Neutrophil activation in acute hemorrhagic fever with renal syndrome is mediated by hantavirus-infected microvascular endothelial cells
Open accessAbstract
Hantaviruses cause hemorrhagic fever with renal syndrome (HFRS) and hantavirus cardiopulmonary syndrome (HCPS) in humans. Both diseases are considered to be immunologically mediated but the exact pathological mechanisms are still poorly understood. Neutrophils are considered as the first line of defense against invading microbes but little is still known of their role in virus infections. We wanted to study the role of neutrophils in HFRS using blood and tissue samples obtained from Puumala hantavirus (PUUV)-infected patients. We found that neutrophil activation products myeloperoxidase and neutrophil elastase, together with interleukin-8 (the major neutrophil chemotactic factor in humans), are strongly elevated in blood of acute PUUV-HFRS and positively correlate with kidney dysfunction, the hallmark clinical finding of HFRS. These markers localized mainly in the tubulointerstitial space in the kidneys of PUUV-HFRS patients suggesting neutrophil activation to be a major likely component of the general immune response towards hantaviruses. We also observed increased levels of circulating extracellular histones at the acute stage of the disease supporting previous findings of neutrophil extracellular trap formation in PUUV-HFRS. Mechanistically, we did not find evidence for direct PUUV-mediated activation of neutrophils but instead primary blood microvascular endothelial cells acquired a pro-inflammatory phenotype and promoted neutrophil degranulation in response to PUUV infection in vitro. These results suggest that neutrophils are activated by hantavirus-infected endothelial cells and may contribute to the kidney pathology which determines the severity of HFRS.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Neutrophil activation products myeloperoxidase, neutrophil elastase, and interleukin-8 were strongly elevated in the blood of patients with hantavirus HFRS and correlate positively with renal dysfunction.
“Tomas Strandin et al., in 2018, found that neutrophil activation products: myeloperoxidase, and neutrophil elastase, along with interleukin-8 (the major neutrophil chemotactic factor in humans), were strongly elevated in the blood of patients with hantavirus HFRS, factors that correlate positively with renal dysfunction [162].”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [162]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Neutrophil Extracellular Traps Kill Bacteria
Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., & Zychlinsky, A. (2004) · Science · doi:10.1126/science.1092385 · Cited by 10,268 · see citing works
Neutrophils, from marrow to microbes.
Borregaard, N. (2010) · Immunity · doi:10.1016/j.immuni.2010.11.011 · Cited by 1,550 · see citing works
Neutrophil kinetics in health and disease
Summers, C., Rankin, S. M., Condliffe, A. M., Singh, N., Peters, A. M., & Chilvers, E. R. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.05.006 · Cited by 1,237 · see citing works
A Global Perspective on Hantavirus Ecology, Epidemiology, and Disease
Jonsson, C. B., Figueiredo, L. T. M., & Vapalahti, O. P. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00062-09 · Cited by 1,150 · see citing works
Essential involvement of interleukin-8 (IL-8) in acute inflammation
Harada, A., Sekido, N., Akahoshi, T., Wada, T., Mukaida, N., & Matsushima, K. (1994) · Journal of Leukocyte Biology · doi:10.1002/jlb.56.5.559 · Cited by 1,041 · see citing works
Branzk, N., Lubojemska, A., Hardison, S. E., Wang, Q., Gutierrez, M. G., Brown, G. D., & Papayannopoulos, V. (2014) · Nature Immunology · doi:10.1038/ni.2987 · Cited by 1,037 · see citing works
Neutrophil serine proteases: specific regulators of inflammation
