Human cytomegalovirus productively infects lymphatic endothelial cells and induces a secretome that promotes angiogenesis and lymphangiogenesis through interleukin-6 and granulocyte-macrophage colony-stimulating factor

Journal of General Virology

Volumn 92, Issue 3, 2011, Pages 650-660

  Fiorentini, Simona ^a   Luganini, Anna ^b   Dell'Oste, Valentina ^b   Lorusso, Bruno ^a   Cervi, Edoardo ^a   Caccuri, Francesca ^a   Bonardelli, Stefano ^a   Landolfo, Santo ^b   Caruso, Arnaldo ^a   Gribaudo, Giorgio ^b  

^a UNIVERSITY OF BRESCIA   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR; INTERLEUKIN 6;

ANGIOGENESIS; ARTICLE; CELL LOSS; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN TISSUE; INFLAMMATION; LYMPH NODE; LYMPHANGIOGENESIS; LYMPHOID TISSUE; NONHUMAN; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SUPERNATANT; VIRUS CULTURE; VIRUS INFECTION; VIRUS ISOLATION;

CELLS, CULTURED; CYTOMEGALOVIRUS; ENDOTHELIAL CELLS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERLEUKIN-6; LYMPHANGIOGENESIS; NEOVASCULARIZATION, PATHOLOGIC;

HUMAN HERPESVIRUS 5;

EID: 79951777800     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.025395-0     Document Type: Article

References (38)

