From COVID-19 to clot: the involvement of the complement system

References

• Bikdeli, B., Madhavan, M. V., Jimenez, D., Chuich, T., Dreyfus, I., Driggin, E., Nigoghossian, C., Ageno, W., Madjid, M., Guo, Y., Tang, L. V., Hu, Y., Giri, J., Cushman, M., Quéré, I., Dimakakos, E. P., Gibson, C. M., Lippi, G., Favaloro, E. J., Fareed, J., … Lip, G. Y. H. (2020). Global COVID-19 Thrombosis Collaborative Group, endorsed by the ISTH, NATF, ESVM, and the IUA, supported by the ESC Working Group on Pulmonary Circulation and Right Ventricular Function. COVID-19 and thrombotic or thromboembolic disease: Implications for prevention, antithrombotic therapy, and follow-up: JACC state-of-the-art review. Journal of the American College of Cardiology, 75(23), 2950–2973. https://doi.org/https://doi.org/10.1016/j.jacc.2020.04.031
   PubMed Web of Science ®Google Scholar
• Chen, N., Zhou, M., Dong, X., Qu, J., Gong, F., Han, Y., Qiu, Y., Wang, J., Liu, Y., Wei, Y., Xia, J., Yu, T., Zhang, X., & Zhang, L. (2020). Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study. The Lancet, 395(10223), 507–513. https://doi.org/https://doi.org/10.1016/S0140-6736(20)30211-7
   PubMed Web of Science ®Google Scholar
• Clinical Trials. (2020). https://clinicaltrials.gov.
   Google Scholar
• Diurno, F., Numis, F. G., Porta, G., Cirillo, F., Maddaluno, S., Ragozzino, A., De Negri, P., Di Gennaro, C., Pagano, A., Allegorico, E., Bressy, L., Bosso, G., Ferrara, A., Serra, C., Montisci, A., D’Amico, M., Schiano Lo Morello, S., Di Costanzo, G., Tucci, A. G., … Facchini, G. (2020). Eculizumab treatment in patients with COVID-19: Preliminary results from real life ASL Napoli 2 Nord experience. European Review for Medical and Pharmacological Sciences, 24(7), 4040–4047. https://doi.org/https://doi.org/10.26355/eurrev_202004_20875
   PubMed Web of Science ®Google Scholar
• Escher, R., Breakey, N., & Lämmle, B. (2020). Severe COVID-19 infection associated with endothelial activation. Thrombosis Research, 190, 62. https://doi.org/https://doi.org/10.1016/j.thromres.2020.04.014
   PubMed Web of Science ®Google Scholar
• Fromell, K., Adler, A., Åman, A., Manivel, V. A., Huang, S., Dührkop, C., Sandholm, K., Ekdahl, K. N., & Nilsson, B. (2020). Assessment of the role of C3(H2O) in the alternative pathway. Frontiers in Immunology, 11, 530. https://doi.org/https://doi.org/10.3389/fimmu.2020.00530
   PubMed Web of Science ®Google Scholar
• Gasque, P., Singhrao, S. K., Neal, J. W., Götze, O., & Morgan, B. P. (1997). Expression of the receptor for complement C5a (CD88) is up-regulated on reactive astrocytes, microglia, and endothelial cells in the inflamed human central nervous system. The American Journal of Pathology, 150(1), 31–41.