Pham, C. T. N. (2006) · Nature reviews. Immunology · doi:10.1038/nri1841 · Cited by 1,017 · see citing works
Yipp, B. G., & Kubes, P. (2013) · Blood · doi:10.1182/blood-2013-04-457671 · Cited by 998 · see citing works
How leukocytes cross the vascular endothelium
Vestweber, D. (2015) · Nature Reviews Immunology · doi:10.1038/nri3908 · Cited by 858 · see citing works
Neutrophil Extracellular Traps Mediate a Host Defense Response to Human Immunodeficiency Virus-1
Saitoh, T., Komano, J. A., Saitoh, Y., Misawa, T., Takahama, M., Kozaki, T., Uehata, T., Iwasaki, H., Omori, H., Yamaoka, S., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.05.015 · Cited by 731 · see citing works
Uncovering the mysteries of hantavirus infections
Vaheri, A. I., Strandin, T. M., Hepojoki, J., Sironen, T. A., Henttonen, H. A., Mäkelä, S., & Mustonen, J. T. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3066 · Cited by 544 · see citing works
Self-citationGupta, A. K., Joshi, M. B., Philippova, M., Erné, P., Hasler, P., Hahn, S., & Resink, T. J. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.06.006 · Cited by 538 · see citing works
Direct inactivation of viruses by human granulocyte defensins
Daher, K. A., Selsted, M. E., & Lehrer, R. I. (1986) · Journal of Virology · doi:10.1128/jvi.60.3.1068-1074.1986 · Cited by 535 · see citing works
Jenne, C. N., Wong, C. H. Y., Zemp, F. J., McDonald, B., Rahman, M. M., Forsyth, P. A., McFadden, G., & Kubes, P. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.01.005 · Cited by 443 · see citing works
A Role for Neutrophils in Viral Respiratory Disease
Camp, J. V., & Jonsson, C. B. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00550 · Cited by 222 · see citing works
Pattern recognition receptor function in neutrophils
Thomas, C. J., & Schroder, K. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.02.008 · Cited by 220 · see citing works
Neutrophils in viral infections: Current concepts and caveats
Galani, I. E., & Andreakos, E. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.4vmr1114-555r · Cited by 214 · see citing works
Viral hemorrhagic fever – a vascular disease?
Feldmann, H., & Schnittler, H. (2003) · Thrombosis and Haemostasis · doi:10.1055/s-0037-1613397 · Cited by 193 · see citing works
β2 integrin mediates hantavirus-induced release of neutrophil extracellular traps
Raftery, M. J., Lalwani, P. J., Krautkrämer, E., Peters, T., Scharffetter‐Kochanek, K., Krüger, R., Hofmann, J., Seeger, K., Krüger, D. H., & Schönrich, G. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20131092 · Cited by 191 · see citing works
Neutrophil-Mediated Regulation of Innate and Adaptive Immunity: The Role of Myeloperoxidase
Odobasic, D., Kitching, A. R., & Holdsworth, S. R. (2016) · Journal of Immunology Research · doi:10.1155/2016/2349817 · Cited by 191 · see citing works
Temonen, M., Mustonen, J. T., Helin, H., Pasternack, A. I., Vaheri, A. I., & Holthöfer, H. (1996) · Clinical Immunology and Immunopathology · doi:10.1006/clin.1996.0007 · Cited by 176 · see citing works
Self-citationDengue virus infects human endothelial cells and induces IL-6 and IL-8 production.
Huang, Y., Lei, H.-Y., Liu, H., Lin, Y.-S., Liu, C., & Yeh, T. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.63.71 · Cited by 175 · see citing works
Vapalahti, O. P., Kallio‐Kokko, H., Närvänen, A. T. O., Julkunen, I., Lundkvist, Å., Plyusnin, A., Lehväslaiho, H., Brummer‐Korvenkontio, M., Vaheri, A. I., & Lankinen, H. (1995) · Journal of Medical Virology · doi:10.1002/jmv.1890460402 · Cited by 172 · see citing works
Self-citationLundkvist, �., & Niklasson, B. (1992) · Archives of Virology · doi:10.1007/bf01309687 · Cited by 116 · see citing works
Renal biopsy findings and clinicopathologic correlations in nephropathia epidemica.
