A dual role of lysophosphatidic acid type 2 receptor (LPAR2) in nonsteroidal anti-inflammatory drug-induced mouse enteropathy.
DBIBB
LPAR2
autotaxin
enteropathy
lysophosphatidic acid
nonsteroidal anti-inflammatory drug
Journal
Acta pharmacologica Sinica
ISSN: 1745-7254
Titre abrégé: Acta Pharmacol Sin
Pays: United States
ID NLM: 100956087
Informations de publication
Date de publication:
10 Oct 2023
10 Oct 2023
Historique:
received:
16
05
2023
accepted:
21
09
2023
medline:
11
10
2023
pubmed:
11
10
2023
entrez:
10
10
2023
Statut:
aheadofprint
Résumé
Lysophosphatidic acid (LPA) is a bioactive phospholipid mediator that has been found to ameliorate nonsteroidal anti-inflammatory drug (NSAID)-induced gastric injury by acting on lysophosphatidic acid type 2 receptor (LPAR2). In this study, we investigated whether LPAR2 signaling was implicated in the development of NSAID-induced small intestinal injury (enteropathy), another major complication of NSAID use. Wild-type (WT) and Lpar2 deficient (Lpar2
Identifiants
pubmed: 37816857
doi: 10.1038/s41401-023-01175-7
pii: 10.1038/s41401-023-01175-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s).
Références
Singh G. Gastrointestinal complications of prescription and over-the-counter nonsteroidal anti-inflammatory drugs: a view from the ARAMIS database. Arthritis, Rheumatism, and Aging Medical Information System. Am J Ther. 2000;7:115–21.
pubmed: 11319579
doi: 10.1097/00045391-200007020-00008
Lanas A, Scarpignato C. Microbial flora in NSAID-induced intestinal damage: a role for antibiotics? Digestion. 2006;73:136–50.
pubmed: 16498262
doi: 10.1159/000089789
Wallace JL. Mechanisms, prevention and clinical implications of nonsteroidal anti-inflammatory drug-enteropathy. World J Gastroenterol. 2013;19:1861–76.
pubmed: 23569332
pmcid: 3613102
doi: 10.3748/wjg.v19.i12.1861
Boelsterli UA, Redinbo MR, Saitta KS. Multiple NSAID-induced hits injure the small intestine: underlying mechanisms and novel strategies. Toxicol Sci. 2013;131:654–67.
pubmed: 23091168
doi: 10.1093/toxsci/kfs310
Bjarnason I, Scarpignato C, Holmgren E, Olszewski M, Rainsford KD, Lanas A. Mechanisms of damage to the gastrointestinal tract from nonsteroidal anti-inflammatory drugs. Gastroenterology. 2018;154:500–14.
pubmed: 29221664
doi: 10.1053/j.gastro.2017.10.049
Tomisato W, Tsutsumi S, Hoshino T, Hwang HJ, Mio M, Tsuchiya T, et al. Role of direct cytotoxic effects of NSAIDs in the induction of gastric lesions. Biochem Pharmacol. 2004;67:575–85.
pubmed: 15037209
doi: 10.1016/j.bcp.2003.09.020
Tanaka K, Tomisato W, Hoshino T, Ishihara T, Namba T, Aburaya M, et al. Involvement of intracellular Ca
pubmed: 15987693
doi: 10.1074/jbc.M502956200
Gyires K. Gastric mucosal protection: from prostaglandins to gene-therapy. Curr Med Chem. 2005;12:203–15.
pubmed: 15638736
doi: 10.2174/0929867053363478
Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn’t the stomach digest itself? Physiol Rev. 2008;88:1547–65.
pubmed: 18923189
doi: 10.1152/physrev.00004.2008
Wallace J, Keenan C, Granger D. Gastric ulceration induced by nonsteroidal anti inflammatory drugs is a neutrophil-dependent process. Am J Physiol. 1990;259:G462–7.
