Renin-angiotensin system in intestinal inflammation-Angiotensin inhibitors to treat inflammatory bowel diseases?
Angiotensin Receptor Antagonists
Angiotensin-Converting Enzyme Inhibitors
/ therapeutic use
Angiotensins
/ antagonists & inhibitors
Animals
Antihypertensive Agents
/ therapeutic use
Colitis
/ drug therapy
Drug Evaluation, Preclinical
Fibrosis
Humans
Hypertension
/ drug therapy
Inflammation
/ drug therapy
Inflammatory Bowel Diseases
/ complications
Mice
Models, Animal
Renin-Angiotensin System
/ drug effects
Retrospective Studies
ACE inhibitors
angiotensin II receptor blockers
colitis
inflammatory bowel diseases
renin-angiotensin system
Journal
Basic & clinical pharmacology & toxicology
ISSN: 1742-7843
Titre abrégé: Basic Clin Pharmacol Toxicol
Pays: England
ID NLM: 101208422
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
revised:
14
05
2021
received:
25
02
2021
accepted:
10
06
2021
pubmed:
16
6
2021
medline:
4
1
2022
entrez:
15
6
2021
Statut:
ppublish
Résumé
Inflammatory bowel diseases (IBDs) are chronic disorders of the gastrointestinal tract, which manifest in recurring gastrointestinal inflammation. The current treatment options of IBD are not curative and are lacking in aspects like prevention of fibrosis. New treatment options are needed to fulfil the unmet needs and provide alternatives to drugs with resistances and side effects. Drugs targeting the renin-angiotensin system (RAS), besides being antihypertensive, also possess anti-inflammatory and antifibrotic properties and could offer an inexpensive alternative to control inflammation and fibrosis in the gut. RAS inhibitors have been effective in preventing and alleviating colitis in preclinical studies, but available human data are still sparse. This review outlines the pathophysiological functions of RAS in the gut and summarizes preclinical studies utilizing pharmacological RAS inhibitors in the treatment of experimental colitis. We discuss the alterations in intestinal RAS and the available evidence of the benefits of RAS inhibitors for IBD patients. Retrospective studies comparing IBD patients using ACE inhibitors or angiotensin II receptor blockers have provided optimistic results regarding a milder disease course and fewer hospitalizations and corticosteroid use in patients using RAS inhibitors. Prospective studies are needed to evaluate the effectiveness of these promising medications in the treatment of IBD.
Substances chimiques
Angiotensin Receptor Antagonists
0
Angiotensin-Converting Enzyme Inhibitors
0
Angiotensins
0
Antihypertensive Agents
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
161-172Subventions
Organisme : Folkhälsan Research Foundation
Organisme : Helsinki University Central Hospital Research Funds
Organisme : Novo Nordisk Foundation
ID : OC0013659
Organisme : Wilhelm och Else Stockmanns Stiftelse
Organisme : Finska Läkaresällskapet, Einar och Karin Stroems Stiftelse
Informations de copyright
© 2021 The Authors. Basic & Clinical Pharmacology & Toxicology published by John Wiley & Sons Ltd on behalf of Nordic Association for the Publication of BCPT (former Nordic Pharmacological Society).