Mustonen, J. T., Helin, H., PIETILÄ, K. A., Brummer‐Korvenkontio, M., Hedman, K., Vaheri, A., & Pasternack, A. I. (1994) · PubMed · Cited by 113 · see citing works
Self-citationHarcourt, B. H., Sanchez, A., & Offermann, M. K. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.3491-3496.1999 · Cited by 111 · see citing works
Endothelial Cells Elicit Immune-Enhancing Responses to Dengue Virus Infection
Dalrymple, N. A., & Mackow, E. R. (2012) · Journal of Virology · doi:10.1128/jvi.00213-12 · Cited by 109 · see citing works
Klebanoff, S. J., & Coombs, R. W. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115810 · Cited by 97 · see citing works
The fundamental role of endothelial cells in hantavirus pathogenesis
Hepojoki, J., Vaheri, A. I., & Strandin, T. M. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00727 · Cited by 93 · see citing works
Self-citationHartshorn, K. L., Liou, L. S., White, M. R., Kazhdan, M., Tauber, J., & Tauber, A. I. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.154.8.3952 · Cited by 77 · see citing works
Cytokine expression during early and late phase of acute Puumala hantavirus infection
Sadeghi, M., Eckerle, I., Daniel, V., Burkhardt, U., Opelz, G., & Schnitzler, P. (2011) · BMC Immunology · doi:10.1186/1471-2172-12-65 · Cited by 74 · see citing works
Kidney disease in Puumala hantavirus infection
Mustonen, J. T., Outinen, T. K., Laine, O., Pörsti, I. H., Vaheri, A. I., & Mäkelä, S. (2017) · Scandinavian Journal of Infectious Diseases · doi:10.1080/23744235.2016.1274421 · Cited by 74 · see citing works
Self-citationInteractions and Oligomerization of Hantavirus Glycoproteins
Hepojoki, J., Strandin, T. M., Vaheri, A. I., & Lankinen, H. (2009) · Journal of Virology · doi:10.1128/jvi.00481-09 · Cited by 73 · see citing works
Self-citationSano, H., Nakagawa, N., Chiba, R., Kurasawa, K., Saito, Y., & Iwamoto, I. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9385 · Cited by 71 · see citing works
Andes virus stimulates interferon‐inducible MxA protein expression in endothelial cells
Khaiboullina, S. F., Rizvanov, A. A., Deyde, V., & Jeor, S. C. S. (2004) · Journal of Medical Virology · doi:10.1002/jmv.20266 · Cited by 60 · see citing works
Kim, S., Kang, E. T., Kim, Y. G., Han, J. S., Lee, J. S., Kim, Y. I., Hall, W. C., Dalrymple, J. M., & Peters, C. J. (1993) · American Journal of Clinical Pathology · doi:10.1093/ajcp/100.4.398 · Cited by 58 · see citing works
Hantavirus-induced disruption of the endothelial barrier: neutrophils are on the payroll
Schönrich, G., ̈ger, D. H. K., & Raftery, M. J. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00222 · Cited by 48 · see citing works
Multiplex Analysis of Serum Cytokines in Humans with Hantavirus Pulmonary Syndrome
Morzunov, S. P., Khaiboullina, S. F., Jeor, S. S., Rizvanov, A. A., & Lombardi, V. C. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00432 · Cited by 47 · see citing works
Understanding the molecular mechanisms of NETs and their role in antiviral innate immunity
Agraz‐Cibrián, J. M., Giraldo, D. M., Mary, F.-M., & Inchima, S. U. (2016) · Virus Research · doi:10.1016/j.virusres.2016.11.033 · Cited by 47 · see citing works
Vaheri, A. I., Strandin, T. M., Jaaskelainen, A. J. J., Vapalahti, O. P., Jarva, H., Lokki, M., Antonen, J. A., Leppänen, I., Mäkelä, S., Meri, S., et al. (2014) · Antiviral Research · doi:10.1016/j.antiviral.2014.08.007 · Cited by 45 · see citing works