   PubMed Web of Science ®Google Scholar
• Guan, W.-J., Ni, Z.-Y., Hu, Y., Liang, W.-H., Ou, C.-Q., He, J.-X., Liu, L., Shan, H., Lei, C.-L., Hui, D. S. C., Du, B., Li, L.-J., Zeng, G., Yuen, K.-Y., Chen, R.-C., Tang, C.-L., Wang, T., Chen, P.-Y., Xiang, J., … Zhong, N.-S. (2020). Clinical characteristics of coronavirus disease 2019 in China. The New England Journal of Medicne, 382(18), 1708–1720. https://doi.org/https://doi.org/10.1056/NEJMoa2002032
   PubMed Web of Science ®Google Scholar
• Jodele, S., Medvedovic, M., Luebbering, N., Chen, J., Dandoy, C. E., Laskin, B. L., & Davies, S. M. (2020). Interferon-complement loop in transplant-associated thrombotic microangiopathy. Blood Advances, 4(6), 1166–1177. https://doi.org/https://doi.org/10.1182/bloodadvances.2020001515
   PubMed Web of Science ®Google Scholar
• Hamming, I., Timens, W., Bulthuis, M. L., Lely, A. T., Navis, G., & van Goor, H. (2004). Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. The Journal of Pathology, 203(2), 631–637. https://doi.org/https://doi.org/10.1002/path.1570
   PubMed Web of Science ®Google Scholar
• Han, H., Yang, L., Liu, R., Liu, F., Wu, K. L., Li, J., Liu, X. H., & Zhu, C. L. (2020). Prominent changes in blood coagulation of patients with SARS-CoV-2 infection. Clinical Chemistry and Laboratory Medicine (CCLM), 58(7), 1116–1120. https://doi.org/https://doi.org/10.1515/cclm-2020-0188
   Google Scholar
• Helms, J., Tacquard, C., Severac, F., Leonard-Lorant, I., Ohana, M., Delabranche, X., Merdji, H., Clere-Jehl, R., Schenck, M., Fagot Gandet, F., Fafi-Kremer, S., Castelain, V., Schneider, F., Grunebaum, L., Anglés-Cano, E., Sattler, L., Mertes, P. M., & Meziani, F. (2020). High risk of thrombosis in patients with severe SARS-CoV-2 infection: A multicenter prospective cohort study. Intensive Care Medicine, 46(6), 1089–1098. https://doi.org/https://doi.org/10.1007/s00134-020-06062-x
   PubMed Web of Science ®Google Scholar
• Hendaus, M. A., & Jomha, F. A. (2020). Covid-19 induced superimposed bacterial infection. Journal of Biomolecular Structure & Dynamics, 1–7. Advance online publication. https://doi.org/https://doi.org/10.1080/07391102.2020.1772110
   Google Scholar
• Henry, B. M., Vikse, J., Benoit, S., Favaloro, E. J., & Lippi, G. (2020). Hyperinflammation and derangement of renin-angiotensin-aldosterone system in COVID-19: A novel hypothesis for clinically suspected hypercoagulopathy and microvascular immunothrombosis. Clinica Chimica Acta; International Journal of Clinical Chemistry, 507, 167–173. https://doi.org/https://doi.org/10.1016/j.cca.2020.04.027
   PubMed Web of Science ®Google Scholar
• Huang, C., Wang, Y., Li, X., Ren, L., Zhao, J., Hu, Y., Zhang, L., Fan, G., Xu, J., Gu, X., Cheng, Z., Yu, T., Xia, J., Wei, Y., Wu, W., Xie, X., Yin, W., Li, H., Liu, M., … Cao, B. (2020). Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. The Lancet, 395(10223), 497–506. https://doi.org/https://doi.org/10.1016/S0140-6736(20)30183-5 https://doi.org/https://doi.org/10.1016/S0140-6736(20)30183-5
   PubMed Web of Science ®Google Scholar
• Ip, W. K., Chan, K. H., Law, H. K., Tso, G. H., Kong, E. K., Wong, W. H., To, Y. F., Yung, R. W., Chow, E. Y., Au, K. L., Chan, E. Y., Lim, W., Jensenius, J. C., Turner, M. W., Peiris, J. S., & Lau, Y. L. (2005). Mannose-binding lectin in severe acute respiratory syndrome coronavirus infection. The Journal of Infectious Diseases, 191(10), 1697–1704. https://doi.org/https://doi.org/10.1086/429631
   PubMed Web of Science ®Google Scholar
• Kim, H., & Conway, E. M. (2019). Platelets and complement cross-talk in early atherogenesis. Frontiers in Cardiovascular Medicine, 6, 131. https://doi.org/https://doi.org/10.3389/fcvm.2019.00131
   PubMed Web of Science ®Google Scholar
• Lee, A. Y. Y., Connors, J. M., & Baumann Kreuziger, L. (2020). Online COVID-19 resources of the American Society of Hematology. https://www.hematology.org/covid-19/covid-19-and-coagulopathy
   Google Scholar
• Legendre, C. M., Licht, C., Muus, P., Greenbaum, L. A., Babu, S., Bedrosian, C., Bingham, C., Cohen, D. J., Delmas, Y., Douglas, K., Eitner, F., Feldkamp, T., Fouque, D., Furman, R. R., Gaber, O., Herthelius, M., Hourmant, M., Karpman, D., Lebranchu, Y., … Loirat, C. (2013). Terminal complement inhibitor eculizumab in atypical hemolytic-uremic syndrome. New England Journal of Medicine, 368(23), 2169–2181. https://doi.org/https://doi.org/10.1056/NEJMoa1208981
   PubMed Web of Science ®Google Scholar
• Li, J. P., & Vlodavsky, I. (2009). Heparin, heparan sulfate and heparanase in inflammatory reactions. Thrombosis and Haemostasis, 102(5), 823–828. https://doi.org/https://doi.org/10.1160/TH09-02-0091
   PubMed Web of Science ®Google Scholar
• Luo, W., Yu, H., Gou, J., Li, X., Sun, Y., Li, J., & Liu, L. (2020). Clinical pathology of critical patient with Novel Coronavirus pneumonia (COVID-19). Preprints, 2020, 2020020407.