Références
Paul M, Poyan Mehr A, Kreutz R. Physiology of local renin-angiotensin systems. Physiol Rev. 2006;86(3):747-803. https://doi.org/10.1152/physrev.00036.2005
Fandriks L. The renin-angiotensin system and the gastrointestinal mucosa. Acta Physiol (Oxf). 2011;201(1):157-167. https://doi.org/10.1111/j.1748-1716.2010.02165.x
Hrenak J, Paulis L, Simko F. Angiotensin A/Alamandine/MrgD Axis: another clue to understanding cardiovascular pathophysiology. Int J Mol Sci. 2016;17(7). https://doi.org/10.3390/ijms17071098
Nehme A, Zibara K. Cellular distribution and interaction between extended renin-angiotensin-aldosterone system pathways in atheroma. Atherosclerosis. 2017;263:334-342. https://doi.org/10.1016/j.atherosclerosis.2017.05.029
Salmenkari H. Renin-Angiotensin System in Intestinal Inflammation-Experimental Studies with Therapeutic Interventions. Dissertation. University of Helsinki; 2019. https://helda.helsinki.fi/handle/10138/306844
Li W, Moore MJ, Vasilieva N, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003;426(6965):450-454. https://doi.org/10.1038/nature02145
Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579(7798):270-273. https://doi.org/10.1038/s41586-020-2012-7
Li MY, Li L, Zhang Y, Wang XS. Expression of the SARS-CoV-2 cell receptor gene ACE2 in a wide variety of human tissues. Infect Dis Poverty. 2020;9(1):45. https://doi.org/10.1186/s40249-020-00662-x
Zhang YZ, Li YY. Inflammatory bowel disease: pathogenesis. World J Gastroenterol. 2014;20(1):91-99. https://doi.org/10.3748/wjg.v20.i1.91
Ramos GP, Papadakis KA. Mechanisms of disease: inflammatory bowel diseases. Mayo Clin Proc. 2019;94(1):155-165. https://doi.org/10.1016/j.mayocp.2018.09.013
Sales-Campos H, Basso PJ, Alves VB, et al. Classical and recent advances in the treatment of inflammatory bowel diseases. Braz J Med Biol Res. 2015;48(2):96-107. https://doi.org/10.1590/1414-431X20143774
Rieder F, Bettenworth D, Ma C, et al. An expert consensus to standardise definitions, diagnosis and treatment targets for anti-fibrotic stricture therapies in Crohn's disease. Aliment Pharmacol Ther. 2018;48(3):347-357. https://doi.org/10.1111/apt.14853
Alvarez A, Cerda-Nicolas M, Naim Abu Nabah Y, et al. Direct evidence of leukocyte adhesion in arterioles by angiotensin II. Blood. 2004;104(2):402-408. https://doi.org/10.1182/blood-2003-08-2974
Ranjbar R, Shafiee M, Hesari A, Ferns GA, Ghasemi F, Avan A. The potential therapeutic use of renin-angiotensin system inhibitors in the treatment of inflammatory diseases. J Cell Physiol. 2019;234(3):2277-2295. https://doi.org/10.1002/jcp.27205
Shi Y, Liu T, He L, et al. Activation of the renin-angiotensin system promotes colitis development. Sci Rep. 2016;6:27552. https://doi.org/10.1038/srep27552
Hirasawa K, Sato Y, Hosoda Y, Yamamoto T, Hanai H. Immunohistochemical localization of angiotensin II receptor and local renin-angiotensin system in human colonic mucosa. J Histochem Cytochem. 2002;50(2):275-282. https://doi.org/10.1177/002215540205000215
Garg M, Royce SG, Tikellis C, et al. Imbalance of the renin-angiotensin system may contribute to inflammation and fibrosis in IBD: a novel therapeutic target? Gut. 2020;69(5):841-851. https://doi.org/10.1136/gutjnl-2019-318512
Mizushima T, Sasaki M, Ando T, et al. Blockage of angiotensin II type 1 receptor regulates TNF-alpha-induced MAdCAM-1 expression via inhibition of NF-kappaB translocation to the nucleus and ameliorates colitis. Am J Physiol Gastrointest Liver Physiol. 2010;298(2):G255-G266. https://doi.org/10.1152/ajpgi.00264.2009
Garg M, Angus PW, Burrell LM, Herath C, Gibson PR, Lubel JS. Review article: the pathophysiological roles of the renin-angiotensin system in the gastrointestinal tract. Aliment Pharmacol Ther. 2012;35(4):414-428. https://doi.org/10.1111/j.1365-2036.2011.04971.x
He L, Du J, Chen Y, et al. Renin-angiotensin system promotes colonic inflammation by inducing TH17 activation via JAK2/STAT pathway. Am J Physiol Gastrointest Liver Physiol. 2019;316(6):G774-G784. https://doi.org/10.1152/ajpgi.00053.2019
Spencer AU, Yang H, Haxhija EQ, Wildhaber BE, Greenson JK, Teitelbaum DH. Reduced severity of a mouse colitis model with angiotensin converting enzyme inhibition. Dig Dis Sci. 2007;52(4):1060-1070. https://doi.org/10.1007/s10620-006-9124-2
Katada K, Yoshida N, Suzuki T, et al. Dextran sulfate sodium-induced acute colonic inflammation in angiotensin II type 1a receptor deficient mice. Inflamm Res. 2008;57(2):84-91. https://doi.org/10.1007/s00011-007-7098-y
Khajah MA, Fateel MM, Ananthalakshmi KV, Luqmani YA. Anti-inflammatory action of angiotensin 1-7 in experimental colitis. PLoS ONE. 2016;11(3):e0150861. https://doi.org/10.1371/journal.pone.0150861
Wengrower D, Zanninelli G, Pappo O, et al. Prevention of fibrosis in experimental colitis by captopril: the role of tgf-beta1. Inflamm Bowel Dis. 2004;10(5):536-545.
