The non-thiol angiotensin-converting enzyme inhibitor quinapril suppresses inflammatory arthritis
Abstract
OBJECTIVES: In addition to its vasoactive effects, angiotensin II has proinflammatory properties. Angiotensin-converting enzyme (ACE) inhibitors reduce the production of angiotensin II and could therefore act as anti-inflammatory agents. Here we investigated the capacity of the ACE inhibitor quinapril to modulate inflammatory arthritis. METHODS: We studied the effect of quinapril on disease activity in mice with collagen-induced arthritis (CIA). Mice received oral quinapril (10 mg/kg/day) at the time of arthritis induction (prophylaxis protocol) or at the onset of mild arthritis (therapy protocol). Concentrations of immunoglobulin G (IgG) subtypes specific for bovine Type II collagen and TNF-alpha were measured by enzyme-linked immunoassay. RESULTS: Quinapril significantly diminished the activity of CIA when given as prophylaxis or therapy (prophylaxis protocol, P<0.001; therapy protocol P=0.002). Antigen-specific IgG2a antibodies were reduced by 52% (P=0.02) in the quinapril prophylaxis protocol. Suppression of arthritis by quinapril was associated with reduced articular expression of TNF-alpha by 68% (P=0.01) in the prophylaxis protocol and 27% (P=0.06) in the therapy protocol. Quinapril therapy also inhibited expression of splenocyte TNF-alpha production following lipopolysaccharide (LPS) in vitro stimulation by 59% (P=0.02). In parallel human in vitro experiments, ACE inhibition suppressed LPS-stimulated production of TNF-alpha by monocytes. In order to confirm that the action of quinapril occurred predominantly through suppression of angiotensin II, parallel experiments with the angiotensin receptor antagonist candesartan cilexetil demonstrated that this agent also inhibited disease activity in CIA. CONCLUSIONS: These data suggest that angiotensin II is a mediator of chronic inflammation and that ACE inhibition may have therapeutic effects in human inflammatory arthritis.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
ACE inhibitors of different types reduce severity of collagen type II-induced arthritis.
“ACE inhibitors of different types reduce severity of collagen type II-induced arthritis [139,140].”
From Interaction of the endocrine system with inflammation: a function of energy and volume regulation (2014) · cites this paper as [139]
Cites
Practical Statistics for Medical Research.
Walter, S., & Altman, D. G. (1992) · Biometrics · doi:10.2307/2532320 · Cited by 11,665 · see citing works
Practical Statistics for Medical Research
Altman, D. G. (1990) · doi:10.1201/9780429258589 · Cited by 10,668 · see citing works
(2000) · New England Journal of Medicine · doi:10.1056/nejm200001203420301 · Cited by 8,663 · see citing works
Practical Statistics for Medical Research.
Bartko, J. J., & Altman, D. G. (1992) · Journal of the American Statistical Association · doi:10.2307/2290246 · Cited by 4,834 · see citing works
Swedberg, K. B., & KJEKSHUS, J. K. (1988) · The American Journal of Cardiology · doi:10.1016/s0002-9149(88)80087-0 · Cited by 3,762 · see citing works
ROLE OF CYTOKINES IN RHEUMATOID ARTHRITIS
Feldmann, M., Brennan, F. M., & Maini, R. N. (1996) · Annual Review of Immunology · doi:10.1146/annurev.immunol.14.1.397 · Cited by 2,486 · see citing works
Cardiovascular Morbidity and Mortality in Women Diagnosed With Rheumatoid Arthritis
Solomon, D. H., Karlson, E. W., Rimm, E. B., Cannuscio, C. C., Mandl, L. A., Manson, J. E., Stampfer, M. J., & Curhan, G. C. (2003) · Circulation · doi:10.1161/01.cir.0000054612.26458.b2 · Cited by 1,240 · see citing works
Youssef, S., Stüve, O., Patarroyo, J. C., Ruiz, P. J., Radosevich, J. L., Hur, E. M., Bravo, M., Mitchell, D. J., Sobel, R. A., Steinman, L., et al. (2002) · Nature · doi:10.1038/nature01158 · Cited by 1,094 · see citing works
Ruggenenti, P., Perna, A., Gherardi, G., Garini, G., Zoccali, C., Salvadori, M., Scolari, F., Schena, F. P., & Remuzzi, G. (1999) · The Lancet · doi:10.1016/s0140-6736(98)10363-x · Cited by 910 · see citing works
McCarey, D. W., McInnes, I. B., Madhok, R., Hampson, R., Scherbakova, O., Ford, I., Capell, H. A., & Sattar, N. A. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16449-0 · Cited by 818 · see citing works
Inflammation and angiotensin II
Suzuki, Y., Ruiz‐Ortega, M., Lorenzo, Ó., Rupérez, M., Esteban, V., & Egido, J. (2003) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00271-6 · Cited by 696 · see citing works
Hernández-Presa, M. Á., Bustos, C., Ortego, M., Tuñon, J., Renedo, G., Ruiz‐Ortega, M., & Egido, J. (1997) · Circulation · doi:10.1161/01.cir.95.6.1532 · Cited by 490 · see citing works
A novel anti-inflammatory role for simvastatin in inflammatory arthritis.