Self-citationEndothelial cell dysfunction in viral hemorrhage and edema
Mackow, E. R., Gorbunova, E. E., & Gavrilovskaya, I. N. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00733 · Cited by 43 · see citing works
Libraty, D. H., Mäkelä, S., Vlk, J., Hurme, M., Vaheri, A. I., Ennis, F. A., & Mustonen, J. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035402 · Cited by 43 · see citing works
Self-citationPlasma Cell-Free DNA Levels Are Elevated in Acute Puumala Hantavirus Infection
Outinen, T., Kuparinen, T., Jylhävä, J., Leppänen, S., Mustonen, J., Mäkelä, S., Pörsti, I., Syrjänen, J., Vaheri, A., & Hurme, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031455 · Cited by 40 · see citing works
Self-citationKoma, T., Yoshimatsu, K., Nagata, N., Sato, Y., Shimizu, K., Yasuda, S. P., Amada, T., Nishio, S., Hasegawa, H., & Arikawa, J. (2014) · Journal of Virology · doi:10.1128/jvi.00254-14 · Cited by 38 · see citing works
Bunz, H., Weyrich, P., Peter, A., Baumann, D., Tschritter, O., Guthoff, M., Beck, R., Jahn, G., Artunç, F., Häring, H., et al. (2015) · BMC Infectious Diseases · doi:10.1186/s12879-015-1180-9 · Cited by 28 · see citing works
Strandin, T. M., Hepojoki, J., Laine, O., Mäkelä, S., Klingström, J., Lundkvist, Å., Julkunen, I., Mustonen, J. T., & Vaheri, A. I. (2015) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiv764 · Cited by 28 · see citing works
Self-citationNeutrophils: Neglected Players in Viral Diseases
Gabriel, C., Her, Z., & Ng, L. F. P. (2013) · DNA and Cell Biology · doi:10.1089/dna.2013.2211 · Cited by 23 · see citing works
Khaiboullina, S. F., Martynova, E. V., Хамидуллина, З. Л., Lapteva, E. V., Nikolaeva, I. V., Anokhin, V. V., Lombardi, V. C., & Rizvanov, A. A. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-014-2176-x · Cited by 23 · see citing works
Inflammatory cytokines kinetics define the severity and phase of nephropathia epidemica
Ахметовна, Б. А., Khaiboullina, S. F., Martynova, E. V., Алексеевич, А. В., Lombardi, V. C., & Rizvanov, A. A. (2014) · Biomarkers in Medicine · doi:10.2217/bmm.14.88 · Cited by 20 · see citing works
Association of ICAM-1 K469E polymorphism with dengue infection in North Indian population
Sharma, S. H., Singh, S. K., Kakkar, K., Nyari, N., Singh, D., Dhole, T. N., Kashyap, R., & Hasan, S. (2016) · Microbial Pathogenesis · doi:10.1016/j.micpath.2016.05.006 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Role of Reactive Species on Innate Immunity
Andrés, C., Pérez de la Lastra, J., Juan, C., Plou, F., & Pérez-Lebeña, E. (2022) · Vaccines · doi:10.3390/vaccines10101735 · Cited by 142 · see citing works
Neutrophil Extracellular Traps Effectively Control Acute Chikungunya Virus Infection
Hiroki, C. H., Toller-Kawahisa, J. E., Fumagalli, M. J., Colón, D. F., Figueiredo, L. T. M., Fonseca, B. A. L. D., França, R. F. D. O., & Cunha, F. Q. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.03108 · Cited by 118 · see citing works
Koehler, F. C., Cristanziano, V. D., Späth, M. R., Hoyer-Allo, K. J. R., Wanken, M., Müller, R., & Burst, V. R. (2022) · Clinical Kidney Journal · doi:10.1093/ckj/sfac008 · Cited by 70 · see citing works
Klingström, J., Smed‐Sörensen, A., Maleki, K. T., Solà-Riera, C., Ahlm, C., Björkström, N. K., & Ljunggren, H. (2019) · Journal of Internal Medicine · doi:10.1111/joim.12876 · Cited by 61 · see citing works
Korva, M., Rus, K. R., Pavletič, M., Saksida, A., Knap, N., Jelovšek, M., Smrdel, K. S., Jakupi, X., Humolli, I., Dedushaj, J., et al. (2019) · Viruses · doi:10.3390/v11080686 · Cited by 43 · see citing works