pubmed: 2169206
Konaka A, Kato S, Tanaka A, Kunikata T, Korolkiewicz R, Takeuchi K. Roles of enterobacteria, nitric oxide and neutrophil in pathogenesis of indomethacin-induced small intestinal lesions in rats. Pharmacol Res. 1999;40:517–24.
pubmed: 10660951
doi: 10.1006/phrs.1999.0550
Beck PL, Xavier R, Lu N, Nanda NN, Dinauer M, Podolsky DK, et al. Mechanisms of NSAID-induced gastrointestinal injury defined using mutant mice. Gastroenterology. 2000;119:699–705.
pubmed: 10982764
doi: 10.1053/gast.2000.16497
Watanabe T, Higuchi K, Kobata A, Nishio H, Tanigawa T, Shiba M, et al. Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent. Gut. 2008;57:181–7.
pubmed: 17639086
doi: 10.1136/gut.2007.125963
Wallace JL. NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. Br J Pharmacol. 2012;165:67–74.
pubmed: 21627632
pmcid: 3252967
doi: 10.1111/j.1476-5381.2011.01509.x
Wallace JL, Syer S, Denou E, de Palma G, Vong L, McKnight W, et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. 2011;141:1314–22.
pubmed: 21745447
doi: 10.1053/j.gastro.2011.06.075
Taha AS, McCloskey C, McSkimming P, McConnachie A. Misoprostol for small bowel ulcers in patients with obscure bleeding taking aspirin and non-steroidal anti-inflammatory drugs (MASTERS): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Gastroenterol Hepatol. 2018;3:469–76.
pubmed: 29754836
doi: 10.1016/S2468-1253(18)30119-5
Yung YC, Stoddard NC, Chun J. LPA receptor signaling: pharmacology, physiology, and pathophysiology. J Lipid Res. 2014;55:1192–214.
pubmed: 24643338
pmcid: 4076099
doi: 10.1194/jlr.R046458
Geraldo LHM, Spohr T, Amaral RFD, Fonseca A, Garcia C, Mendes FA, et al. Role of lysophosphatidic acid and its receptors in health and disease: novel therapeutic strategies. Signal Transduct Target Ther. 2021;6:45.
pubmed: 33526777
pmcid: 7851145
doi: 10.1038/s41392-020-00367-5
Aoki J, Inoue A, Okudaira S. Two pathways for lysophosphatidic acid production. Biochim Biophys Acta. 2008;1781:513–8.
pubmed: 18621144
doi: 10.1016/j.bbalip.2008.06.005
Tanaka T, Horiuchi G, Matsuoka M, Hirano K, Tokumura A, Koike T, et al. Formation of lysophosphatidic acid, a wound-healing lipid, during digestion of cabbage leaves. Biosci Biotechnol Biochem. 2009;73:1293–300.
pubmed: 19502739
doi: 10.1271/bbb.80813
Lin S, Yeruva S, He P, Singh AK, Zhang H, Chen M, et al. Lysophosphatidic acid stimulates the intestinal brush border Na
pubmed: 19800338
doi: 10.1053/j.gastro.2009.09.055
Wang Z, Shi W, Tian D, Qin H, Vallance BA, Yang H, et al. Autotaxin stimulates LPA2 receptor in macrophages and exacerbates dextran sulfate sodium-induced acute colitis. J Mol Med (Berl). 2020;98:1781–94.
pubmed: 33128578
doi: 10.1007/s00109-020-01997-6
Deng W, Balazs L, Wang DA, Van Middlesworth L, Tigyi G, Johnson LR. Lysophosphatidic acid protects and rescues intestinal epithelial cells from radiation- and chemotherapy-induced apoptosis. Gastroenterology. 2002;123:206–16.