   Google Scholar
• Magro, C., Mulvey, J. J., Berlin, D., Nuovo, G., Salvatore, S., Harp, J., Baxter-Stoltzfus, A., & Laurence, J. (2020). Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: A report of five cases. Translational Research, 220, 1–13. https://doi.org/https://doi.org/10.1016/j.trsl.2020.04.007
   PubMed Web of Science ®Google Scholar
• Morgan, B. P., Boyd, C., & Bubeck, D. (2017). Molecular cell biology of complement membrane attack. Seminars in Cell & Developmental Biology, 72, 124–132. https://doi.org/https://doi.org/10.1016/j.semcdb.2017.06.009
   PubMed Web of Science ®Google Scholar
• Marini, J. J., & Gattinoni, L. (2020). Management of COVID-19 respiratory distress. JAMA, 323(22), 2329. https://doi.org/https://doi.org/10.1001/jama.2020.6825
   PubMed Web of Science ®Google Scholar
• McCullough, R. L., McMullen, M. R., Poulsen, K. L., Kim, A., Medof, M. E., & Nagy, L. E. (2018). Anaphylatoxin receptors C3aR and C5aR1 are important factors that influence the impact of ethanol on the adipose secretome. Frontiers in Immunology, 9, 2133. https://doi.org/https://doi.org/10.3389/fimmu.2018.02133
   PubMed Web of Science ®Google Scholar
• Noris, M., Benigni, A., & Remuzzi, G. (2020). The case of complement activation in COVID-19 multiorgan impact. Kidney International, 98(2), 314–322. https://doi.org/https://doi.org/10.1016/j.kint.2020.05.013
   PubMed Web of Science ®Google Scholar
• Olson, S. R., Lu, E., Sulpizio, E., Shatzel, J. J., Rueda, J. F., & DeLoughery, T. G. (2018). When to stop eculizumab in complement-mediated thrombotic microangiopathies. American Journal of Nephrology, 48(2), 96–107. https://doi.org/https://doi.org/10.1159/000492033
   PubMed Web of Science ®Google Scholar
• Pant, S., Singh, M., Ravichandiran, V., Murty, U., & Srivastava, H. K. (2020). Peptide-like and small-molecule inhibitors against Covid-19. Journal of Biomolecular Structure & Dynamics, 1–10. https://doi.org/https://doi.org/10.1080/07391102.2020.1757510
   Google Scholar
• Pittock, S. J., Berthele, A., Fujihara, K., Kim, H. J., Levy, M., Palace, J., Nakashima, I., Terzi, M., Totolyan, N., Viswanathan, S., Wang, K. C., Pace, A., Fujita, K. P., Armstrong, R., & Wingerchuk, D. M. (2019). Eculizumab in Aquaporin-4-positive neuromyelitis optica spectrum disorder. New England Journal of Medicine, 381(7), 614–625. https://doi.org/https://doi.org/10.1056/NEJMoa1900866
   PubMed Web of Science ®Google Scholar
• Risitano, A. M., Mastellos, D. C., Huber-Lang, M., Yancopoulou, D., Garlanda, C., Ciceri, F., & Lambris, J. D. (2020). Complement as a target in COVID-19? Nature Reviews. Immunology, 20(6), 343–344. https://doi.org/https://doi.org/10.1038/s41577-020-0320-7
   PubMed Web of Science ®Google Scholar
• Roumenina, L. T., Rayes, J., Frimat, M., & Fremeaux-Bacchi, V. (2016). Endothelial cells: Source, barrier, and target of defensive mediators. Immunological Reviews, 274(1), 307–329. https://doi.org/https://doi.org/10.1111/imr.12479
   PubMed Web of Science ®Google Scholar
• Soy, M., Keser, G., Atagündüz, P., Tabak, F., Atagündüz, I., & Kayhan, S. (2020). Cytokine storm in COVID-19: Pathogenesis and overview of anti-inflammatory agents used in treatment. Clinical Rheumatology, 39(7), 2085–2094. https://doi.org/https://doi.org/10.1007/s10067-020-05190-5
   PubMed Web of Science ®Google Scholar