1. Adler, B. & Sinzger, C. (2009). Endothelial cells in HCMV infection: one host cell out of many or a crucial target for virus spread? Thromb Haemost 102, 1057-1063.
2. Almeida, G. D., Porada, C. D., St Jeor, S. & Ascensao, J. L. (1994). Human cytomegalovirus alters interleukin-6 production by endothelial cells. Blood 83, 370-376. (Pubitemid 24030561)
3. Almeida-Porada, G., Porada, C. D., Shanley, J. D. & Ascensao, J. L. (1997). Altered production of GM-CSF and IL-8 in cytomegalovirus-infected, IL-1-primed umbilical cord endothelial cells. Exp Hematol 25, 1278-1285. (Pubitemid 27508876)
4. Bentz, G. L. & Yurochko, A. D. (2008). Human CMV infection of endothelial cells induces an angiogenic response through viral binding to EGF receptor and β1 and β3 integrins. Proc Natl Acad Sci U S A 105, 5531-5536. (Pubitemid 351753897)
5. Boriskin, Y. S., Moore, P., Murday, A. J., Booth, J. C. & Butcher, P. D. (1999). Human cytomegalovirus genome sequences in lymph nodes. Microbes Infect 1, 279-283.
6. Botto, S., Streblow, D. N., DeFilippis, V., White, L., Kreklywich, G. N., Smith, P. P. & Caposio, P. (2010). Il-6 in human cytomegalovirus secretome promotes angiogenesis and survival of endothelial cells through the stimulation of surviving. Blood 117, 352-361.
7. Britt, W. (2008). Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 325, 417-470.
8. Caposio, P., Riera, L., Hahn, G., Landolfo, S. & Gribaudo, G. (2004). Evidence that the human cytomegalovirus 46-kDa UL72 protein is not an active dUTPase but a late protein dispensable for replication in fibroblasts. Virology 325, 264-276. (Pubitemid 38902792)
9. Caposio, P., Musso, T., Luganini, A., Inoue, H., Gariglio, M., Landolfo, S. & Gribaudo, G. (2007a). Targeting the NF-κB pathway through pharmacological inhibition of IKK2 prevents human cytomegalovirus replication and virus-induced inflammatory response in infected endothelial cells. Antiviral Res 73, 175-184.
10. Caposio, P., Luganini, A., Hahn, G., Landolfo, S. & Gribaudo, G. (2007b). Activation of the virus-induced IKK/NF-κB signalling axis is critical for the replication of human cytomegalovirus in quiescent cells. Cell Microbiol 9, 2040-2054. (Pubitemid 47087094)
11. Carmeliet, P. (2003). Angiogenesis in health and disease. Nat Med 9, 653-660.
12. Caruso, A., Caselli, E., Fiorentini, S., Rotola, A., Prandini, A., Garrafa, E., Saba, E., Alessandri, G., Cassai, E. & Di Luca, D. (2009). U94 of human herpesvirus 6 inhibits in vitro angiogensis and lymphoangiogenesis. Proc Natl Acad Sci U S A 106, 20446-20451.
13. Chen, T. & Hudnall, S. D. (2006). Anatomical mapping of human herpesvirus reservoirs of infection. Mod Pathol 19, 726-737.
14. Cueni, L. N. & Detmar, M. (2008). The lymphatic system in health and disease. Lymphat Res Biol 6, 109-122.
15. Digel, M. & Sinzger, C. (2006). Determinant of endothelial cell tropism of human cytomegalovirus. In Cytomegaloviruses: Molecular Biology and Immunology, pp. 445-464. Edited by M. Reddehase. Norfolk: Caister Academic Press.
16. Dumortier, J., Streblow, D. N., Moses, A. V., Jacobs, J. M., Kreklywich, C. N., Camp, D., Smith, R. D., Orloff, S. L. & Nelson, J. A. (2008). Human cytomegalovirus secretome contains factors that induce angiogenesis and wound healing. J Virol 82, 6524-6535. (Pubitemid 351875129)
17. Garrafa, E., Trainini, L., Benetti, A., Saba, E., Fezzardi, L., Lorusso, B., Borghetti, P., Bottio, T., Ceri, E. & other authors (2005). Isolation, purification, and heterogeneity of human lymphatic endothelial cells from different tissues. Lymphology 38, 159-166. (Pubitemid 43165433)
18. Garrafa, E., Alessandri, G., Benetti, A., Turetta, D., Corradi, A., Cantoni, A. M., Cervi, E., Bonardelli, S., Parati, E. & other authors (2006). Isolation and characterization of lymphatic microvascular endothelial cells from human tonsils. J Cell Physiol 207, 107-113.
19. Hoshina, T., Kusuhara, K., Saito, M., Hara, T., Matsuura, S., Yano, T., Aoki, T. & Hara, T. (2009). Cytomegalovirus-associated protein-losing enteropathy resulting from lymphangiectasia in an immunocompetent child. Jpn J Infect Dis 62, 236-238.
20. Jarvis, M. A. & Nelson, J. A. (2007). Human cytomegalovirus tropism for endothelial cells: not all endothelial cells are created equal. J Virol 81, 2095-2101.
21. Ji, R. C. (2005). Characteristics of lymphatic endothelial cells in physiological and pathological conditions. Histol Histopathol 20, 155-175.
22. Kapetanos, D., Abuouda, H., Iodanidis, F., Katsinelos, P. & Kitis, G. (2010). Unique case of intestinal lymphangiectasia in an immunocompetent adult, caused by CMV and EBV co-infection. Ann Gastroenterol 23, 136-138.
23. Karlsen, T. V., Karkkainen, M. J., Alitalo, K. & Wiig, H. (2006). Transcapillary fluid balance consequences of missing initial lymphatics studied in a mouse model of primary lymphoedema. J Physiol 574, 583-596.
24. Krubasik, D., Eisenach, P. A., Kunz-Schughart, L. A., Murphy, G. & English, W. R. (2008). Granulocyte-macrophage colony stimulating factor induces endothelial capillary formation through induction of membrane-type 1 matrix metalloproteinase expression in vitro. Int J Cancer 122, 1261-1272. (Pubitemid 351287225)
25. Luo, M. H. & Fortunato, E. A. (2007). Long-term infection and shedding of human cytomegalovirus in T98G glioblastoma cells. J Virol 81, 10424-10436.
26. Mocarski, E. S., Jr, Shenk, T. & Pass, R. F. (2006). Cytomegaloviruses. In Fields Virology, 5th edn, pp. 2701-2772. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
27. Nakase, H., Itani, T., Mimura, J., Takeuchi, R., Kawasaki, T., Komori, H., Hashimoto, K. & Chiba, T. (1998). Transient protein-losing enteropathy associated with cytomegalovirus in a noncompromised host: a case report. Am J Gastroenterol 93, 1005-1006. (Pubitemid 29076998)
28. Podgrabinska, S., Braun, P., Velasco, P., Kloos, B., Pepper, M. S. & Skobe, M. (2002). Molecular characterization of lymphatic endothelial cells. Proc Natl Acad Sci U S A 99, 16069-16074. (Pubitemid 35462750)
29. Reinhardt, B., Schaarschmidt, P., Bossert, A., Luske, A., Finkenzeller, G., Mertens, T. & Michel, D. (2005). Upregulation of functionally active vascular endothelial growth factor by human cytomegalovirus. J Gen Virol 86, 23-30. (Pubitemid 40081147)
30. Revello, M. G. & Gerna, G. (2010). Human cytomegalovirus tropism for endothelial/epithelial cells: scientific background and clinical implications. Rev Med Virol 20, 136-155.
31. Revello, M. G., Baldanti, F., Percivalle, E., Sarasini, A., De-Giuli, L., Genini, E., Lilleri, D., Labò, N. & Gerna, G. (2001). In vitro selection of human cytomegalovirus variants unable to transfer virus and virus products from infected cells to polymorphonuclear leukocytes and to grow in endothelial cells. J Gen Virol 82, 1429-1438.
32. Ricotta, D., Alessandri, G., Pollara, C., Fiorentini, S., Favilli, F., Tosetti, M., Mantovani, A., Grassi, M., Garrafa, E. & other authors (2001). Adult human heart microvascular endothelial cells are permissive for non-lytic infection by human cytomegalovirus. Cardiovasc Res 49, 440-448. (Pubitemid 32119561)
33. Sinzger, C., Digel, M. & Jahn, G. (2008). Cytomegalovirus cell tropism. Curr Top Microbiol Immunol 325, 63-83.
34. Söderberg-Nauclér, C. (2006). Does cytomegalovirus play a causative role in the development of various inflammatory diseases and cancer? J Intern Med 259, 219-246.
35. Söderberg-Nauclér, C. (2008). HCMV microinfections in inflammatory diseases and cancer. J Clin Virol 41, 218-223.
36. Streblow, D. N., Durmontier, J., Moses, A. V., Orloff, S. L. & Nelson, J. A. (2008). Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325, 397-415.
37. Wuest, T. R. & Carr, D. J. J. (2010). VEGF-A expression by HSV-1-infected cells drives corneal lymphangiogenesis. J Exp Med 207, 101-115.
38. Yao, J. S., Zhai, W., Young, W. L. & Yang, G. Y. (2006). Interleukin-6 triggers human cerebral endothelial cells proliferation and migration: the role for KDR and MMP-9. Biochem Biophys Res Commun 342, 1396-1404.