Neutrophil Extracellular Traps in Dengue Are Mainly Generated NOX-Independently
Garishah, F. M., Rother, N., Riswari, S. F., Alisjahbana, B., Overheul, G. J., van Rij, R. P., van der Ven, A. J. A. M., van der Vlag, J., & de Mast, Q. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.629167 · Cited by 39 · see citing works
Zhang, Y., Song, R., Shen, Y., Zhao, Y., Zhao, Z., Fan, T., Yang, X., Wang, L., Zhang, W., Chen, C., et al. (2019) · Clinical Infectious Diseases · doi:10.1093/cid/ciz553 · Cited by 35 · see citing works
Hantavirus Research in Finland: Highlights and Perspectives
Vaheri, A. I., Henttonen, H. A., & Mustonen, J. T. (2021) · Viruses · doi:10.3390/v13081452 · Cited by 31 · see citing works
Self-citationHantavirus-Driven PD-L1/PD-L2 Upregulation: An Imperfect Viral Immune Evasion Mechanism
Raftery, M. J., Abdelaziz, M. O., Hofmann, J., & Schönrich, G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02560 · Cited by 30 · see citing works
Viral-Induced Inflammatory Coagulation Disorders: Preparing for Another Epidemic
Iba, T., Levy, J. H., & Levi, M. M. (2021) · Thrombosis and Haemostasis · doi:10.1055/a-1562-7599 · Cited by 29 · see citing works
Coagulopathy in Acute Puumala Hantavirus Infection
Koskela, S. M., Mäkelä, S., Strandin, T. M., Vaheri, A. I., Outinen, T. K., Joutsi‐Korhonen, L., Pörsti, I. H., Mustonen, J. T., & Laine, O. (2021) · Viruses · doi:10.3390/v13081553 · Cited by 29 · see citing works
Self-citationSeoul Virus Tropism and Pathology in Naturally Infected Feeder Rats
Maas, M., van Heteren, M., de Vries, A., Kuiken, T., Hoornweg, T. E., Kroeze, E. J. B. V., & Rockx, B. (2019) · Viruses · doi:10.3390/v11060531 · Cited by 27 · see citing works
Neutrophil extracellular traps: Modulation mechanisms by pathogens
Gonzalez-Contreras, F. D. J., & Zárate, X. (2022) · Cellular Immunology · doi:10.1016/j.cellimm.2022.104640 · Cited by 27 · see citing works
Dendritic Cells (DCs) as “Fire Accelerants” of Hantaviral Pathogenesis
Schönrich, G., & Raftery, M. J. (2019) · Viruses · doi:10.3390/v11090849 · Cited by 20 · see citing works
Iglesias, A., Períolo, N., Bellomo, C., Lewis, L. C., Olivera, C. P., Anselmo, C. R., García, M., Coelho, R. M., Alonso, D. O., Dighero-Kemp, B., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2021.103765 · Cited by 18 · see citing works
Hantavirus infection-induced B cell activation elevates free light chains levels in circulation
Hepojoki, J., Cabrera, L. E., Hepojoki, S., Bellomo, C., Kareinen, L., Andersson, L. C., Vaheri, A. I., Mäkelä, S., Mustonen, J. T., Vapalahti, O. P., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009843 · Cited by 18 · see citing works
Self-citationRibeiro, G. E., León, L. E., Perez, R., Cuiza, A., Vial, P., Marcela Ferrés, G., MERTZ, G. J., & Vial, C. (2019) · Viruses · doi:10.3390/v11080680 · Cited by 16 · see citing works
Vangeti, S., Strandin, T. M., Liu, S., Tauriainen, J., Räisänen-Sokolowski, A. K., Cabrera, L. E., Hassinen, A., Mäkelä, S., Mustonen, J. T., Vaheri, A. I., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009400 · Cited by 16 · see citing works
Self-citationBourquain, D. R., Bodenstein, C., Schuerer, S., & Schaade, L. (2019) · Viruses · doi:10.3390/v11090855 · Cited by 16 · see citing works
Cabrera, L. E., Schmotz, C., Saleem, M. A., Lehtonen, S. H., Vapalahti, O. P., Vaheri, A. I., Mäkelä, S., Mustonen, J. T., & Strandin, T. M. (2022) · Viruses · doi:10.3390/v14030450 · Cited by 15 · see citing works
