Efficiency of porcine endothelial cell infection with human cytomegalovirus depends on both virus tropism and endothelial cell vascular origin

Xenotransplantation

Volumn 17, Issue 4, 2010, Pages 274-287

  Millard, Anne Laure ^a   Häberli, Lea ^a   Sinzger, Christian ^b   Ghielmetti, Maddalena ^a   Schneider, Mårten K J ^a   Bossart, Walter ^c   Seebach, Jörg D ^d   Mueller, Nicolas J ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d University of Zürich ^*  (Switzerland)

Author keywords

Cross species infection; Endothelial cells; Human cytomegalovirus; Transplantation; Xenotransplantation

Indexed keywords

ANIMAL CELL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CYTOMEGALOVIRUS INFECTION; CYTOPATHOLOGY; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SWINE; VIROGENESIS; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS STRAIN;

ANIMALS; ANTIGENS, VIRAL; AORTA; APOPTOSIS; CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; SWINE; TRANSPLANTATION, HETEROLOGOUS; TROPISM; VIRUS REPLICATION;

EID: 77955900381     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/j.1399-3089.2010.00594.x     Document Type: Article

References (48)

1. Davison AJ, Dolan A, Akter P et al. The human cytomegalovirus genome revisited: comparison with the chimpanzee cytomegalovirus genome (vol 84, pg 17, 2003). J Gen Virol 2003 84 : 1053.
2. Streblow DN, Orloff SL, Nelson JA. Acceleration of allograft failure by cytomegalovirus. Curr Opin Immunol 2007 19 : 577 582.
3. Rubin RH. The pathogenesis and clinical management of cytomegalovirus infection in the organ transplant recipient: the end of the 'silo hypothesis'. Curr Opin Infect Dis 2007 20 : 399 407.
4. Sprangers B, Waer M, Billiau AD. Xenotransplantation: where are we in 2008? Kidney Int 2008 74 : 14 21.
5. Perot K, Walker CM, Spaete RR. Primary chimpanzee skin fibroblast cells are fully permissive for human cytomegalovirus replication. J Gen Virol 1992 73 : 3281 3284.
6. Kim KS, Carp RI. Abortive infection of human diploid cells by murine cytomegalovirus. Infect Immun 1972 6 : 793 797.
7. Plachter B, Sinzger C, Jahn G. Cell types involved in replication and distribution of human cytomegalovirus. Adv Virus Res 1996 46 : 195 261.
8. Fioretti A, Furukawa T, Santoli D, Plotkin SA. Nonproductive infection of guinea-pig cells with human cytomegalovirus. J Virol 1973 11 : 998 1003.
9. Mocarski ES, Courcelle CT. Cytomegaloviruses and their replication. In : Knipe DM, Howley PM, eds. In Fields Virology, 4th edn. Philadelphia : Lippincott-Williams-Wilkins, 2001 : 2629 2673.
10. Degre M, Rannenberg-Nilsen T, Beck S, Rollag H, Fiane AE. Human cytomegalovirus productively infects porcine endothelial cells in vitro. Transplantation 2001 72 : 1334 1337.
11. Mocarski ES. Cytomegaloviruses and their replication. In : Fields BN, Knipe DM, Howley PM, eds. In Fields Virology, 3rd edn. New York : Lippincott-Raven, 1996 : 2447 2492.
12. Salvant BS, Fortunato EA, Spector DH. Cell cycle dysregulation by human cytomegalovirus: influence of the cell cycle phase at the time of infection and effects on cyclin transcription. J Virol 1998 72 : 3729 3741.
13. Pleskoff O, Casarosa P, Verneuil L et al. The human cytomegalovirus- encoded chemokine receptor US28 induces caspase-dependent apoptosis. FEBS J 2005 272 : 4163 4177.
14. Sedmak DD, Guglielmo AM, Knight DA, Birmingham DJ, Huang EH, Waldman WJ. Cytomegalovirus inhibits major histocompatibility class-Ii expression on infected endothelial-cells. Am J Pathol 1994 144 : 683 692.
15. Grundy JE, Lawson KM, MacCormac LP, Fletcher JM, Yong KL. Cytomegalovirus-infected endothelial cells recruit neutrophils by the secretion of C-X-C chemokines and transmit virus by direct neutrophil-endothelial cell contact and during neutrophil transendothelial migration. J Infect Dis 1998 177 : 1465 1474.
16. Fish KN, Soderberg-Naucler C, Mills LK, Stenglein S, Nelson JA. Human cytomegalovirus persistently infects aortic endothelial cells. J Virol 1998 72 : 5661 5668.
17. Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA. Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Hum Cytomegalovirus 2008 325 : 397 415.
18. Seebach JD, Schneider MKJ, Comrack CA et al. Immortalized bone-marrow derived pig endothelial cells. Xenotransplantation 2001 8 : 48 61.
19. Kolber-Simonds D, Lai LX, Watt SR et al. Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc Natl Acad Sci USA 2004 101 : 7335 7340.
20. Seebach JD, Yamada K, McMorrow IM, Sachs DH, DerSimonian H. Xenogeneic human anti-pig cytotoxicity mediated by activated natural killer cells. Xenotransplantation 1996 3 : 188 197.