Inokuchi Y, Morohashi T, Kawana I, Nagashima Y, Kihara M, Umemura S. Amelioration of 2,4,6-trinitrobenzene sulphonic acid induced colitis in angiotensinogen gene knockout mice. Gut. 2005;54(3):349-356. https://doi.org/10.1136/gut.2003.036343
Ehlers MR, Gordon K, Schwager SL, Sturrock ED. Shedding the load of hypertension: the proteolytic processing of angiotensin-converting enzyme. S Afr Med J. 2012;102(6):461-464. https://doi.org/10.7196/samj.5596
English WR, Corvol P, Murphy G. LPS activates ADAM9 dependent shedding of ACE from endothelial cells. Biochem Biophys Res Commun. 2012;421(1):70-75. https://doi.org/10.1016/j.bbrc.2012.03.113
Salmenkari H, Issakainen T, Vapaatalo H, Korpela R. Local corticosterone production and angiotensin-I converting enzyme shedding in a mouse model of intestinal inflammation. World J Gastroenterol. 2015;21(35):10072-10079. https://doi.org/10.3748/wjg.v21.i35.10072
Salmenkari H, Holappa M, Forsgard RA, Korpela R, Vapaatalo H. Orally administered angiotensin-converting enzyme-inhibitors captopril and isoleucine-proline-proline have distinct effects on local renin-angiotensin system and corticosterone synthesis in dextran sulfate sodium-induced colitis in mice. J Physiol Pharmacol. 2017;68(3):355-362.
Salmenkari H, Laitinen A, Forsgard RA, et al. The use of unlicensed bone marrow-derived platelet lysate-expanded mesenchymal stromal cells in colitis: a pre-clinical study. Cytotherapy. 2019;21(2):175-188. https://doi.org/10.1016/j.jcyt.2018.11.011
Jaszewski R, Tolia V, Ehrinpreis MN, et al. Increased colonic mucosal angiotensin I and II concentrations in Crohn's colitis. Gastroenterology. 1990;98(6):1543-1548.
Nowak JK, Lindstrom JC, Kalla R, Ricanek P, Halfvarson J, Satsangi J. Age, inflammation, and disease location are critical determinants of intestinal expression of SARS-CoV-2 receptor ACE2 and TMPRSS2 in inflammatory bowel disease. Gastroenterology. 2020;159(3):1151-1154 e2. https://doi.org/10.1053/j.gastro.2020.05.030
Hume GE, Doecke JD, Huang N, et al. Altered expression of angiotensinogen and mediators of angiogenesis in ileal Crohn's Disease. J Gastrointestin Liver Dis. 2016;25(1):39-48. https://doi.org/10.15403/jgld.2014.1121.251.chr
Garg M, Burrell LM, Velkoska E, et al. Upregulation of circulating components of the alternative renin-angiotensin system in inflammatory bowel disease: a pilot study. J Renin Angiotensin Aldosterone Syst. 2015;16(3):559-569. https://doi.org/10.1177/1470320314521086
Jahovic N, Ercan F, Gedik N, Yuksel M, Sener G, Alican I. The effect of angiotensin-converting enzyme inhibitors on experimental colitis in rats. Regul Pept. 2005;130(1-2):67-74. https://doi.org/10.1016/j.regpep.2005.03.009
Lee C, Chun J, Hwang SW, Kang SJ, Im JP, Kim JS. Enalapril inhibits nuclear factor-kappaB signaling in intestinal epithelial cells and peritoneal macrophages and attenuates experimental colitis in mice. Life Sci. 2014;95(1):29-39. https://doi.org/10.1016/j.lfs.2013.11.005
Salmenkari H, Pasanen L, Linden J, Korpela R, Vapaatalo H. Beneficial anti-inflammatory effect of angiotensin-converting enzyme inhibitor and angiotensin receptor blocker in the treatment of dextran sulfate sodium-induced colitis in mice. J Physiol Pharmacol. 2018;69(4). https://doi.org/10.26402/jpp.2018.4.07