pubmed: 12105849
doi: 10.1053/gast.2002.34209
Deng W, Shuyu E, Tsukahara R, Valentine WJ, Durgam G, Gududuru V, et al. The lysophosphatidic acid type 2 receptor is required for protection against radiation-induced intestinal injury. Gastroenterology. 2007;132:1834–51.
pubmed: 17484878
doi: 10.1053/j.gastro.2007.03.038
Patil R, Szabo E, Fells JI, Balogh A, Lim KG, Fujiwara Y, et al. Combined mitigation of the gastrointestinal and hematopoietic acute radiation syndromes by an LPA2 receptor-specific nonlipid agonist. Chem Biol. 2015;22:206–16.
pubmed: 25619933
pmcid: 4336611
doi: 10.1016/j.chembiol.2014.12.009
Kuo B, Szabo E, Lee SC, Balogh A, Norman D, Inoue A, et al. The LPA
pubmed: 30063964
pmcid: 6163127
doi: 10.1016/j.cellsig.2018.07.007
Shukla PK, Meena AS, Gangwar R, Szabo E, Balogh A, Chin Lee S, et al. LPAR2 receptor activation attenuates radiation-induced disruption of apical junctional complexes and mucosal barrier dysfunction in mouse colon. FASEB J. 2020;34:11641–57.
pubmed: 32654268
doi: 10.1096/fj.202000544R
Tigyi GJ, Johnson LR, Lee SC, Norman DD, Szabo E, Balogh A, et al. Lysophosphatidic acid type 2 receptor agonists in targeted drug development offer broad therapeutic potential. J Lipid Res. 2019;60:464–74.
pubmed: 30692142
pmcid: 6399510
doi: 10.1194/jlr.S091744
Tanaka T, Ohmoto M, Morito K, Kondo H, Urikura M, Satouchi K, et al. Type 2 lysophosphatidic acid receptor in gastric surface mucous cells: possible implication of prostaglandin E2 production. Biofactors. 2014;40:355–61.
pubmed: 24375908
doi: 10.1002/biof.1147
Afroz S, Yagi A, Fujikawa K, Rahman MM, Morito K, Fukuta T, et al. Lysophosphatidic acid in medicinal herbs enhances prostaglandin E
pubmed: 29462674
doi: 10.1016/j.prostaglandins.2018.01.003
Yun CC, Sun H, Wang D, Rusovici R, Castleberry A, Hall RA, et al. LPA2 receptor mediates mitogenic signals in human colon cancer cells. Am J Physiol Cell Physiol. 2005;289:C2–11.
pubmed: 15728708
doi: 10.1152/ajpcell.00610.2004
Yamashita H, Kitayama J, Shida D, Ishikawa M, Hama K, Aoki J, et al. Differential expression of lysophosphatidic acid receptor-2 in intestinal and diffuse type gastric cancer. J Surg Oncol. 2006;93:30–5.
pubmed: 16353194
doi: 10.1002/jso.20397
Dong YL, Duan XY, Liu YJ, Fan H, Xu M, Chen QY, et al. Autotaxin-lysophosphatidic acid axis blockade improves inflammation by regulating Th17 cell differentiation in DSS-induced chronic colitis mice. Inflammation. 2019;42:1530–41.
pubmed: 31102124
doi: 10.1007/s10753-019-01015-z
Lin S, Wang D, Iyer S, Ghaleb AM, Shim H, Yang VW, et al. The absence of LPA2 attenuates tumor formation in an experimental model of colitis-associated cancer. Gastroenterology. 2009;136:1711–20.
pubmed: 19328876
doi: 10.1053/j.gastro.2009.01.002
Contos JJ, Ishii I, Fukushima N, Kingsbury MA, Ye X, Kawamura S, et al. Characterization of lpa
pubmed: 12215548
pmcid: 134025
doi: 10.1128/MCB.22.19.6921-6929.2002
Liang X, Bittinger K, Li X, Abernethy DR, Bushman FD, FitzGerald GA. Bidirectional interactions between indomethacin and the murine intestinal microbiota. Elife. 2015;4:e08973.
