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Correlation of CD38 expression with the progression of hemorrhagic fever with renal syndrome

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Abstract

To assess the relationship between the expression of CD38 and the progression of hemorrhagic fever with renal syndrome (HFRS), we determined the levels of CD38 during different phases of HFRS and evaluated the relationship between changes in CD38 expression and the progression of HFRS. The expression of CD38 in 68 patients with HFRS was analyzed by flow cytometry, and this method was also used to determine the levels of CD4+T, CD8+T, and B lymphocytes and NK cells. Furthermore, creatinine (Cr), uric acid (UA), and urea in serum at each stage of HFRS were measured using commercial kits. The basic clinical reference values for leukocytes, platelets (PLT), and red blood cells were determined by conventional methods. The colloidal gold method was used to measure HFRS antibody levels in the patients. A significant change in CD38 expression was observed from the fever phase to the recovery phase in patients with HFRS. Moreover, the expression of CD38 was proportionally correlated with the levels of Cr, UA, and urea in serum. In contrast, there was an inverse correlation between CD38 and PLT. Interestingly, an increase in CD38 expression correlated with an increase in CD8+T lymphocytes, B cells, and NK cells, but with a decrease in CD4+T lymphocytes. The expression of CD38 is associated with the progression of HFRS, suggesting that it may be a potent indicator of the stages of this disorder.

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References

  1. Lee HW, Lee PW, Johnson KM (2004) Isolation of the etiologic agent of Korean hemorrhagic fever. 1978. J Infect Dis 190(9):1711–1721

    Article  Google Scholar 

  2. Muranyi W, Bahr U, Zeier M, van der Woude FJ (2005) Hantavirus infection. J Am Soc Nephrol 16(12):3669–3679

    Article  CAS  Google Scholar 

  3. Ma Y, Wang J, Yuan B et al (2013) HLA-A2 and B35 restricted hantaan virus nucleoprotein CD8+ T-cell epitope-specific immune response correlates with milder disease in hemorrhagic fever with renal syndrome. PLoS Negl Trop Dis 7(2):e2076

    Article  CAS  Google Scholar 

  4. Kanerva M, Mustonen J, Vaheri A (1998) Pathogenesis of puumala and other hantavirus infections. Rev Med Virol 8(2):67–86

    Article  CAS  Google Scholar 

  5. Yan L, Fang LQ, Huang HG et al (2007) Landscape elements and Hantaan virus-related hemorrhagic fever with renal syndrome, People’s Republic of China. Emerg Infect Dis 13(9):1301–1306

    Article  Google Scholar 

  6. Mertz GJ, Hjelle BL, Bryan RT (1997) Hantavirus infection. Adv Intern Med 42:369–421

    CAS  PubMed  Google Scholar 

  7. Huang C, Jin B, Wang M, Li E, Sun C (1994) Hemorrhagic fever with renal syndrome: relationship between pathogenesis and cellular immunity. J Infect Dis 169(4):868–870

    Article  CAS  Google Scholar 

  8. Markotic A, Dasic G, Gagro A et al (1999) Role of peripheral blood mononuclear cell (PBMC) phenotype changes in the pathogenesis of haemorrhagic fever with renal syndrome (HFRS). Clin Exp Immunol 115(2):329–334

    Article  CAS  Google Scholar 

  9. Terajima M, Ennis FA (2011) T cells and pathogenesis of hantavirus cardiopulmonary syndrome and hemorrhagic fever with renal syndrome. Viruses 3(7):1059–1073

    Article  Google Scholar 

  10. Kraus AA, Raftery MJ, Giese T et al (2004) Differential antiviral response of endothelial cells after infection with pathogenic and nonpathogenic hantaviruses. J Virol 78(12):6143–6150

    Article  CAS  Google Scholar 

  11. Malavasi F, Funaro A, Alessio M et al (1992) CD38: a multi-lineage cell activation molecule with a split personality. Int J Clin Lab Res 22(2):73–80

    Article  CAS  Google Scholar 

  12. Alessio M, Roggero S, Funaro A et al (1990) CD38 molecule: structural and biochemical analysis on human T lymphocytes, thymocytes, and plasma cells. J Immunol 145(3):878–884

    CAS  PubMed  Google Scholar 

  13. Kestens L, Vanham G, Gigase P et al (1992) Expression of activation antigens, HLA-DR and CD38, on CD8 lymphocytes during HIV-1 infection. AIDS 6(8):793–797

    Article  CAS  Google Scholar 

  14. Henriques A, Silva I, Ines L et al (2016) CD38, CD81 and BAFFR combined expression by transitional B cells distinguishes active from inactive systemic lupus erythematosus. Clin Exp Med 16(2):227–232

    Article  CAS  Google Scholar 

  15. Matsuoka T, Kajimoto Y, Watada H et al (1995) Expression of CD38 gene, but not of mitochondrial glycerol-3-phosphate dehydrogenase gene, is impaired in pancreatic islets of GK rats. Biochem Biophys Res Commun 214(1):239–246

    Article  CAS  Google Scholar 

  16. Sun L, Adebanjo OA, Moonga BS et al (1999) CD38/ADP-ribosyl cyclase: A new role in the regulation of osteoclastic bone resorption. J Cell Biol 146(5):1161–1172