Self-citationDu, H., Hu, H., Wang, P., Wang, X., Zhang, Y., Jiang, H. X., Li, J., Bai, X., & Lian, J. (2021) · BMC Infectious Diseases · doi:10.1186/s12879-021-06145-0 · Cited by 14 · see citing works
Direct and indirect effects of Puumala hantavirus on platelet function
Schrottmaier, W. C., Schmuckenschlager, A., Thunberg, T., Byström, J. W., Connolly-Andersen, A.-M., Assinger, A., Ahlm, C., & Forsell, M. N. E. (2023) · Thrombosis Research · doi:10.1016/j.thromres.2023.11.017 · Cited by 12 · see citing works
Nußhag, C., Gruber, G., Zeier, M. G., & Krautkrämer, E. (2024) · Journal of Medical Virology · doi:10.1002/jmv.29759 · Cited by 12 · see citing works
García, M., García, A. C., Weigel, W., Christ, W., Lira‐Junior, R., Wirth, L. E., Tauriainen, J., Maleki, K. T., Vanoni, G., Vaheri, A. I., et al. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1012390 · Cited by 11 · see citing works
Self-citationSeoul orthohantavirus evades innate immune activation by reservoir endothelial cells
Klimaj, S. D., LaPointe, A. T., Martinez, K., Acosta, E. H., & Kell, A. M. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1012728 · Cited by 10 · see citing works
Yang, Z., Hu, Q., Feng, Z., & Sun, Y. (2021) · Open Medicine · doi:10.1515/med-2021-0307 · Cited by 10 · see citing works
Iheozor-Ejiofor, R. P., Vapalahti, K., Sironen, T. A., Levanov, L., Hepojoki, J., Lundkvist, Å., Mäkelä, S., Vaheri, A. I., Mustonen, J. T., Plyusnin, A., et al. (2022) · Viruses · doi:10.3390/v14050901 · Cited by 10 · see citing works
Self-citationWei, Z., Shimizu, K., Sarii, R. S., Muthusinghe, D. S., Lokupathirage, S. M. W., Nio‐Kobayashi, J., & Yoshimatsu, K. (2022) · Viruses · doi:10.3390/v14102247 · Cited by 9 · see citing works
A Putative Role for TRPC6 in Immune-Mediated Kidney Injury
Hart, D. C. ‘., van der Vlag, J., & Nijenhuis, T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216419 · Cited by 8 · see citing works
Cytokine Profiles and Antibody Response Associated to Choclo Orthohantavirus Infection
Salinas, T. P., Garrido, J. L. V., Salazar, J. R., González, P., Zambrano, N., Fuentes‐Villalobos, F., Bravo, F., Fica-León, V., Salas-Burgos, A., Calvo, M. A., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.603228 · Cited by 8 · see citing works
Tietäväinen, J., Mäkelä, S., Huhtala, H., Pörsti, I. H., Strandin, T. M., Vaheri, A. I., & Mustonen, J. T. (2021) · Viruses · doi:10.3390/v13061177 · Cited by 8 · see citing works
Self-citationSerum Cytokine Alterations Associated with Age of Patients with Nephropathia Epidemica
Shakirova, V. G., Khaertynova, I., Markelova, M., Tarlinton, R., Behnke, J., Martynova, E. V., Garanina, E., Rizvanov, A. A., & Khaiboullina, S. (2022) · BioMed Research International · doi:10.1155/2022/4685288 · Cited by 8 · see citing works
Wang, S., Wang, F., Ma, Y., Zhuang, R., Zhang, Y., Zhang, C., Tang, K., Wei, Y., Zuo, J., Xu, X., et al. (2025) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2025.108280 · Cited by 6 · see citing works
Hemorrhagic Fever Renal Syndrome
Romero, M. G., & Anjum, F. (2021) · StatPearls · Cited by 5 · see citing works
Cabrera, L. E., Tietäväinen, J., Jokiranta, S. T., Mäkelä, S., Vaheri, A. I., Mustonen, J. T., Vapalahti, O. P., Kanerva, M. J., & Strandin, T. M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1419787 · Cited by 5 · see citing works