Koga H, Yang H, Adler J, Zimmermann EM, Teitelbaum DH. Transanal delivery of angiotensin converting enzyme inhibitor prevents colonic fibrosis in a mouse colitis model: development of a unique mode of treatment. Surgery. 2008;144(2):259-268. https://doi.org/10.1016/j.surg.2008.03.043
Sueyoshi R, Ignatoski KM, Daignault S, Okawada M, Teitelbaum DH. Angiotensin converting enzyme-inhibitor reduces colitis severity in an IL-10 knockout model. Dig Dis Sci. 2013;58(11):3165-3177. https://doi.org/10.1007/s10620-013-2825-4
Okawada M, Wilson MW, Larsen SD, Lipka E, Hillfinger J, Teitelbaum DH. Blockade of the renin-angiotensin system prevents acute and immunologically relevant colitis in murine models. Pediatr Surg Int. 2016;32(12):1103-1114. https://doi.org/10.1007/s00383-016-3965-3
Santiago OI, Rivera E, Ferder L, Appleyard CB. An angiotensin II receptor antagonist reduces inflammatory parameters in two models of colitis. Regul Pept. 2008;146(1-3):250-259. https://doi.org/10.1016/j.regpep.2007.10.004
Okawada M, Koga H, Larsen SD, et al. Use of enterally delivered angiotensin II type Ia receptor antagonists to reduce the severity of colitis. Dig Dis Sci. 2011;56(9):2553-2565. https://doi.org/10.1007/s10620-011-1651-9
Wengrower D, Zanninelli G, Latella G, et al. Losartan reduces trinitrobenzene sulphonic acid-induced colorectal fibrosis in rats. Can J Gastroenterol. 2012;26(1):33-39.
Liu TJ, Shi YY, Wang EB, Zhu T, Zhao Q. AT1R blocker losartan attenuates intestinal epithelial cell apoptosis in a mouse model of Crohn's disease. Mol Med Rep. 2016;13(2):1156-1162. https://doi.org/10.3892/mmr.2015.4686
Arab HH, Al-Shorbagy MY, Abdallah DM, Nassar NN. Telmisartan attenuates colon inflammation, oxidative perturbations and apoptosis in a rat model of experimental inflammatory bowel disease. PLoS ONE. 2014;9(5):e97193. https://doi.org/10.1371/journal.pone.0097193
Guerra GC, Araujo AA, Lira GA, et al. Telmisartan decreases inflammation by modulating TNF-alpha, IL-10, and RANK/RANKL in a rat model of ulcerative colitis. Pharmacol Rep. 2015;67(3):520-526. https://doi.org/10.1016/j.pharep.2014.12.011
Saber S, Basuony M, Eldin AS. Telmisartan ameliorates dextran sodium sulfate-induced colitis in rats by modulating NF-kappaB signalling in the context of PPARgamma agonistic activity. Arch Biochem Biophys. 2019;671:185-195. https://doi.org/10.1016/j.abb.2019.07.014
Nagib MM, Tadros MG, ElSayed MI, Khalifa AE. Anti-inflammatory and anti-oxidant activities of olmesartan medoxomil ameliorate experimental colitis in rats. Toxicol Appl Pharmacol. 2013;271(1):106-113. https://doi.org/10.1016/j.taap.2013.04.026
Patel RB, Prajapati KD, Sonara BM, et al. Ameliorative potential of aliskiren in experimental colitis in mice. Eur J Pharmacol. 2014;737:70-76. https://doi.org/10.1016/j.ejphar.2014.05.009
Khajah MA, Fateel MM, Ananthalakshmi KV, Luqmani YA. Anti-inflammatory action of angiotensin 1-7 in experimental colitis may be mediated through modulation of serum cytokines/chemokines and immune cell functions. Dev Comp Immunol. 2017;74:200-208. https://doi.org/10.1016/j.dci.2017.05.005
Fukuzawa M, Satoh J, Sagara M, et al. Angiotensin converting enzyme inhibitors suppress production of tumor necrosis factor-alpha in vitro and in vivo. Immunopharmacology. 1997;36(1):49-55.