Leung, B. P., Sattar, N., Crilly, A., Prach, M., McCarey, D. W., Payne, H., Madhok, R., Campbell, C., Gracie, J. A., Liew, F. Y., et al. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.3.1524 · Cited by 434 · see citing works
Handbook of Laboratory Animal Management and Welfare
Wolfensohn, S. (2003) · Wiley eBooks · doi:10.1002/9780470751077 · Cited by 419 · see citing works
A continuous spectrophotometric assay for angiotensin converting enzyme
Holmquist, B., Bünning, P., & Riordan, J. F. (1979) · Analytical Biochemistry · doi:10.1016/0003-2697(79)90769-3 · Cited by 411 · see citing works
del Rincón, I., Williams, K., D, M. P. S. M., Freeman, G. L., O’Leary, D. H., & Escalante, A. (2003) · Arthritis & Rheumatism · doi:10.1002/art.11078 · Cited by 353 · see citing works
Stuart, J. M., Cremer, M. A., Townes, A. S., et al. (1982) · The Journal of Experimental Medicine · doi:10.1084/jem.155.1.1 · Cited by 336 · see citing works
Activation of the transcription factor nuclear factor‐κB in human inflamed synovial tissue
Marok, R., Winyard, P. G., Coumbe, A., Kus, M. L., Gaffney, K., Blades, S., Mapp, P. I., Morris, C. J., Blake, D. R., Kaltschmidt, C., et al. (1996) · Arthritis & Rheumatism · doi:10.1002/art.1780390407 · Cited by 316 · see citing works
B cell-deficient mice do not develop type II collagen-induced arthritis (CIA)
Svensson, L., Jirholt, J., Holmdahl, R., & Jansson, L. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00529.x · Cited by 315 · see citing works
Ruiz‐Ortega, M., Bustos, C., Hernández-Presa, M. Á., Lorenzo, Ó., Plaza, J. J. G., & Egido, J. (1998) · PubMed · Cited by 284 · see citing works
Angiotensin II is associated with activation of NF-κB-mediated genes and downregulation of PPARs
Tham, D. M., Martin-McNulty, B., Wang, Y.-X., Wilson, D. W., Vergona, R. A., Sullivan, M. E., Dole, W. P., & Rutledge, J. C. (2002) · Physiological Genomics · doi:10.1152/physiolgenomics.00062.2002 · Cited by 276 · see citing works
Dzau, V. J., Bernstein, K. E., Celermajer, D. S., Cohen, J. D., Dahlöf, B., Deanfield, J. E., Dı́ez, J., Drexler, H., Ferrari, R., van Gilst, W. H., et al. (2001) · The American Journal of Cardiology · doi:10.1016/s0002-9149(01)01878-1 · Cited by 260 · see citing works
Upregulation of renin-angiotensin system during differentiation of monocytes to macrophages
Okamura, A., Rakugi, H., Ohishi, M., Yanagitani, Y., Takiuchi, S., Moriguchi, K., Fennessy, P., Higaki, J., & Ogihara, T. (1999) · Journal of Hypertension · doi:10.1097/00004872-199917040-00012 · Cited by 221 · see citing works
Boom, W. H., Liano, D., & Abbas, A. K. (1988) · The Journal of Experimental Medicine · doi:10.1084/jem.167.4.1350 · Cited by 191 · see citing works
Kranzhöfer, R., Browatzki, M., Schmidt, J., & Kübler, W. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0543 · Cited by 191 · see citing works
CAPTOPRIL: A NEW TREATMENT FOR RHEUMATOID ARTHRITIS?