pubmed: 26701907
pmcid: 4755745
doi: 10.7554/eLife.08973
Lazar B, Laszlo SB, Hutka B, Toth AS, Mohammadzadeh A, Berekmeri E, et al. A comprehensive time course and correlation analysis of indomethacin-induced inflammation, bile acid alterations and dysbiosis in the rat small intestine. Biochem Pharmacol. 2021;190:114590.
pubmed: 33940029
doi: 10.1016/j.bcp.2021.114590
Knowlden SA, Hillman SE, Chapman TJ, Patil R, Miller DD, Tigyi G, et al. Novel inhibitory effect of a lysophosphatidic acid 2 agonist on allergen-driven airway inflammation. Am J Respir Cell Mol Biol. 2016;54:402–9.
pubmed: 26248018
pmcid: 4821034
doi: 10.1165/rcmb.2015-0124OC
Laszlo SB, Lazar B, Brenner GB, Makkos A, Balogh M, Al-Khrasani M, et al. Chronic treatment with rofecoxib but not ischemic preconditioning of the myocardium ameliorates early intestinal damage following cardiac ischemia/reperfusion injury in rats. Biochem Pharmacol. 2020;178:114099.
pubmed: 32540483
doi: 10.1016/j.bcp.2020.114099
Zadori ZS, Toth VE, Feher A, Al-Khrasani M, Puskar Z, Kozsurek M, et al. Inhibition of alpha2A-adrenoceptors ameliorates dextran sulfate sodium-induced acute intestinal inflammation in mice. J Pharmacol Exp Ther. 2016;358:483–91.
pubmed: 27418171
doi: 10.1124/jpet.116.235101
Bankhead P, Loughrey MB, Fernandez JA, Dombrowski Y, McArt DG, Dunne PD, et al. QuPath: open source software for digital pathology image analysis. Sci Rep. 2017;7:16878.
pubmed: 29203879
pmcid: 5715110
doi: 10.1038/s41598-017-17204-5
Yoshimi T, Yamagishi Y, Kanegawa I, Suda M, Saiki R, Tanaka KI, et al. Study of the inhibitory effects of enteral nutrition formula on indomethacin-induced gastric lesions in mice. Nutrients. 2019;11:3058.
Banerjee S, Norman DD, Lee SC, Parrill AL, Pham TC, Baker DL, et al. Highly potent non-carboxylic acid autotaxin inhibitors reduce melanoma metastasis and chemotherapeutic resistance of breast cancer stem cells. J Med Chem. 2017;60:1309–24.
pubmed: 28112925
pmcid: 7938327
doi: 10.1021/acs.jmedchem.6b01270
Koga H, Aoyagi K, Matsumoto T, Iida M, Fujishima M. Experimental enteropathy in athymic and euthymic rats: synergistic role of lipopolysaccharide and indomethacin. Am J Physiol. 1999;276:G576–82.
pubmed: 10070032
Stadnyk A, Dollard C, Issekutz T, Issekutz A. Neutrophil migration into indomethacin induced rat small intestinal injury is CD11a/CD18 and CD11b/CD18 co-dependent. Gut. 2002;50:629–35.
pubmed: 11950807
pmcid: 1773205
doi: 10.1136/gut.50.5.629
Bertrand V, Guimbaud R, Tulliez M, Mauprivez C, Sogni P, Couturier D, et al. Increase in tumor necrosis factor-alpha production linked to the toxicity of indomethacin for the rat small intestine. Br J Pharmacol. 1998;124:1385–94.
pubmed: 9723949
pmcid: 1565527
doi: 10.1038/sj.bjp.0701968
Tsatsanis C, Androulidaki A, Venihaki M, Margioris AN. Signalling networks regulating cyclooxygenase-2. Int J Biochem Cell Biol. 2006;38:1654–61.
