Inflammation and intussusceptive angiogenesis in COVID-19: everything in and out of flow

Maximilian Ackermann, Steven J Mentzer, Martin Kolb, Danny Jonigk, Maximilian Ackermann, Steven J Mentzer, Martin Kolb, Danny Jonigk

Abstract

Inflammation and intussusceptive angiogenesis in COVID-19 https://bit.ly/30lLh8K

Conflict of interest statement

Conflict of interest: M. Ackermann has nothing to disclose. Conflict of interest: S.J. Mentzer has nothing to disclose. Conflict of interest: M. Kolb reports grants and personal fees from Roche, Boehringer Ingelheim and Prometic, grants from GSK, Respivert, Alkermes, Pharmaxis and Canadian Institute for Health Research, personal fees from Genoa, Indalo, Third Pole and Pieris, outside the submitted work. Conflict of interest: D. Jonigk has nothing to disclose.

Figures

FIGURE 1
FIGURE 1
a) Schematic of pulmonary endothelialitis, thrombosis, and intussusceptive angiogenesis in coronavirus disease 2019 (COVID-19). SARS-CoV-2: severe acute respiratory syndrome coronavirus 2. b) Intussusceptive angiogenesis is a morphogenetic process which rapidly expands the vascular plexus. c) Transmission electron micrograph of lung tissue of a deceased COVID-19 patient highlights the formation of an intussusceptive pillar (red arrowheads) which spans the lumen of the vascular walls. rbc: red blood cells. d) A disrupted vascularity with distorted vessels and intussusceptive pillars (blue arrowheads) is observed in COVID-19 lungs, as depicted as scanning electron micrograph of microvascular corrosion casts of COVID-19 autopsies.