MARTIN, M. F. R., Mckenna, F., Bird, H. A., Surrall, K. E., Dixon, J. S., & Wright, V. A. (1984) · The Lancet · doi:10.1016/s0140-6736(84)91821-x · Cited by 159 · see citing works
Rosloniec, E. F., Cremer, M. A., Kang, A. H., et al. (1996) · Current Protocols in Immunology · doi:10.1002/0471142735.im1505s20 · Cited by 157 · see citing works
Cardiovascular mortality in women with rheumatoid arthritis.
Myllykangas-Luosujärvi, R., Aho, K., Kautiainen, H., et al. (1995) · PubMed · Cited by 155 · see citing works
Modulation of oral bioavailability of anticancer drugs: from mouse to man
Schellens, J. H. M., Malingré, M. M., Kruijtzer, C. M. F., Bardelmeijer, H. A., van Tellingen, O., Schinkel, A. H., & Beijnen, J. H. (2000) · European Journal of Pharmaceutical Sciences · doi:10.1016/s0928-0987(00)00153-6 · Cited by 147 · see citing works
Control of dendritic cell differentiation by angiotensin II
Nahmod, K. A., Vermeulen, M. E., Radien, S., Salamone, G. V., Gamberale, R., Fernández‐Calotti, P., Alvarez, A. L., Nahmod, V. E., Giordano, M., & Geffner, J. R. (2003) · The FASEB Journal · doi:10.1096/fj.02-0755fje · Cited by 124 · see citing works
Kuno, A., Yamada, T., Masuda, K., Ogawa, K., Sogawa, M., Nakamura, S., Nakazawa, T., Ohara, H., Nomura, T., Joh, T., et al. (2003) · Gastroenterology · doi:10.1053/gast.2003.50147 · Cited by 122 · see citing works
Fukuzawa, M., Satoh, J., Sagara, M., Muto, G., Muto, Y., Nishimura, S., Miyaguchi, S., Qiang, X., Sakata, Y., NAKAZAWA, T., et al. (1997) · Immunopharmacology · doi:10.1016/s0162-3109(96)00160-9 · Cited by 87 · see citing works
Evidence That Angiotensin II Is Present in Human Monocytes
Kitazono, T., Padgett, R. C., Armstrong, M. L., Tompkins, P. K., & Heistad, D. D. (1995) · Circulation · doi:10.1161/01.cir.91.4.1129 · Cited by 85 · see citing works
Captopril Prevents Experimental Autoimmune Myocarditis
Godsel, L. M., León, J. S., Wang, K., Fornek, J. L., Molteni, A., & Engman, D. M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.1.346 · Cited by 76 · see citing works
[32] Type II collagen-induced arthritis in rats
Ridge, S. C., Oronsky, A. L., & Kerwar, S. S. (1988) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(88)62090-8 · Cited by 74 · see citing works
Activation and suppression of renin–angiotensin system in human dendritic cells
Lapteva, N., Ide, K., Nieda, M., et al. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)00855-0 · Cited by 68 · see citing works
Constantinescu, C. S., Ventura, E. S., Hilliard, B. A., et al. (1995) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923979509016382 · Cited by 65 · see citing works
Walsh, D. A., Catravas, J., & Wharton, J. (2000) · Annals of the Rheumatic Diseases · doi:10.1136/ard.59.2.125 · Cited by 57 · see citing works
AT1 receptor characteristics of angiotensin analogue binding in human synovium
Walsh, D. A., Suzuki, T., Knock, G. A., Blake, D. R., Polak, J. M., & Wharton, J. (1994) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1994.tb13091.x · Cited by 52 · see citing works
Goto, M., Fujisawa, M., Yamada, A., et al. (1990) · Annals of the Rheumatic Diseases · doi:10.1136/ard.49.3.172 · Cited by 51 · see citing works
Renal Tubulointerstitial Damage Caused by Persistent Proteinuria Is Attenuated in AT1-Deficient Mice
Suzuki, Y., López‐Franco, Ó., Gómez‐Garré, D., et al. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63036-2 · Cited by 49 · see citing works
Sawada, T., Ishíi, Y., Tojimbara, T., et al. (2002) · Pharmacological Research · doi:10.1016/s1043661802002281 · Cited by 46 · see citing works
Production of angiotensin converting enzyme by rheumatoid synovial membrane.
