Acute hantavirus infection induces galectin-3-binding protein

Journal of General Virology

Volumn 95, Issue , 2014, Pages 2356-2364

  Hepojoki, Jussi ^a   Strandin, Tomas ^a   Hetzel, Udo ^b   Sironen, Tarja ^a   Klingström, Jonas ^c   Sane, Jussi ^a   Mäkelä, Satu ^d,e   Mustonen, Jukka ^d,e   Meri, Seppo ^a   Lundkvist, Åke ^f   Vapalahti, Olli ^a,b,g   Lankinen, Hilkka ^a   Vaheri, Antti ^a,g  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

^e TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^f SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^g HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C4; COMPLEMENT MEMBRANE ATTACK COMPLEX; CREATININE; GALECTIN 3 BINDING PROTEIN; GLYCOPROTEIN; IMMUNOGLOBULIN M; INTERLEUKIN 10; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS ANTIGEN; CARRIER PROTEIN; GALECTIN 3; LGALS3BP PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR MARKER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; HANTAVIRUS; HANTAVIRUS INFECTION; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MACACA; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SECRETION; UPREGULATION; VERO CELL LINE; ACUTE DISEASE; ANIMAL; BIOSYNTHESIS; BLOOD; CHLOROCEBUS AETHIOPS; FEMALE; IMMUNOLOGY; MACACA FASCICULARIS; MALE; METABOLISM; PUUMALA VIRUS; TISSUE DISTRIBUTION; UMBILICAL VEIN ENDOTHELIAL CELL; VIROLOGY;

ACUTE DISEASE; ANIMALS; ANTIGENS, NEOPLASM; ANTIGENS, VIRAL; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; COMPLEMENT ACTIVATION; FEMALE; GALECTIN 3; GLYCOPROTEINS; HANTAVIRUS INFECTIONS; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MACACA FASCICULARIS; MALE; PUUMALA VIRUS; TISSUE DISTRIBUTION; TUMOR MARKERS, BIOLOGICAL; VERO CELLS;

EID: 84908270467     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.066837-0     Document Type: Article

References (44)