Self-citationYao, L., Wang, X., Wang, Z.-H., & Wang, X. (2024) · International Journal of General Medicine · doi:10.2147/ijgm.s480204 · Cited by 5 · see citing works
Zhong, L., Shi, H., Li, H., Lü, X., Peng, Q., Liu, Z., Wu, P., & Mo, X. (2024) · Infection and Drug Resistance · doi:10.2147/idr.s499197 · Cited by 4 · see citing works
Li, P., Zhang, C., Wang, M., Zhang, X., Zhang, Y., Tang, K., Hu, H., Jia, X., Zhuang, R., Jin, B., et al. (2022) · Viral Immunology · doi:10.1089/vim.2022.0007 · Cited by 4 · see citing works
Zheng, Z., Geng, J., Jiang, Y., Zhang, M., Yang, R., Ge, G., Xu, H., & Zhang, X. (2021) · Springer eBooks · doi:10.1007/978-981-16-1037-0_36 · Cited by 4 · see citing works
RNA Viruses, Pregnancy and Vaccination: Emerging Lessons from COVID-19 and Ebola Virus Disease
Dhanya, C. R., Shailaja, A., Mary, A. S., Kandiyil, S. P., Savithri, A., Vishnu, S. K., Veettil, J. T., Vandanamthadathil, J. J., & Madhavan, M. (2022) · Pathogens · doi:10.3390/pathogens11070800 · Cited by 4 · see citing works
Glomerular Injury Is Associated with Severe Courses of Orthohantavirus Infection
Nußhag, C., Uhrig, J., Gruber, G., Schreiber, P., Zeier, M., & Krautkrämer, E. (2024) · Pathogens · doi:10.3390/pathogens13080693 · Cited by 3 · see citing works
Hantavirus Research in Finland
Mustonen, J. T., Strandin, T. M., Tietäväinen, J., Pörsti, I. H., Mäkelä, S., & Vaheri, A. I. (2024) · Viruses · doi:10.3390/v16101591 · Cited by 2 · see citing works
Self-citationCao, X., Jin, Y., Du, H., Wang, W., Zhao, Y., Zheng, X., Wang, L., Bian, P., Wang, L., & Jiang, H. X. (2025) · Vector-Borne and Zoonotic Diseases · doi:10.1089/vbz.2024.0063 · Cited by 2 · see citing works
ABO and Rhesus Blood Groups in Acute Puumala Hantavirus Infection
Tietäväinen, J., Laine, O., Mäkelä, S., Huhtala, H., Pörsti, I. H., Vaheri, A. I., & Mustonen, J. T. (2021) · Viruses · doi:10.3390/v13112271 · Cited by 2 · see citing works
Self-citationHantaviruses in a Global Perspective
Krautkrämer, E., Peintner, L., & Essbauer, S. S. (2023) · Springer eBooks · doi:10.1007/978-3-031-27164-9_30 · Cited by 2 · see citing works
Research Progress on the Pathogenesis of Hemorrhagic Fever with Renal Syndrome
Du, H., Wang, P., Bai, X., Li, J., Wang, X., Hu, H., Zhang, Y., Jiang, H. X., Shen, H., Zhan, J., et al. (2022) · Infectious Diseases & Immunity · doi:10.1097/id9.0000000000000042 · Cited by 1 · see citing works
The role of immune mechanisms in the pathogenesis of hemorrhagic fever with renal syndrome
Ivanov, M. F. (2023) · Aspirantskiy Vestnik Povolzhiya · doi:10.55531/2072-2354.2023.23.3.4-12 · Cited by 1 · see citing works
Ye, C., Zhang, R., Wu, S., Wei, M., Cao, J., Du, X., Yang, X., Fan, C., Kang, B., Zhang, G., et al. (2026) · Immunity Inflammation and Disease · doi:10.1002/iid3.70366 · Cited by 1 · see citing works
Infección por Hantavirus: Visión global y situación en España
Bouza, E., Fructuoso, A. S., Villegas, A., & Alvar, J. (2026) · ANALES RANM · doi:10.32440/ar.2026.143.02.as01 · Cited by 1 · see citing works
García, M., García, A. C., Tauriainen, J., Maleki, K. T., Vaheri, A. I., Mäkelä, S., Mustonen, J. T., Smed‐Sörensen, A., Strandin, T. M., Mjösberg, J., et al. (2022) · medRxiv · doi:10.1101/2022.05.10.22274837 · Cited by 1 · see citing works
Self-citationRole of monocytes in endothelial glycocalyx shedding during Puumala orthohantavirus infectionPreprint
Cabrera, L. E., Polanco, I., Tietäväinen, J., Mäkelä, S., Vapalahti, O. P., Vaheri, A. I., Mustonen, J. T., & Strandin, T. M. (2024) · medRxiv · doi:10.1101/2024.08.25.24312546 · Cited by 1 · see citing works
