S, Ritzmann M, Heinritzi K, Palzer A, Elicker S, Kramer M, Felder KM, Hoelzle LE, Vaccine 2009 27 5376 5382 10.1016/j.vaccine.2009.06.072 19596408
27. Immortalized bone-marrow derived pig endothelial cells. Seebach JD, Schneider MK, Comrack CA, LeGuern A, Kolb SA, Knolle PA, Germana S, DerSimonian H, LeGuern C, Sachs DH, Xenotransplantation 2001 8 48 61 10.1034/j.1399-3089. 2001.00075.x 11208191 (Pubitemid 32127075)
28. Lack of galactose-alpha-1,3-galactose expression on porcine endothelial cells prevents complement-induced lysis but not direct xenogeneic NK cytotoxicity. Baumann BC, Forte P, Hawley RJ, Rieben R, Schneider MK, Seebach JD, J Immunol 2004 172 6460 6467 15128838 (Pubitemid 38621256)
29. The surface-localised alpha-enolase of Mycoplasma suis is an adhesion protein. Schreiner SA, Sokoli A, Felder KM, Wittenbrink MM, Schwarzenbach S, Guhl B, Hoelzle K, Hoelzle LE, Vet Microbiol 2012 156 88 95 10.1016/j.vetmic. 2011.10.010 22047714
30. Pre-embedding Nanogold Silver and Gold Intensification. Yamamoto A, Masaki R, Methods Mol Biol 2010 657 225 235 10.1007/978-1-60761-783-9-18 20602220
31. First identification and functional characterization of an immunogenic protein in unculturable haemotrophic Mycoplasmas (Mycoplasma suis HspA1). Hoelzle LE, Hoelzle K, Harder A, Ritzmann M, Aupperle H, Schoon HA, Heinritzi K, Wittenbrink MM, FEMS Immunol Med Microbiol 2007 49 215 223 10.1111/j.1574-695X. 2006.00184.x 17328755
32. Transcriptional activation of vascular cell adhesion molecule-1 gene in vivo and its role in the pathophysiology of neutrophil-induced liver injury in murine endotoxin shock. Essani NA, Bajt ML, Farhood A, Vonderfecht SL, Jaeschke H, J Immunol 1997 158 5941 5948 9190948 (Pubitemid 127484003)
33. PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated beta-catenin. Ilan N, Mahooti S, Rimm DL, Madri JA, J Cell Sci 1999 112 3005 3014 10462517 (Pubitemid 29465719)
34. E-selectin and intercellular adhesion molecule-1 are released by activated human endothelial cells in vitro. Leeuwenberg JF, Smeets EF, Neefjes JJ, Shaffer MA, Cinek T, Jeunhomme TM, Ahern TJ, Buurman WA, Immunology 1992 77 543 549 1283598 (Pubitemid 23000475)
35. Endothelial cells derived from pigs lacking Gal alpha(1,3)Gal: no reduction of human leukocyte adhesion and natural killer cell cytotoxicity. Baumann BC, Schneider MK, Lilienfeld BG, Antsiferova MA, Rhyner DM, Hawley RJ, Seebach JD, Transplantation 2005 79 1067 1072 10.1097/01.TP.0000157231.11083.7C 15880045 (Pubitemid 40663999)
36. Rolling adhesion of human NK cells to porcine endothelial cells mainly relies on CD49d-CD106 interactions. Schneider MK, Strasser M, Gilli UO, Kocher M, Moser R, Seebach JD, Transplantation 2002 73 789 796 10.1097/00007890- 200203150-00023 11907429 (Pubitemid 34260579)
37. Bartonella interactions with endothelial cells and erythrocytes. Dehio C, Trends Microbiol 2001 9 279 285 10.1016/S0966-842X(01)02047-9 11390243 (Pubitemid 32522808)
38. Beta-thalassaemia and sickle cell anaemia as paradigms of hypercoagulability. Ataga KI, Cappellini MD, Rachmilewitz EA, Br J Haematol 2007 139 3 13 10.1111/j.1365-2141.2007.06740.x 17854302 (Pubitemid 47389919)
39. Hypercoagulability in sickle cell disease: new approaches to an old problem. Ataga KI, Key NS, Hematology Am Soc Hematol Educ Program 2007 2007 91 96 10.1182/asheducation-2007.1.91
40. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA, Am J Pathol 1985 119 385 401 3893148 (Pubitemid 15051887)
41. Enhanced adherence of sickle erythrocytes to thrombin-treated endothelial cells involves interendothelial cell gap formation. Manodori AB, Matsui NM, Chen JY, Embury SH, Blood 1998 92 3445 3454 9787186 (Pubitemid 28492357)
42. Plasmodium falciparum-infected erythrocytes increase intercellular adhesion molecule 1 expression on brain endothelium through NF-kappaB. Tripathi AK, Sullivan DJ, Stins MF, Infect Immun 2006 74 3262 3270 10.1128/IAI.01625-05 16714553 (Pubitemid 43794513)
43. Fibrin activation of vascular endothelial cells. Induction of IL-8 expression. Qi J, Kreutzer DL, J Immunol 1995 155 867 876 7608564
44. A 130-kDa protein on endothelial cells binds to amino acids 15-42 of the B beta chain of fibrinogen. Erban JK, Wagner DD, J Biol Chem 1992 267 2451 2458 1370821