21. Sinzger C, Kahl M, Laib K et al. Tropism of human cytomegalovirus for endothelial cells is determined by a post-entry step dependent on efficient translocation to the nucleus. J Gen Virol 2000 81 : 3021 3035.
22. Mahy BWJ, Kangro HO. Virology Methods Manual. London, UK : Academic Press Ltd, 1996.
23. Yun ZB, Lewensohn-Fuchs I, Ljungman P, Vahlne A. Real-time monitoring of cytomegalovirus infections after stem cell transplantation using the TaqMan polymerase chain reaction assays. Transplantation 2000 69 : 1733 1736.
24. Mueller NJ, Barth RN, Yamamoto S et al. Activation of cytomegalovirus in pig-to-primate organ xenotransplantation. J Virol 2002 76 : 4734 4740.
25. Lai LL, Britt WJ. The interaction between the major capsid protein and the smallest capsid protein of human cytomegalovirus is dependent on two linear sequences in the smallest capsid protein. J Virol 2003 77 : 2730 2735.
26. Sinzger C, Knapp J, Plachter B, Schmidt K, Jahn G. Quantification of replication of clinical cytomegalovirus isolates in cultured endothelial cells and fibroblasts by a focus expansion assay. J Virol Methods 1997 63 : 103 112.
27. Jarvis MA, Nelson JA. Human cytomegalovirus tropism for endothelial cells: not all endothelial cells are created equal. J Virol 2007 81 : 2095 2101.
28. Sinzger C. Entry route of HCMV into endothelial cells. J Clin Virol 2008 41 : 174 179.
29. MacCormac LP, Grundy JE. Two clinical isolates and the toledo strain of cytomegalovirus contain endothelial cell tropic variants that are not present in the AD169, Towne, or Davis strains. J Med Virol 1999 57 : 298 307.
30. Jurak I, Brune W. Induction of apoptosis limits cytomegalovirus cross-species infection. EMBO J 2006 25 : 2634 2642.
31. Sachs DH. The pig as a xenograft donor. Pathol Biol 1994 42 : 217 219.
32. Cooper DKC, Gollackner B, Sachs DH. Will the pig solve the transplantation backlog? Annu Rev Med 2002 53 : 133 147.
33. d'Apice AJ, Cowan PJ. Xenotransplantation: the next generation of engineered animals. Transpl Immunol 2009 21 : 111 115.
34. Griesche N, Zikos D, Witkowski P et al. Growth characteristics of human adenoviruses on porcine cell lines. Virology 2008 373 : 400 410.
35. Nishida K, Yamaguchi O, Otsu K. Crosstalk between autophagy and apoptosis in heart disease. Circ Res 2008 103 : 343 351.
36. Leuner K, Pantel J, Frey C et al. Enhanced apoptosis, oxidative stress and mitochondrial dysfunction in lymphocytes as potential biomarkers for Alzheimer's disease. J Neural Transm Suppl 2007 Suppl 72 207 215.
37. Mudter J, Neurath MF. Apoptosis of T cells and the control of inflammatory bowel disease: therapeutic implications. Gut 2007 56 : 293 303.
38. Castillo JP, Kowalik TF. HCMV infection: modulating the cell cycle and cell death. Int Rev Immunol 2004 23 : 113 139.
39. Arnoult D, Bartle LM, Skaletskaya A et al. Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. Proc Natl Acad Sci USA 2004 101 : 7988 7993.
40. Skaletskaya A, Bartle LM, Chittenden T, McCormick AL, Mocarski ES, Goldmacher VS. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc Natl Acad Sci USA 2001 98 : 7829 7834.
41. Sinzger C, Schmidt K, Knapp J et al. Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome. J Gen Virol 1999 80 : 2867 2877.
42. Slobbe-van Drunen MEP, Hendrickx ATM, Vossen RCRM, Speel EJM, Dam-Mieras MCE, Bruggeman CA. Nuclear import as a barrier to infection of human umbilical vein endothelial cells by human cytomegalovirus strain AD169. Virus Res 1998 56 : 149 156.
43. Dolan A, Cunningham C, Hector RD et al. Genetic content of wild-type human cytomegalovirus. J Gen Virol 2004 85 : 1301 1312.
44. Murphy E, Yu D, Grimwood J et al. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc Natl Acad Sci USA 2003 100 : 14976 14981.
45. Prichard MN, Penfold MET, Duke GM, Spaete RR, Kemble GW. A review of genetic differences between limited and extensively passaged human cytomegalovirus strains. Rev Med Virol 2001 11 : 191 200.
46. Cha TA, Tom E, Kemble GW, Duke GM, Mocarski ES, Spaete RR. Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J Virol 1996 70 : 78 83.
47. Kemble G, Duke G, Winter R, Spaete R. Defined large-scale alteration of the human cytomegalovirus genome constructed by cotransfection of overlapping cosmids. J Virol 1996 70 : 2044 2048.
48. Haught WH, Mansour M, Rothlein R et al. Alterations in circulating intercellular adhesion molecule-1 and L-selectin: further evidence for chronic inflammation in ischemic heart disease. Am Heart J 1996 132 : 1 8.