Mechanical Ventilation with Moderate Tidal Volume Exacerbates Extrapulmonary Sepsis-Induced Lung Injury via IL33-WISP1 Signaling Pathway.
Animals
CCN Intercellular Signaling Proteins
/ physiology
Disease Models, Animal
Interleukin-33
/ physiology
Male
Mice
Mice, Inbred C57BL
Proto-Oncogene Proteins
/ physiology
Respiration, Artificial
/ adverse effects
Sepsis
/ complications
Signal Transduction
/ physiology
Tidal Volume
/ physiology
Ventilator-Induced Lung Injury
/ etiology
Journal
Shock (Augusta, Ga.)
ISSN: 1540-0514
Titre abrégé: Shock
Pays: United States
ID NLM: 9421564
Informations de publication
Date de publication:
01 09 2021
01 09 2021
Historique:
pubmed:
5
1
2021
medline:
9
3
2022
entrez:
4
1
2021
Statut:
ppublish
Résumé
IL-33 and WNT1-inducible secreted protein (WISP1) play central roles in acute lung injury (ALI) induced by mechanical ventilation with moderate tidal volume (MTV) in the setting of sepsis. Here, we sought to determine the inter-relationship between IL-33 and WISP1 and the associated signaling pathways in this process.We used a two-hit model of cecal ligation puncture (CLP) followed by MTV ventilation (4 h 10 mL/kg) in wild-type, IL-33-/- or ST2-/- mice or wild-type mice treated with intratracheal antibodies to WISP1. Macrophages (Raw 264.7 and alveolar macrophages from wild-type or ST2-/- mice) were used to identify specific signaling components.CLP + MTV resulted in ALI that was partially sensitive to genetic ablation of IL-33 or ST2 or antibody neutralization of WISP1. Genetic ablation of IL-33 or ST2 significantly prevented ALI after CLP + MTV and reduced levels of WISP1 in the circulation and bronchoalveolar lung fluid. rIL-33 increased WISP1 in alveolar macrophages in an ST2, PI3K/AKT, and ERK dependent manner. This WISP1 upregulation and WNT β-catenin activation were sensitive to inhibition of the β-catenin/TCF/CBP/P300 nuclear pathway.We show that IL-33 drives WISP1 upregulation and ALI during MTV in CLP sepsis. The identification of this relationship and the associated signaling pathways reveals a number of possible therapeutic targets to prevent ALI in ventilated sepsis patients.
Identifiants
pubmed: 33394970
doi: 10.1097/SHK.0000000000001714
pii: 00024382-202109000-00017
doi:
Substances chimiques
CCN Intercellular Signaling Proteins
0
CCN4 protein, mouse
0
Il33 protein, mouse
0
Interleukin-33
0
Proto-Oncogene Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
461-472Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM108639
Pays : United States
Informations de copyright
Copyright © 2021 by the Shock Society.
Déclaration de conflit d'intérêts
The authors report no conflicts of interest.
Références
Bellani G, Laffey JG, Pham T, Fan E, Brochard L, Esteban A, Gattinoni L, van Haren F, Larsson A, McAuley DF, et al. Epidemiology, patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries. JAMA 315 (8):788–800, 2016.
Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med 353 (16):1685–1693, 2005.
Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest 122 (8):2731–2740, 2012.
Slutsky AS, Ranieri VM. Ventilator-induced lung injury. N Engl J Med 369 (22):2126–2136, 2013.
Englert JA, Bobba C, Baron RM. Integrating molecular pathogenesis and clinical translation in sepsis-induced acute respiratory distress syndrome. JCI Insight 4 (2):e124061, 2019.
Ding X, Tong Y, Jin S, Chen Z, Li T, Billiar TR, Pitt BR, Li Q, Zhang LM. Mechanical ventilation enhances extrapulmonary sepsis-induced lung injury: role of WISP1-αvβ5 integrin pathway in TLR4-mediated inflammation and injury. Crit Care 22 (1):302, 2018.
Ding X, Jin S, Shao Z, Xu L, Yu Z, Tong Y, Chen Z, Turnquist H, Pitt BR, Billiar TR, et al. The IL-33-ST2 pathway contributes to ventilator-induced lung injury in septic mice in a tidal volume-dependent manner. Shock 52 (3):e1–e11, 2019.
Iskander KN, Craciun FL, Stepien DM, Duffy ER, Kim J, Moitra R, Vaickus LJ, Osuchowski MF, Remick DG. Cecal ligation and puncture-induced murine sepsis does not cause lung injury. Crit Care Med 41 (1):159–170, 2013.
Chen Z, Ding X, Jin S, Pitt B, Zhang L, Billiar T, Li Q. WISP1-αvβ3 integrin signaling positively regulates TLR-triggered inflammation response in sepsis induced lung injury. Sci Rep 6:28841, 2016.
Li HH, Li Q, Liu P, Liu Y, Li J, Wasserloos K, Chao W, You M, Oury TD, Chhinder S, et al. WNT1-inducible signaling pathway protein 1 contributes to ventilator-induced lung injury. Am J Respir Cell Mol Biol 47 (4):528–535, 2012.