1. Artini, M., Natoli, C., Tinari, N., Costanzo, A., Marinelli, R., Balsano, C., Porcari, P., Angelucci, D., D’Egidio, M. & other authors (1996). Elevated serum levels of 90K/MAC-2 BP predict unresponsiveness to a-interferon therapy in chronic HCV hepatitis patients. J Hepatol 25, 212–217.
2. Björkström, N. K., Lindgren, T., Stoltz, M., Fauriat, C., Braun, M., Evander, M., Michaëlsson, J., Malmberg, K. J., Klingström, J. & other authors (2011). Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 208, 13–21.
3. Borges, A. A., Campos, G. M., Moreli, M. L., Souza, R. L., Aquino, V. H., Saggioro, F. P. & Figueiredo, L. T. (2006). Hantavirus cardiopulmonary syndrome: immune response and pathogenesis. Microbes Infect 8, 2324–2330.
4. Darcissac, E. C., Vidal, V., De La Tribonniere, X., Mouton, Y. & Bahr, G. M. (2001). Variations in serum IL-7 and 90K/Mac-2 binding protein (Mac-2 BP) levels analysed in cohorts of HIV-1 patients and correlated with clinical changes following antiretroviral therapy. Clin Exp Immunol 126, 287–294.
5. Denard, J., Beley, C., Kotin, R., Lai-Kuen, R., Blot, S., Leh, H., Asokan, A., Samulski, R. J., Moullier, P. & other authors (2012). Human galectin 3 binding protein interacts with recombinant adenoassociated virus type 6. J Virol 86, 6620–6631.
6. Gavrilovskaya, I., Gorbunova, E., Koster, F. & Mackow, E. (2012). Elevated VEGF levels in pulmonary edema fluid and PBMCs from patients with acute hantavirus pulmonary syndrome. Adv Virol 2012, 674360.
7. Geimonen, E., Neff, S., Raymond, T., Kocer, S. S., Gavrilovskaya, I. N. & Mackow, E. R. (2002). Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc Natl Acad Sci U S A 99, 13837–13842.
8. Gorbunova, E., Gavrilovskaya, I. N. & Mackow, E. R. (2010). Pathogenic hantaviruses Andes virus and Hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cells. J Virol 84, 7405–7411.
9. Grassadonia, A., Tinari, N., Iurisci, I., Piccolo, E., Cumashi, A., Innominato, P., D’Egidio, M., Natoli, C., Piantelli, M. & Iacobelli, S. (2002). 90K (Mac-2 BP) and galectins in tumor progression and metastasis. Glycoconj J 19, 551–556.
10. Gröschel, B., Braner, J. J., Funk, M., Linde, R., Doerr, H. W., Cinatl, J., Jr & Iacobelli, S. (2000). Elevated plasma levels of 90K (Mac-2 BP) immunostimulatory glycoprotein in HIV-1-infected children. J Clin Immunol 20, 117–122.
11. Hepojoki, J., Strandin, T., Vaheri, A. & Lankinen, H. (2010a). Interactions and oligomerization of hantavirus glycoproteins. J Virol 84, 227–242.
12. Hepojoki, J., Strandin, T., Wang, H., Vapalahti, O., Vaheri, A. & Lankinen, H. (2010b). Cytoplasmic tails of hantavirus glycoproteins interact with the nucleocapsid protein. J Gen Virol 91, 2341–2350.
13. Huiskonen, J. T., Hepojoki, J., Laurinmäki, P., Vaheri, A., Lankinen, H., Butcher, S. J. & Grünewald, K. (2010). Electron cryotomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J Virol 84, 4889–4897.
14. Ichikawa, Y., Ishikawa, T., Momiyama, N., Kamiyama, M., Sakurada, H., Matsuyama, R., Hasegawa, S., Chishima, T., Hamaguchi, Y. & other authors (2006). Matrilysin (MMP-7) degrades VE-cadherin and accelerates accumulation of b-catenin in the nucleus of human umbilical vein endothelial cells. Oncol Rep 15, 311–315.
15. Ii, M., Yamamoto, H., Adachi, Y., Maruyama, Y. & Shinomura, Y. (2006). Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med (Maywood) 231, 20–27.
16. Jonsson, C. B., Figueiredo, L. T. & Vapalahti, O. (2010). A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23, 412–441.
17. Kittl, E. M., Hofmann, J., Hartmann, G., Sebesta, C., Beer, F., Bauer, K. & Huber, K. R. (2000). Serum protein 90K/Mac-2BP is an independent predictor of disease severity during hepatitis C virus infection. Clin Chem Lab Med 38, 205–208.
18. Klempa, B., Meisel, H., Räth, S., Bartel, J., Ulrich, R. & Krüger, D. H. (2003). Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol 41, 4894–4897.
19. Klingström, J., Plyusnin, A., Vaheri, A. & Lundkvist, A. (2002). Wild-type Puumala hantavirus infection induces cytokines, C-reactive protein, creatinine, and nitric oxide in cynomolgus macaques. J Virol 76, 444–449.
20. Klingström, J., Stoltz, M., Hardestam, J., Ahlm, C. & Lundkvist, A. (2008). Passive immunization protects cynomolgus macaques against Puumala hantavirus challenge. Antivir Ther 13, 125–133.
21. Laferte´, S., Loh, L. C. & Keeler, V. (2000). Monoclonal antibodies specific for human tumor-associated antigen 90K/Mac-2 binding protein: tools to examine protein conformation and function. J Cell Biochem 77, 540–559.
22. Li, Y., Wang, W., Wang, J. P., Pan, L., Zhang, Y., Yu, H. T., Jiang, W., Wang, P. Z. & Bai, X. F. (2012). Elevated vascular endothelial growth factor levels induce hyperpermeability of endothelial cells in hantavirus infection. J Int Med Res 40, 1812–1821.
23. Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 25, 402–408.
24. Lodermeyer, V., Suhr, K., Schrott, N., Kolbe, C., Stürzel, C. M., Krnavek, D., Münch, J., Dietz, C., Waldmann, T. & other authors (2013). 90K, an interferon-stimulated gene product, reduces the infectivity of HIV-1. Retrovirology 10, 111.