Self-citationDu, H., Hu, H., Wang, P., Wang, X., Zhang, Y., Jiang, H. X., Li, J., Bai, X., & Lian, J. (2020) · doi:10.21203/rs.3.rs-30998/v1
Prediction of chronic kidney disease in patients with hemorrhagic fever with renal syndrome
Stulova, M. V., Konstantinov, D. Y., Popova, L. L., Валентиновна, Л. А., & Владимирович, Н. Г. (2021) · Science and Innovations in Medicine · doi:10.35693/2500-1388-2022-7-1-35-38
Du, H. X., Hu, H., Wang, P., Wang, X., Zhang, Y., Jiang, H., Li, J., Bai, X., & Lian, J. (2020) · doi:10.21203/rs.3.rs-30998/v2
Hantaviruses in a Global Perspective
Krautkrämer, E., Peintner, L., & Essbauer, S. S. (2022) · Springer eBooks · doi:10.1007/978-3-030-85877-3_30-1
Wang, M., Zhou, Y. G., Wang, Y., Du, Y., Guo, Z., Ma, L., Zhang, H., & Wang, Y. (2023) · Frontiers in Pediatrics · doi:10.3389/fped.2023.1168205
Bai, F., 雷泽恺, Bai, H., Li, D., & Tang, N. (2026) · Clinica Chimica Acta · doi:10.1016/j.cca.2026.121065
Temporal Dynamics of Viremia in Hemorrhagic Fever With Renal Syndrome Patients
Ma, S., Zhan, J., Fan, C., Zheng, X. H., Du, H., Wang, L. X., & Jiang, H. (2026) · Journal of Medical Virology · doi:10.1002/jmv.70963
Wang, T., Qi, K., Li, Y., Zhao, Q., Yao, Y., Zheng, L., Zheng, X., & Shi, H. (2026) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2026.1744838
Duong, T. T. N., Sasaki, M., Orba, Y., Aoshima, K., Ichii, O., Maezono, K., Thammahakin, P., Eguchi, H., Kobayashi, S., & Kariwa, H. (2026) · Journal of Virology · doi:10.1128/jvi.00321-26
Ma, H., Ye, W., Lv, Y., Lei, Y., Jiang, S., 张芳琳, & 徐志凯 (2026) · Current Research in Microbial Sciences · doi:10.1016/j.crmicr.2026.100668
- Authors
- Strandin, T., Mäkelä, S., Mustonen, J., & Vaheri, A.
- Affiliations
- University of Helsinki (FI)
- Tampere University Hospital (FI)
- Corresponding author
- Strandin, Tomas
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2018-09-18
- Volume
- 9
- Pages
- 2098-2098
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC6157395
- OpenAlex
- W2892301109
- Cited by
- 61
- References
- 50
- Citations by year
- 2026: 7 · 2025: 2 · 2024: 9 · 2023: 5 · 2022: 13 · 2021: 14 · 2020: 3 · 2019: 7 · 2018: 1
- FWCI
- 4.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Tampere University Institutional Repository (Tampere University) (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Työväentutkimus Vuosikirja (submittedVersion)
- Tampere University Institutional Repository (Tampere University) (submittedVersion, cc-by)
- Funders
- Academy of Finland (1275597)
- Sigrid Juséliuksen Säätiö
- Magnus Ehrnroothin Säätiö
- Tampereen TuberkuloosisäätiÖ
- Topics
- Health Sciences › Medicine › Infectious Diseases › Viral Infections and Vectors
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Keywords
- hemorrhagic fever with renal syndrome, Puumala hantavirus, neutrophil activation, hantavirus infection, microvascular endothelial cells, myeloperoxidase, neutrophil elastase, interleukin-8, extracellular histones, neutrophil extracellular traps, neutrophil degranulation, renal dysfunction, hantavirus pulmonary syndrome
- MeSH terms
- Acute Disease, Cells, Cultured, Hemorrhagic Fever with Renal Syndrome, Humans, Immunity, Innate, Kidney, Peroxidase, Neutrophils, Interleukin-8, Hantaan virus, Neutrophil Activation, Leukocyte Elastase, Nitric Oxide Synthase Type III, Microvessels, Extracellular Traps
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