Veale, D. J., Yanni, G., Bresnihan, B., & FitzGerald, O. (1992) · Annals of the Rheumatic Diseases · doi:10.1136/ard.51.4.476 · Cited by 45 · see citing works
Agha, A. M., & Mansour, M. A. (2000) · Toxicology and Applied Pharmacology · doi:10.1006/taap.2000.8985 · Cited by 43 · see citing works
Bird, H. A., Gallez, P. L., Dixon, J. S., et al. (1990) · PubMed · Cited by 34 · see citing works
Angiotensin Converting Enzyme Inhibition
Waeber, B., Nussberger, J., Juillerat, L., et al. (1989) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-198900000-00012 · Cited by 33 · see citing works
Oubiña, M. P., Heras, N. D. L., Cediel, E., Sanz‐Rosa, D., Aragoncillo, P., Dı́az-Jullien, C., Hernández, G., Lahera, V., & Cachofeiro, V. (2003) · Clinical Science · doi:10.1042/cs20030127 · Cited by 30 · see citing works
Experimental autoimmune arthritis in mice
Boissier, M., Carlioz, A., & Fournier, C. M. (1988) · Clinical Immunology and Immunopathology · doi:10.1016/0090-1229(88)90086-4 · Cited by 28 · see citing works
Caspritz, G., Alpermann, H. G., & Schleyerbach, R. (1986) · PubMed · Cited by 24 · see citing works
Goto, M., Sasano, M., Fuzisawa, M., et al. (1992) · Annals of the Rheumatic Diseases · doi:10.1136/ard.51.6.741 · Cited by 21 · see citing works
Nash, D. T. (1992) · The American Journal of Cardiology · doi:10.1016/0002-9149(92)90278-7 · Cited by 19 · see citing works
MacDonald, J. R., Susick, R. L., Pegg, D. G., et al. (1992) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199202000-00017 · Cited by 16 · see citing works
Cardioprotective effects of quinapril after myocardial infarction in hypertensive rats
Mori, T., Nishimura, H., Okabe, M., et al. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(98)00155-1 · Cited by 8 · see citing works
Waeber, B., Nussberger, J., Juillerat, L., et al. (1989) · IRIS · Cited by 2 · see citing works
Komuro (2001) · doi:10.1002/1529-0131(200112)44:12
Flagged first, then by citations
Cited by
Sorted by citations
Interaction of the endocrine system with inflammation: a function of energy and volume regulation
Straub, R. H. (2014) · Arthritis Research & Therapy · doi:10.1186/ar4484 · Cited by 121 · see citing works
“arthritis [139,140].”
- Authors
- Dalbeth, N.
- Affiliations
- Imperial College London (GB)
- Corresponding author
- Dalbeth, N.
- ORCID
- Dalbeth, N.
- Venue
- Rheumatology
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-01-01
- Volume
- 44
- Issue
- 1
- Pages
- 24-31
- ISSN
- 0263-7103 (ISSN-L)
- 1460-2172
- OpenAlex
- W2129492896
- Cited by
- 61
- References
- 56
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 2 · 2022: 5 · 2021: 4 · 2020: 1 · 2019: 4 · 2018: 3 · 2016: 2 · 2015: 4 · 2014: 4 · 2013: 5 · 2012: 3
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- British journal of rheumatology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Renin-Angiotensin System Studies
- Health Sciences › Medicine › Complementary and alternative medicine › Natural Compounds in Disease Treatment
- Keywords
- quinapril, ACE inhibitors, angiotensin II, inflammatory arthritis, collagen-induced arthritis, TNF-α, anti-inflammatory activity, candesartan cilexetil, angiotensin receptor blockers, IgG2a antibodies, chronic inflammation
- MeSH terms
- Quinapril, Angiotensin-Converting Enzyme Inhibitors, Animals, Epitopes, Arthritis, Experimental, Immunoglobulin G, Peptidyl-Dipeptidase A, Male, Mice, Inbred DBA, Monocytes, Tumor Necrosis Factor-alpha, Cytokines, Collagen Type II, Tetrahydroisoquinolines, Angiotensin II Type 1 Receptor Blockers, Mice
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