pubmed: 16713323
doi: 10.1016/j.biocel.2006.03.021
Wallace JL, McKnight W, Reuter BK, Vergnolle N. NSAID-induced gastric damage in rats: requirement for inhibition of both cyclooxygenase 1 and 2. Gastroenterology. 2000;119:706–14.
pubmed: 10982765
doi: 10.1053/gast.2000.16510
Tanaka A, Hase S, Miyazawa T, Ohno R, Takeuchi K. Role of cyclooxygenase (COX)-1 and COX-2 inhibition in nonsteroidal anti-inflammatory drug-induced intestinal damage in rats: relation to various pathogenic events. J Pharmacol Exp Ther. 2002;303:1248–54.
pubmed: 12438549
doi: 10.1124/jpet.102.041715
Doni A, Stravalaci M, Inforzato A, Magrini E, Mantovani A, Garlanda C, et al. The long pentraxin PTX3 as a link between innate immunity, tissue remodeling, and cancer. Front Immunol. 2019;10:712.
pubmed: 31019517
pmcid: 6459138
doi: 10.3389/fimmu.2019.00712
Chow JY, Li ZJ, Wu WK, Cho CH. Cathelicidin a potential therapeutic peptide for gastrointestinal inflammation and cancer. World J Gastroenterol. 2013;19:2731–5.
pubmed: 23687409
pmcid: 3653146
doi: 10.3748/wjg.v19.i18.2731
Lin S, Lee SJ, Shim H, Chun J, Yun CC. The absence of LPA receptor 2 reduces the tumorigenesis by ApcMin mutation in the intestine. Am J Physiol Gastrointest Liver Physiol. 2010;299:G1128–38.
pubmed: 20724530
pmcid: 2993170
doi: 10.1152/ajpgi.00321.2010
Maity P, Bindu S, Dey S, Goyal M, Alam A, Pal C, et al. Indomethacin, a non-steroidal anti-inflammatory drug, develops gastropathy by inducing reactive oxygen species-mediated mitochondrial pathology and associated apoptosis in gastric mucosa: a novel role of mitochondrial aconitase oxidation. J Biol Chem. 2009;284:3058–68.
pubmed: 19049974
doi: 10.1074/jbc.M805329200
Fukumoto K, Naito Y, Takagi T, Yamada S, Horie R, Inoue K, et al. Role of tumor necrosis factor-alpha in the pathogenesis of indomethacin-induced small intestinal injury in mice. Int J Mol Med. 2011;27:353–9.
pubmed: 21249312
Andrews C, McLean MH, Durum SK. Cytokine tuning of intestinal epithelial function. Front Immunol. 2018;9:1270.
pubmed: 29922293
pmcid: 5996247
doi: 10.3389/fimmu.2018.01270
Blander JM. Death in the intestinal epithelium-basic biology and implications for inflammatory bowel disease. FEBS J. 2016;283:2720–30.
pubmed: 27250564
pmcid: 4956528
doi: 10.1111/febs.13771
Patton J, Bonne-Année S, Deckman J, Hess J, Torigian A, Nolan T, et al. Methylprednisolone acetate induces, and Δ7-dafachronic acid suppresses, Strongyloides stercoralis hyperinfection in NSG mice. Proc Natl Acad Sci USA. 2018;115:204–9.
pubmed: 29203662
doi: 10.1073/pnas.1712235114
Sturm A, Sudermann T, Schulte K, Goebell H, Dignass A. Modulation of intestinal epithelial wound healing in vitro and in vivo by lysophosphatidic acid. Gastroenterology. 1999;11:368–77.
doi: 10.1053/gast.1999.0029900368
Lee SJ, Leoni G, Neumann PA, Chun J, Nusrat A, Yun CC. Distinct phospholipase C-beta isozymes mediate lysophosphatidic acid receptor 1 effects on intestinal epithelial homeostasis and wound closure. Mol Cell Biol. 2013;33:2016–28.