45. Fibrin structure and wound healing. Laurens N, Koolwijk P, De Maat MP, J Thromb Haemost 2006 4 932 939 10.1111/j.1538-7836.2006.01861.x 16689737
46. In vitro studies of erythrocyte-vascular endothelium interactions. Shiu YT, McIntire LV, Ann Biomed Eng 2003 31 1299 1313 14758921
47. Fibrinogen, a modulator of erythrocyte adhesion to vascular endothelium. Wautier JL, Pintigny D, Wautier MP, Paton RC, Galacteros F, Passa P, Caen JP, J Lab Clin Med 1983 101 911 920 6854127 (Pubitemid 13100686)
48. Biofilm formation by mycoplasma species and its role in environmental persistence and survival. McAuliffe L, Ellis RJ, Miles K, Ayling RD, Nicholas RA, Microbiology 2006 152 913 922 10.1099/mic.0.28604-0 16549656
49. Mycoplasma corogypsi sp. nov., a new species from the footpad abscess of a black vulture, Coragyps atratus. Panangala VS, Stringfellow JS, Dybvig K, Woodard A, Sun F, Rose DL, Gresham MM, Int J Syst Bacteriol 1993 43 585 590 10.1099/00207713-43-3-585 8347515 (Pubitemid 23210441)
50. Erythrocyte membrane alterations associated with the attachment and replication of Eperythrozoon suis: a light and electron microscopic study. Zachary JF, Basgall EJ, Vet Pathol 1985 22 164 170 3984160
51. Eperythrozoon suis in naturally infected pigs: a light and electron microscopic study. Pospischil A, Hoffmann R, Vet Pathol 1982 19 651 657 10.1177/030098588201900609 7147624 (Pubitemid 13178677)
52. Fibrils as extracellular appendages of bacteria: their role in contact-mediated cell-cell interactions in Myxococcus xanthus. Dworkin M, Bioessays 1999 21 590 595 10.1002/(SICI)1521-1878(199907)21:7<590::AID- BIES7>3.0.CO;2-E 10472185 (Pubitemid 29337597)
53. MSG1, a surface-localised protein of Mycoplasma suis is involved in the adhesion to erythrocytes. Hoelzle LE, Hoelzle K, Helbling M, Aupperle H, Schoon HA, Ritzmann M, Heinritzi K, Felder KM, Wittenbrink MM, Microbes Infect 2007 9 466 474 10.1016/j.micinf.2007.01.004 17336568 (Pubitemid 46436545)
54. Two mammalian cell internalization strategies used by pathogenic bacteria. Isberg RR, Van Nhieu GT, Annu Rev Genet 1994 28 395 422 10.1146/annurev.ge.28.120194.002143 7893133
55. Internalin must be on the bacterial surface to mediate entry of Listeria monocytogenes into epithelial cells. Lebrun M, Mengaud J, Ohayon H, Nato F, Cossart P, Mol Microbiol 1996 21 579 592 10.1111/j.1365-2958.1996.tb02566.x 8866480 (Pubitemid 26323780)
56. Complete genome sequence of the hemotrophic Mycoplasma suis strain KI3806. Oehlerking J, Kube M, Felder KM, Matter D, Wittenbrink MM, Schwarzenbach S, Kramer MM, Hoelzle K, Hoelzle LE, J Bacteriol 2011 193 2369 2370 10.1128/JB.00187-11 21398558
57. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Ley K, Laudanna C, Cybulsky MI, Nourshargh S, Nat Rev Immunol 2007 7 678 689 10.1038/nri2156 17717539 (Pubitemid 47327397)
58. Markers of endothelial damage in organ dysfunction and sepsis. Reinhart K, Bayer O, Brunkhorst F, Meisner M, Crit Care Med 2002 30 302 S312 10.1097/00003246-200205001-00021 12004252
59. Locomotion of monocytes on endothelium is a critical step during extravasation. Schenkel AR, Mamdouh Z, Muller WA, Nat Immunol 2004 5 393 400 10.1038/ni1051 15021878 (Pubitemid 38500088)
60. The structure of the two amino-terminal domains of human ICAM-1 suggests how it functions as a rhinovirus receptor and as an LFA-1 integrin ligand. Bella J, Kolatkar PR, Marlor CW, Greve JM, Rossmann MG, Proc Natl Acad Sci U S A 1998 95 4140 4145 10.1073/pnas.95.8.4140 9539703 (Pubitemid 28207878)
61. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Brown S, Heinisch I, Ross E, Shaw K, Buckley CD, Savill J, Nature 2002 418 200 203 10.1038/nature00811 12110892 (Pubitemid 34773776)
62. CD31 delays phagocyte membrane repolarization to promote efficient binding of apoptotic cells. Vernon-Wilson EF, Aurade F, Tian L, Rowe IC, Shipston MJ, Savill J, Brown SB, J Leukoc Biol 2007 82 1278 1288 10.1189/jlb.0507283 17684043 (Pubitemid 350133526)
63. Mechanisms of leukocyte transendothelial migration. Muller WA, Annu Rev Pathol 2011 6 323 344 10.1146/annurev-pathol-011110-130224 21073340