Lapteva N, Ide K, Nieda M, et al. Activation and suppression of renin-angiotensin system in human dendritic cells. Biochem Biophys Res Commun. 2002;296(1):194-200.
Briskin M, Winsor-Hines D, Shyjan A, et al. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol. 1997;151(1):97-110.
Duijvestein M, D'Haens GR. Rational and clinical development of the anti-MAdCAM monoclonal antibody for the treatment of IBD. Expert Opin Biol Ther. 2019;19(4):361-366. https://doi.org/10.1080/14712598.2019.1576631
Sandborn WJ, Lee SD, Tarabar D, et al. Phase II evaluation of anti-MAdCAM antibody PF-00547659 in the treatment of Crohn's disease: report of the OPERA study. Gut. 2018;67(10):1824-1835. https://doi.org/10.1136/gutjnl-2016-313457
Saruta M, Park DI, Kim YH, et al. Anti-MAdCAM-1 antibody (PF-00547659) for active refractory Crohn's disease in Japanese and Korean patients: the OPERA study. Intest Res. 2020;18(1):45-55. https://doi.org/10.5217/ir.2019.00039
Border WA, Noble NA. Transforming growth factor beta in tissue fibrosis. N Engl J Med. 1994;331(19):1286-1292. https://doi.org/10.1056/NEJM199411103311907
Szabo H, Fiorino G, Spinelli A, et al. Review article: anti-fibrotic agents for the treatment of Crohn's disease - lessons learnt from other diseases. Aliment Pharmacol Ther. 2010;31(2):189-201. https://doi.org/10.1111/j.1365-2036.2009.04171.x
Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol. 2003;91(3A):7A-11A. https://doi.org/10.1016/s0002-9149(02)03144-2
Benson SC, Pershadsingh HA, Ho CI, et al. Identification of telmisartan as a unique angiotensin II receptor antagonist with selective PPARgamma-modulating activity. Hypertension. 2004;43(5):993-1002. https://doi.org/10.1161/01.HYP.0000123072.34629.57
Rousseaux C, Lefebvre B, Dubuquoy L, et al. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator-activated receptor-gamma. J Exp Med. 2005;201(8):1205-1215. https://doi.org/10.1084/jem.20041948
Byrnes JJ, Gross S, Ellard C, Connolly K, Donahue S, Picarella D. Effects of the ACE2 inhibitor GL1001 on acute dextran sodium sulfate-induced colitis in mice. Inflamm Res. 2009;58(11):819-827. https://doi.org/10.1007/s00011-009-0053-3
Jacobs JD, Wagner T, Gulotta G, et al. Impact of angiotensin II signaling blockade on clinical outcomes in patients with inflammatory bowel disease. Dig Dis Sci. 2019;64(7):1938-1944. https://doi.org/10.1007/s10620-019-5474-4
Fairbrass KM, Hoshen D, Gracie DJ, Ford AC. Effect of ACE inhibitors and angiotensin II receptor blockers on disease outcomes in inflammatory bowel disease. Gut. 2020. https://doi.org/10.1136/gutjnl-2020-321186
Mantaka A, Tsoukali E, Fragkaki M, et al. Is there any role of renin-angiotensin system inhibitors in modulating inflammatory bowel disease outcome? Eur J Gastroenterol Hepatol. 2021;33(3):364-371. https://doi.org/10.1097/MEG.0000000000001912
Willemze RA, Bakker T, Pippias M, Ponsioen CY, de Jonge WJ. β-Blocker use is associated with a higher relapse risk of inflammatory bowel disease: a Dutch retrospective case-control study. Eur J Gastroenterol Hepatol. 2018;30(2):161-166. https://doi.org/10.1097/MEG.0000000000001016
Hume GE, Radford-Smith GL. ACE inhibitors and angiotensin II receptor antagonists in Crohn's disease management. Expert Rev Gastroenterol Hepatol. 2008;2(5):645-651. https://doi.org/10.1586/17474124.2.5.645