    Article  CAS  Google Scholar 

  17. Lin P, Owens R, Tricot G, Wilson CS (2004) Flow cytometric immunophenotypic analysis of 306 cases of multiple myeloma. Am J Clin Pathol 121(4):482–488

    Article  Google Scholar 

  18. Perfetti V, Bellotti V, Garini P et al (1994) AL amyloidosi. Characterization of amyloidogenic cells by anti-idiotypic monoclonal antibodies. Lab Invest 71(6):853–861

    CAS  PubMed  Google Scholar 

  19. Suzuki R, Suzumiya J, Nakamura S et al (2004) Aggressive natural killer-cell leukemia revisited: large granular lymphocyte leukemia of cytotoxic NK cells. Leukemia 18(4):763–770

    Article  CAS  Google Scholar 

  20. van de Donk NW, Lokhorst HM, Anderson KC, Richardson PG (2012) How I treat plasma cell leukemia. Blood 120(12):2376–2389

    Article  Google Scholar 

  21. Khaiboullina SF, St Jeor SC (2002) Hantavirus immunology. Viral Immunol 15(4):609–625

    Article  CAS  Google Scholar 

  22. de Carvalho Nicacio C, Gonzalez Della Valle M, Padula P, Bjorling E, Plyusnin A, Lundkvist A (2002) Cross-protection against challenge with Puumala virus after immunization with nucleocapsid proteins from different hantaviruses. J Virol 76(13):6669–6677

    Article  Google Scholar 

  23. Rasmuson J, Andersson C, Norrman E, Haney M, Evander M, Ahlm C (2011) Time to revise the paradigm of hantavirus syndromes? Hantavirus pulmonary syndrome caused by European hantavirus. Eur J Clin Microbiol Infect Dis 30(5):685–690

    Article  CAS  Google Scholar 

  24. Belkaid Y, Rouse BT (2005) Natural regulatory T cells in infectious disease. Nat Immunol 6(4):353–360

    Article  CAS  Google Scholar 

  25. Dianzani U, Funaro A, DiFranco D et al (1994) Interaction between endothelium and CD4+CD45RA+ lymphocytes. Role of the human CD38 molecule. J Immunol 153(3):952–959

    CAS  PubMed  Google Scholar 

  26. Zaki SR, Greer PW, Coffield LM et al (1995) Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol 146(3):552–579

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Liang W, Gu X, Li X et al (2018) Mapping the epidemic changes and risks of hemorrhagic fever with renal syndrome in Shaanxi Province, China, 2005–2016. Sci Rep 8(1):749

    Article  Google Scholar 

  28. Du H, Li J, Yu H et al (2015) HMGB-1 as a novel predictor of disease severity and prognosis in patients with hemorrhagic fever with renal syndrome. Mediat Inflamm 2015:696248

    Google Scholar 

  29. Lodoen MB, Lanier LL (2006) Natural killer cells as an initial defense against pathogens. Curr Opin Immunol 18(4):391–398

    Article  CAS  Google Scholar 

  30. Santoli D, Trinchieri G, Koprowski H (1978) Cell-mediated cytotoxicity against virus-infected target cells in humans. II. Interferon induction and activation of natural killer cells. J Immunol 121(2):532–538

    CAS  PubMed  Google Scholar 

  31. Orange JS (2006) Human natural killer cell deficiencies. Curr Opin Allergy Clin Immunol 6(6):399–409

    Article  Google Scholar 

  32. Bryceson YT, Rudd E, Zheng C et al (2007) Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 110(6):1906–1915

    Article  CAS  Google Scholar 

  33. Bjorkstrom NK, Lindgren T, Stoltz M et al (2011) Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 208(1):13–21

    Article  Google Scholar 

  34. Garcia M, Iglesias A, Landoni VI et al (2017) Massive plasmablast response elicited in the acute phase of hantavirus pulmonary syndrome. Immunology 151(1):122–135

    Article  CAS  Google Scholar 

  35. Nolte KB, Feddersen RM, Foucar K et al (1995) Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum Pathol 26(1):110–120

    Article  CAS  Google Scholar 

  36. Lindgren T, Ahlm C, Mohamed N, Evander M, Ljunggren HG, Bjorkstrom NK (2011) Longitudinal analysis of the human T cell response during acute hantavirus infection. J Virol 85(19):10252–10260

    Article  CAS  Google Scholar 

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Funding

This work was supported by National Natural Science Foundation of China (no. 81572435).

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Contributions

H.-D. Zhao: data curation, writing—original draft preparation. Y.-P. Li: visualization, investigation, supervision. W.-W. Zhao: conceptualization, methodology, software. P. Li: software, validation. H.-L. Liu: writing—reviewing, funding acquisition and editing.

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Correspondence to Hong-Li Liu.

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The authors report no conflicts of interest.

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Handling Editor: Hideki Ebihara.

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Zhao, HD., Li, YP., Zhao, WW. et al. Correlation of CD38 expression with the progression of hemorrhagic fever with renal syndrome. Arch Virol 166, 2399–2406 (2021). https://doi.org/10.1007/s00705-021-05136-5

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  • DOI: https://doi.org/10.1007/s00705-021-05136-5

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