References

    1. Ackermann M, Verleden SE, Kuehnel M, et al. . Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med 2020; 383: 120–128. doi:10.1056/NEJMoa2015432.
    1. Cardot-Leccia N, Hubiche T, Dellamonica J, et al. . Pericyte alteration sheds light on micro-vasculopathy in COVID-19 infection. Intensive Care Med 2020; 46: 1777–1778. doi:10.1007/s00134-020-06147-7
    1. Huertas A, Montani D, Savale L, et al. . Endothelial cell dysfunction: a major player in SARS-CoV-2 infection (COVID-19)? Eur Respir J 2020; 56: 2001634. doi:10.1183/13993003.01634-2020
    1. Goldsmith CS, Miller SE, Martines RB, et al. . Electron microscopy of SARS-CoV-2: a challenging task. Lancet 2020; 395: e99. doi:10.1016/S0140-6736(20)31188-0.
    1. Ackermann M, Mentzer SJ, Jonigk D. Pulmonary vascular pathology in Covid-19. Reply. N Engl J Med 2020; 383: 888–889. doi:10.1056/NEJMc2022068.
    1. Martines RB, Ritter JM, Matkovic E, et al. . Pathology and pathogenesis of SARS-CoV-2 associated with fatal coronavirus disease, United States. Emerging Infect Dis 2020; 26: 2005–2015. doi:10.3201/eid2609.202095
    1. Bradley BT, Maioli H, Johnston R, et al. . Histopathology and ultrastructural findings of fatal COVID-19 infections in Washington State: a case series. Lancet 2020; 396: 320–332. doi:10.1016/S0140-6736(20)31305-2.
    1. Price LC, McCabe C, Garfield B, et al. . Thrombosis and COVID-19 pneumonia: the clot thickens! Eur Respir J 2020; 56: 2001608. doi:10.1183/13993003.01608-2020
    1. Leppkes M, Knopf J, Naschberger E, et al. . Vascular occlusion by neutrophil extracellular traps in COVID-19. EBioMedicine 2020; 58: 102925. doi:10.1016/j.ebiom.2020.102925.
    1. Sugiyama MG, Gamage A, Zyla R, et al. . Influenza virus infection induces platelet-endothelial adhesion which contributes to lung injury. J Virol 2016; 90: 1812–1823. doi:10.1128/JVI.02599-15
    1. Ackermann M, Wagner WL, Rellecke P, et al. . Parvovirus B19-induced angiogenesis in fulminant myocarditis. Eur Heart J 2020; 41: 1309. doi:10.1093/eurheartj/ehaa092
    1. Gattinoni L, Coppola S, Cressoni M, et al. . COVID19 does not lead to a typical acute respiratory distress syndrome. Am J Respir Crit Care Med 2020; 201: 1299–1300. doi:10.1164/rccm.202003-0817LE
    1. Lee GS, Filipovic N, Miele LF, et al. . Blood flow shapes intravascular pillar geometry in the chick chorioallantoic membrane. J Angiogenes Res 2010; 2: 11. doi:10.1186/2040-2384-2-11
    1. Filipovic N, Tsuda A, Lee GS, et al. . Computational flow dynamics in a geometric model of intussusceptive angiogenesis. Microvasc Res 2009; 78: 286–293. doi:10.1016/j.mvr.2009.08.004
    1. Ravnic DJ, Konerding MA, Tsuda A, et al. . Structural adaptations in the murine colon microcirculation associated with hapten-induced inflammation. Gut 2007; 56: 518–523. doi:10.1136/gut.2006.101824
    1. Jain RK, Tong RT, Munn LL. Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res 2007; 67: 2729–2735. doi:10.1158/0008-5472.CAN-06-4102
    1. Miele LF, Turhan A, Lee GS, et al. . Blood flow patterns spatially associated with platelet aggregates in murine colitis. Anat Rec (Hoboken) 2009; 292: 1143–1153. doi:10.1002/ar.20954
    1. Napoli C, Ignarro LJ. Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res 2009; 32: 1103–1108. doi:10.1007/s12272-009-1801-1.
    1. von Andrian UH, Mackay CR. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000; 343: 1020–1034. doi:10.1056/NEJM200010053431407
    1. Li X, Abdi K, Rawn J, et al. . LFA-1 and L-selectin regulation of recirculating lymphocyte tethering and rolling on lung microvascular endothelium. Am J Respir Cell Mol Biol 1996; 14: 398–406. doi:10.1165/ajrcmb.14.4.8600945
    1. Secomb TW, Konerding MA, West CA, et al. . Microangiectasias: structural regulators of lymphocyte transmigration. Proc Natl Acad Sci USA 2003; 100: 7231–7234. doi:10.1073/pnas.1232173100.
    1. Ranchoux B, Antigny F, Rucker-Martin C, et al. . Endothelial-to-mesenchymal transition in pulmonary hypertension. Circulation 2015; 131: 1006–1018. doi:10.1161/CIRCULATIONAHA.114.008750
    1. Andonegui G, Bonder CS, Green F, et al. . Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 2003; 111: 1011–1020. doi:10.1172/JCI16510
    1. Butchi N, Kapil P, Puntambekar S, et al. . Myd88 initiates early innate immune responses and promotes CD4 T cells during coronavirus encephalomyelitis. J Virol 2015; 89: 9299–9312. doi:10.1128/JVI.01199-15
    1. Khakpour S, Wilhelmsen K, Hellman J. Vascular endothelial cell Toll-like receptor pathways in sepsis. Innate Immun 2015; 21: 827–846. doi:10.1177/1753425915606525
    1. Ackermann M, Morse BA, Delventhal V, et al. . Anti-VEGFR2 and anti-IGF-1R-Adnectins inhibit Ewing's sarcoma A673-xenograft growth and normalize tumor vascular architecture. Angiogenesis 2012; 15: 685–695. doi:10.1007/s10456-012-9294-9
    1. Ackermann M, Houdek JP, Gibney BC, et al. . Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization. Angiogenesis 2014; 17: 541–551. doi:10.1007/s10456-013-9399-9.
    1. Mentzer SJ, Konerding MA. Intussusceptive angiogenesis: expansion and remodeling of microvascular networks. Angiogenesis 2014; 17: 499–509. doi:10.1007/s10456-014-9428-3.
    1. Dimova I, Karthik S, Makanya A, et al. . SDF-1/CXCR4 signalling is involved in blood vessel growth and remodelling by intussusception. J Cell Mol Med 2019; 23: 3916–3926. doi:10.1111/jcmm.14269
    1. Konerding MA, Turhan A, Ravnic DJ, et al. . Inflammation-induced intussusceptive angiogenesis in murine colitis. Anat Rec (Hoboken) 2010; 293: 849–857. doi:10.1002/ar.21110
    1. Ackermann M, Tsuda A, Secomb TW, et al. . Intussusceptive remodeling of vascular branch angles in chemically-induced murine colitis. Microvasc Res 2013; 87: 75–82. doi:10.1016/j.mvr.2013.02.002.
    1. Ackermann M, Stark H, Neubert L, et al. . Morphomolecular motifs of pulmonary neoangiogenesis in interstitial lung diseases. Eur Respir J 2020; 55: 1900933. doi:10.1183/13993003.00933-2019
    1. Yanagihara T, Jones KD. Demystifying morphomolecular alterations of vasculature in interstitial lung diseases. Eur Respir J 2020; 55: 1902446. doi:10.1183/13993003.02446-2019
    1. Ackermann M, Gaumann A, Mentzer SJ, et al. . Plexiform vasculopathy in chronic thromboembolic pulmonary hypertension. Am J Respir Crit Care Med 2017; 196: e48–e51. doi:10.1164/rccm.201703-0591IM
    1. Neubert L, Borchert P, Shin HO, et al. . Comprehensive three-dimensional morphology of neoangiogenesis in pulmonary veno-occlusive disease and pulmonary capillary hemangiomatosis. J Pathol Clin Res 2019; 5: 108–114. doi:10.1002/cjp2.125.
    1. Weatherald J, Dorfmüller P, Perros F, et al. . Pulmonary capillary haemangiomatosis: a distinct entity? Eur Respir Rev 2020; 29: 190168. doi:10.1183/16000617.0168-2019
    1. Bochenek ML, Rosinus NS, Lankeit M, et al. . From thrombosis to fibrosis in chronic thromboembolic pulmonary hypertension. Thromb Haemost 2017; 117: 769–783. doi:10.1160/TH16-10-0790
    1. Wuyts WA, Agostini C, Antoniou KM, et al. . The pathogenesis of pulmonary fibrosis: a moving target. Eur Respir J 2013; 41: 1207–1218. doi:10.1183/09031936.00073012.
    1. Probst CK, Montesi SB, Medoff BD, et al. . Vascular permeability in the fibrotic lung. Eur Respir J 2020; 56: 1900100. doi:10.1183/13993003.00100-2019
    1. Kreuter M, Wijsenbeek MS, Vasakova M, et al. . Unfavourable effects of medically indicated oral anticoagulants on survival in idiopathic pulmonary fibrosis. Eur Respir J 2016; 47: 1776–1784. doi:10.1183/13993003.02087-2015.

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する