Altemeier WA, Matute-Bello G, Frevert CW, Kawata Y, Kajikawa O, Martin TR, Glenny RW. Mechanical ventilation with moderate tidal volumes synergistically increases lung cytokine response to systemic endotoxin. Am J Physiol Lung Cell Mol Physiol 287 (3):L533–542, 2004.
Brégeon F, Delpierre S, Chetaille B, Kajikawa O, Martin TR, Autillo-Touati A, Jammes Y, Pugin J. Mechanical ventilation affects lung function and cytokine production in an experimental model of endotoxemia. Anesthesiology 102 (2):331–339, 2005.
Lee JS, Su X, Rackley C, Matthay MA, Gupta N. Priming with endotoxin increases acute lung injury in mice by enhancing the severity of lung endothelial injury. Anat Rec (Hoboken) 294 (1):165–172, 2011.
Müller-Redetzky HC, Will D, Hellwig K, Kummer W, Tschernig T, Pfeil U, Paddenberg R, Menger MD, Kershaw O, Gruber AD, et al. Mechanical ventilation drives pneumococcal pneumonia into lung injury and sepsis in mice: protection by adrenomedullin. Crit Care 18 (2):R73, 2014.
Kuiper JW, Plötz FB, Groeneveld AJ, Haitsma JJ, Jothy S, Vaschetto R, Zhang H, Slutsky AS. High tidal volume mechanical ventilation-induced lung injury in rats is greater after acid instillation than after sepsis-induced acute lung injury, but does not increase systemic inflammation: an experimental study. BMC Anesthesiol 11:26, 2011.
Nin N, Lorente JA, Fernández-Segoviano P, De Paula M, Ferruelo A, Esteban A. High-tidal volume ventilation aggravates sepsis-induced multiorgan dysfunction in a dexamethasone-inhibitable manner. Shock 31 (4):429–434, 2009.
Nakamura T, Malloy J, McCaig L, Yao LJ, Joseph M, Lewis J, Veldhuizen R. Mechanical ventilation of isolated septic rat lungs: effects on surfactant and inflammatory cytokines. J Appl Physiol (1985) 91 (2):811–820, 2001.
Uematsu S, Engelberts D, Peltekova V, Otulakowski G, Post M, Kavanagh BP. Dissociation of inflammatory mediators and function: experimental lung injury in nonpulmonary sepsis. Crit Care Med 41 (1):151–158, 2013.
Yehya N, Xin Y, Oquendo Y, Cereda M, Rizi RR, Margulies SS. Cecal ligation and puncture accelerates development of ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol 308 (5):L443–451, 2015.
Perbal B, Tweedie S, Bruford E. The official unified nomenclature adopted by the HGNC calls for the use of the acronyms, CCN1–6, and discontinuation in the use of CYR61, CTGF, NOV and WISP 1–3 respectively. J Cell Commun Signal 12 (4):625–629, 2018.
Xu H, Xu J, Xu L, Jin S, Turnquist HR, Hoffman R, Loughran P, Billiar TR, Deng M. Interleukin-33 contributes to ILC2 activation and early inflammation-associated lung injury during abdominal sepsis. Immunol Cell Biol 96 (9):935–947, 2018.
Chang J, Xia Y, Wasserloos K, Deng M, Blose KJ, Vorp DA, Turnquist HR, Billiar TR, Pitt BA, Zhang MZ, et al. Cyclic stretch induced IL-33 production through HMGB1/TLR-4 signaling pathway in murine respiratory epithelial cells. PLoS One 12 (9):e0184770, 2017.
Sanada S, Hakuno D, Higgins LJ, Schreiter ER, McKenzie AN, Lee RT. IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system. J Clin Invest 117 (6):1538–1549, 2007.
Heise RL, Stober V, Cheluvaraju C, Hollingsworth JW, Garantziotis S. Mechanical stretch induces epithelial-mesenchymal transition in alveolar epithelia via hyaluronan activation of innate immunity. J Biol Chem 286 (20):17435–17444, 2011.
Yu Z, Wang T, Zhang L, Yang X, Li Q, Ding X. WISP1 and TLR4 on macrophages contribute to ventilator-induced lung injury. Inflammation 43 (2):425–432, 2020.
Li J, Zhang L, Chen X, Chen D, Hua X, Bian F, Deng R, Lu F, Li Z, Pflugfelder SC, et al. Pollen/TLR4 innate immunity signaling initiates IL-33/ST2/Th2 pathways in allergic inflammation. Sci Rep 6:36150, 2016.
Oboki K, Ohno T, Kajiwara N, Arae K, Morita H, Ishii A, Nambu A, Abe T, Kiyonari H, Matsumoto K, et al. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc Natl Acad Sci U S A 107 (43):18581–18586, 2010.
Wu J, Yan Z, Schwartz DE, Yu J, Malik AB, Hu G. Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol 190 (7):3590–3599, 2013.
Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10 (12):1443–1454, 1996.
Liu Q, Dwyer GK, Zhao Y, Li H, Mathews LR, Chakka AB, Chandran UR, Demetris JA, Alcorn JF, Robinson KM, et al. IL-33-mediated IL-13 secretion by ST2+ Tregs controls inflammation after lung injury. JCI Insight 4 (6):e123919, 2019.