• Susen, S., Tacquard, C. A., Godon, A., Mansour, A., Garrigue, D., Nguyen, P., Godier, A., Testa, S., Levy, J. H., Albaladejo, P., & Gruel, Y. (2020). Prevention of thrombotic risk in hospitalized patients with COVID-19 and hemostasis monitoring. Critical Care, 24(1), 364. https://doi.org/https://doi.org/10.1186/s13054-020-03000-7
   PubMed Web of Science ®Google Scholar
• Tang, N., Li, D., Wang, X., & Sun, Z. (2020). Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. Journal of Thrombosis and Haemostasis, 18(4), 844–847. https://doi.org/https://doi.org/10.1111/jth.14768
   PubMed Web of Science ®Google Scholar
• Thachil, J., Tang, N., Gando, S., Falanga, A., Cattaneo, M., Levi, M., Clark, C., & Iba, T. (2020). ISTH interim guidance on recognition and management of coagulopathy in COVID-19. Journal of Thrombosis and Haemostasis: JTH, 18(5), 1023–1026. https://doi.org/https://doi.org/10.1111/jth.14810
   PubMed Web of Science ®Google Scholar
• Thiel, S., Kolev, M., Degn, S., Steffensen, R., Hansen, A. G., Ruseva, M., & Jensenius, J. C. (2009). Polymorphisms in mannan-binding lectin (MBL)-associated serine protease 2 affect stability, binding to MBL, and enzymatic activity. Journal of Immunology (Baltimore, MD: 1950), 182(5), 2939–2947. https://doi.org/https://doi.org/10.4049/jimmunol.0802053
   PubMed Web of Science ®Google Scholar
• van Hinsbergh, V. W. (2012). Endothelium-role in regulation of coagulation and inflammation. Seminars in Immunopathology, 34(1), 93–106. https://doi.org/https://doi.org/10.1007/s00281-011-0285-5
   PubMed Web of Science ®Google Scholar
• Wang, D., Hu, B., Hu, C., Zhu, F., Liu, X., Zhang, J., Wang, B., Xiang, H., Cheng, Z., Xiong, Y., Zhao, Y., Li, Y., Wang, X., & Peng, Z. (2020). Clinical characteristics of 138 hospitalized patients with 2019 Novel Coronavirus-infected pneumonia in Wuhan, China. JAMA, 323(11), 1061–1069. https://doi.org/https://doi.org/10.1001/jama.2020.1585
   PubMed Web of Science ®Google Scholar
• Wang, J., Hajizadeh, N., Moore, E. E., McIntyre, R. C., Moore, P. K., Veress, L. A., Yaffe, M. B., Moore, H. B., & Barrett, C. D. (2020). Tissue plasminogen activator (tPA) treatment for COVID-19 associated acute respiratory distress syndrome (ARDS): A case series. Journal of Thrombosis and Haemostasis: JTH, 18(7), 1752–1755. https://doi.org/https://doi.org/10.1111/jth.14828
   PubMed Web of Science ®Google Scholar
• Wu, C., Chen, X., Cai, Y., Xia, J., Zhou, X., Xu, S., Huang, H., Zhang, L., Zhou, X., Du, C., Zhang, Y., Song, J., Wang, S., Chao, Y., Yang, Z., Xu, J., Zhou, X., Chen, D., Xiong, W., … Song, Y. (2020). Risk factors associated with acute respiratory distress syndrome and death in patients with Coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Internal Medicine, 180(7), 911–934. https://doi.org/https://doi.org/10.1001/jamainternmed.2020.0994
   PubMed Web of Science ®Google Scholar
• Young, E. (2008). The anti-inflammatory effects of heparin and related compounds. Thrombosis Research, 122(6), 743–752. https://doi.org/https://doi.org/10.1016/j.thromres.2006.10.026
   PubMed Web of Science ®Google Scholar
• Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G. F., & Tan, W. (2020). A novel coronavirus from patients with pneumonia in China, 2019. The New England Journal of Medicine, 382(8), 727–733. https://doi.org/https://doi.org/10.1056/NEJMoa2001017
   PubMed Web of Science ®Google Scholar