25. Longo, G., Natoli, C., Rafanelli, D., Tinari, N., Morfini, M., Rossi- Ferrini, P., D’Ostilio, N. & Iacobelli, S. (1993). Prognostic value of a novel circulating serum 90K antigen in HIV-infected haemophilia patients. Br J Haematol 85, 207–209.
26. Mackow, E. R. & Gavrilovskaya, I. N. (2009). Hantavirus regulation of endothelial cell functions. Thromb Haemost 102, 1030–1041.
27. Mäkelä, S., Mustonen, J., Ala-Houhala, I., Hurme, M., Partanen, J., Vapalahti, O., Vaheri, A. & Pasternack, A. (2002). Human leukocyte antigen-B8-DR3 is a more important risk factor for severe Puumala hantavirus infection than the tumor necrosis factor-a(2308) G/A polymorphism. J Infect Dis 186, 843–846.
28. Mustonen, J., Partanen, J., Kanerva, M., Pietilä, K., Vapalahti, O., Pasternack, A. & Vaheri, A. (1996). Genetic susceptibility to severe course of nephropathia epidemica caused by Puumala hantavirus. Kidney Int 49, 217–221.
29. Natoli, C., Ortona, L., Tamburrini, E., Tinari, N., Di Stefano, P., D’Egidio, M., Ghinelli, F., Sighinolfi, L., D’Ostilio, N. & other authors (1994). Elevated serum levels of a 90,000 daltons tumor-associated antigen in cancer and in infection by human immunodeficiency virus (HIV). Anticancer Res 14 (3B), 1457–1460.
30. Outinen, T. K., Mäkelä, S. M., Ala-Houhala, I. O., Huhtala, H. S., Hurme, M., Paakkala, A. S., Pörsti, I. H., Syrjänen, J. T. & Mustonen, J. T. (2010). The severity of Puumala hantavirus induced nephropathia epidemica can be better evaluated using plasma interleukin-6 than C-reactive protein determinations. BMC Infect Dis 10, 132.
31. Paakkala, A., Mustonen, J., Viander, M., Huhtala, H. & Pasternack, A. (2000). Complement activation in nephropathia epidemica caused by Puumala hantavirus. Clin Nephrol 53, 424–431.
32. Park, Y. P., Choi, S. C., Kim, B. Y., Kim, J. T., Song, E. Y., Kang, S. H., Yoon, D. Y., Paik, S. G., Kim, K. D. & other authors (2008). Induction of Mac-2BP by nerve growth factor is regulated by the PI3K/Akt/NFkB- dependent pathway in the HEK293 cell line. BMB Rep 41, 784–789.
33. Piccolo, E., Tinari, N., Semeraro, D., Traini, S., Fichera, I., Cumashi, A., La Sorda, R., Spinella, F., Bagnato, A. & other authors (2013). LGALS3BP, lectin galactoside-binding soluble 3 binding protein, induces vascular endothelial growth factor in human breast cancer cells and promotes angiogenesis. J Mol Med (Berl) 91, 83–94.
34. Sane, J., Laine, O., Makela, S., Paakkala, A., Jarva, H., Mustonen, J., Vapalahti, O., Meri, S. & Vaheri, A. (2011). Complement activation in puumala hantavirus infection correlates with disease severity. Ann Med 44, 468–475.
35. Shrivastava-Ranjan, P., Rollin, P. E. & Spiropoulou, C. F. (2010). Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VEcadherin. J Virol 84, 11227–11234.
36. Sironen, T., Klingström, J., Vaheri, A., Andersson, L. C., Lundkvist, A. & Plyusnin, A. (2008). Pathology of Puumala hantavirus infection in macaques. PLoS ONE 3, e3035.
37. Thrailkill, K. M., Clay Bunn, R. & Fowlkes, J. L. (2009). Matrix metalloproteinases: their potential role in the pathogenesis of diabetic nephropathy. Endocrine 35, 1–10.
38. Tuuminen, T., Kekäläinen, E., Mäkelä, S., Ala-Houhala, I., Ennis, F. A., Hedman, K., Mustonen, J., Vaheri, A. & Arstila, T. P. (2007). Human CD8+ T cell memory generation in Puumala hantavirus infection occurs after the acute phase and is associated with boosting of EBVspecific CD8+ memory T cells. J Immunol 179, 1988–1995.
39. Ullrich, A., Sures, I., D’Egidio, M., Jallal, B., Powell, T. J., Herbst, R., Dreps, A., Azam, M., Rubinstein, M. & other authors (1994). The secreted tumor-associated antigen 90K is a potent immune stimulator. J Biol Chem 269, 18401–18407.
40. Ulmer, T. A., Keeler, V., Andre´, S., Gabius, H. J., Loh, L. & Laferte´, S. (2010). The tumor-associated antigen 90K/Mac-2-binding protein secreted by human colon carcinoma cells enhances extracellular levels of promatrilysin and is a novel substrate of matrix metalloproteinases- 2, -7 (matrilysin) and -9: implications of proteolytic cleavage. Biochim Biophys Acta 1800, 336–343.
41. Vaheri, A., Mills, J. N., Spiropoulou, C. F. & Hjelle, B. (2011). Hantaviruses. In Zoonoses: Biology, Clinical Practice and Public Health, 2nd edn, pp. 307–322.Edited by S. R. Palmer, L. Soulsby, D. Brown & P. Torgeson. Oxford: Oxford University Press.
42. Vaheri, A., Strandin, T., Hepojoki, J., Sironen, T., Henttonen, H., Mäkelä, S. & Mustonen, J. (2013). Uncovering the mysteries of hantavirus infections. Nat Rev Microbiol 11, 539–550.
43. Vapalahti, O., Kallio-Kokko, H., Salonen, E. M., Brummer- Korvenkontio, M. & Vaheri, A. (1992). Cloning and sequencing of Puumala virus Sotkamo strain S and M RNA segments: evidence for strain variation in hantaviruses and expression of the nucleocapsid protein. J Gen Virol 73, 829–838.
44. Vapalahti, O., Lundkvist, A., Kallio-Kokko, H., Paukku, K., Julkunen, I., Lankinen, H. & Vaheri, A. (1996). Antigenic properties and diagnostic potential of puumala virus nucleocapsid protein expressed in insect cells. J Clin Microbiol 34, 119–125.