Ding X, Wang X, Zhao X, Jin S, Tong Y, Ren H, Chen Z, Li Q. RGD peptides protects against acute lung injury in septic mice through Wisp1-integrin β6 pathway inhibition. Shock 43 (4):352–360, 2015.
Villar J, Cabrera NE, Casula M, Valladares F, Flores C, López-Aguilar J, Blanch L, Zhang H, Kacmarek RM, Slutsky AS. WNT/β-catenin signaling is modulated by mechanical ventilation in an experimental model of acute lung injury. Intensive Care Med 37 (7):1201–1209, 2011.
Dejager L, Pinheiro I, Dejonckheere E, Libert C. Cecal ligation and puncture: the gold standard model for polymicrobial sepsis? Trends Microbiol 19 (4):198–208, 2011.
Gurbuz I, Chiquet-Ehrismann R. CCN4/WISP1 (WNT1 inducible signaling pathway protein 1): a focus on its role in cancer. Int J Biochem Cell Biol 62:142–146, 2015.
Blom AB, Brockbank SM, van Lent PL, van Beuningen HM, Geurts J, Takahashi N, van der Kraan PM, van de Loo FA, Schreurs BW, Clements K, et al. Involvement of the Wnt signaling pathway in experimental and human osteoarthritis: prominent role of Wnt-induced signaling protein 1. Arthritis Rheum 60 (2):501–512, 2009.
Königshoff M, Kramer M, Balsara N, Wilhelm J, Amarie OV, Jahn A, Rose F, Fink L, Seeger W, Schaefer L, et al. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest 119 (4):772–787, 2009.
Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23 (5):479–490, 2005.
Liew FY, Girard JP, Turnquist HR. Interleukin-33 in health and disease. Nat Rev Immunol 16 (11):676–689, 2016.
Salmond RJ, Mirchandani AS, Besnard AG, Bain CC, Thomson NC, Liew FY. IL-33 induces innate lymphoid cell-mediated airway inflammation by activating mammalian target of rapamycin. J Allergy Clin Immunol 130 (5):1159–1166, 2012.
Yang SH, Lin JC, Wu SY, Huang KL, Jung F, Ma MC, Wang Hsu GS, Jow GM. Membrane translocation of IL-33 receptor in ventilator induced lung injury. PLoS One 10 (3):e0121391, 2015.
Vaneker M, Joosten LA, Heunks LM, Snijdelaar DG, Halbertsma FJ, van Egmond J, Netea MG, van der Hoeven JG, Scheffer GJ. Low-tidal-volume mechanical ventilation induces a toll-like receptor 4-dependent inflammatory response in healthy mice. Anesthesiology 109 (3):465–472, 2008.
Li H, Su X, Yan X, Wasserloos K, Chao W, Kaynar AM, Liu ZQ, Leikauf GD, Pitt BR, Zhang LM. Toll-like receptor 4-myeloid differentiation factor 88 signaling contributes to ventilator-induced lung injury in mice. Anesthesiology 113 (3):619–629, 2010.
Xia YF, Chang J, Yang JF, Ouyang W, Pitt B, Billiar T, Zhang LM. Non-canonical Wnt signaling contributes to ventilator-induced lung injury through upregulation of WISP1 expression. Int J Mol Med 43 (3):1217–1228, 2019.
Ding Q, Xia W, Liu JC, Yang JY, Lee DF, Xia J, Bartholomeusz G, Li Y, Pan Y, Li Z, et al. Erk associates with and primes GSK-3beta for its inactivation resulting in upregulation of beta-catenin. Mol Cell 19 (2):159–170, 2005.
Monick MM, Carter AB, Robeff PK, Flaherty DM, Peterson MW, Hunninghake GW. Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumulation and transcriptional activity of beta-catenin. J Immunol 166 (7):4713–4720, 2001.
Li C, Li H, Jiang Z, Zhang T, Wang Y, Li Z, Wu Y, Ji S, Xiao S, Ryffel B, et al. Interleukin-33 increases antibacterial defense by activation of inducible nitric oxide synthase in skin. PLoS Pathog 10 (2):e1003918, 2014.
Wang H, Zhang R, Wen S, McCafferty DM, Beck PL, MacNaughton WK. Nitric oxide increases Wnt-induced secreted protein-1 (WISP-1/CCN4) expression and function in colitis. J Mol Med 87 (4):435–445, 2009.
Nascimento DC, Melo PH, Piñeros AR, Ferreira RG, Colón DF, Donate PB, Castanheira FV, Gozzi A, Czaikoski PG, Niedbala W, et al. IL-33 contributes to sepsis-induced long-term immunosuppression by expanding the regulatory T cell population. Nat Commun 8:14919, 2017.
Quiros M, Nishio H, Neumann PA, Siuda D, Brazil JC, Azcutia V, Hilgarth R, O’Leary MN, Garcia-Hernandez V, Leoni G, et al. Macrophage-derived IL-10 mediates mucosal repair by epithelial WISP-1 signaling. J Clin Invest 127 (9):3510–3520, 2017.