pubmed: 23478264
pmcid: 3647975
doi: 10.1128/MCB.00038-13
Adachi M, Horiuchi G, Ikematsu N, Tanaka T, Terao J, Satouchi K, et al. Intragastrically administered lysophosphatidic acids protect against gastric ulcer in rats under water-immersion restraint stress. Dig Dis Sci. 2011;56:2252–61.
pubmed: 21298479
doi: 10.1007/s10620-011-1595-0
Tanaka T, Morito K, Kinoshita M, Ohmoto M, Urikura M, Satouchi K, et al. Orally administered phosphatidic acids and lysophosphatidic acids ameliorate aspirin-induced stomach mucosal injury in mice. Dig Dis Sci. 2013;58:950–8.
pubmed: 23161268
doi: 10.1007/s10620-012-2475-y
Thompson KE, Ray RM, Alli S, Ge W, Boler A, Shannon McCool W, et al. Prevention and treatment of secretory diarrhea by the lysophosphatidic acid analog Rx100. Exp Biol Med (Maywood). 2018;243:1056–65.
pubmed: 30253666
doi: 10.1177/1535370218803349
Tsutsumi S, Gotoh T, Tomisato W, Mima S, Hoshino T, Hwang HJ, et al. Endoplasmic reticulum stress response is involved in nonsteroidal anti-inflammatory drug-induced apoptosis. Cell Death Differ. 2004;11:1009–16.
pubmed: 15131590
doi: 10.1038/sj.cdd.4401436
Omatsu T, Naito Y, Handa O, Mizushima K, Hayashi N, Qin Y, et al. Reactive oxygen species-quenching and anti-apoptotic effect of polaprezinc on indomethacin-induced small intestinal epithelial cell injury. J Gastroenterol. 2010;45:692–702.
pubmed: 20174833
doi: 10.1007/s00535-010-0213-9
Kumar S. Caspase function in programmed cell death. Cell Death Differ. 2007;14:32–43.
pubmed: 17082813
doi: 10.1038/sj.cdd.4402060
Booth C, Tudor G, Tudor J, Katz BP, MacVittie TJ. Acute gastrointestinal syndrome in high-dose irradiated mice. Health Phys. 2012;103:383–99.
pubmed: 23091876
pmcid: 3530834
doi: 10.1097/HP.0b013e318266ee13
Zheng Y, Kong Y, Goetzl EJ. Lysophosphatidic acid receptor-selective effects on Jurkat T cell migration through a Matrigel model basement membrane. J Immunol. 2001;166:2317–22.
pubmed: 11160288
doi: 10.4049/jimmunol.166.4.2317
Knowlden S, Georas SN. The autotaxin-LPA axis emerges as a novel regulator of lymphocyte homing and inflammation. J Immunol. 2014;192:851–7.
pubmed: 24443508
doi: 10.4049/jimmunol.1302831
Hozumi H, Hokari R, Kurihara C, Narimatsu K, Sato H, Sato S, et al. Involvement of autotaxin/lysophospholipase D expression in intestinal vessels in aggravation of intestinal damage through lymphocyte migration. Lab Invest. 2013;93:508–19.
pubmed: 23478591
doi: 10.1038/labinvest.2013.45
Rahaman M, Costello RW, Belmonte KE, Gendy SS, Walsh MT. Neutrophil sphingosine 1-phosphate and lysophosphatidic acid receptors in pneumonia. Am J Respir Cell Mol Biol. 2006;34:233–41.
pubmed: 16224106
doi: 10.1165/rcmb.2005-0126OC
Saatian B, Zhao Y, He D, Georas SN, Watkins T, Spannhake EW, et al. Transcriptional regulation of lysophosphatidic acid-induced interleukin-8 expression and secretion by p38 MAPK and JNK in human bronchial epithelial cells. Biochem J. 2006;393:657–68.
pubmed: 16197369
pmcid: 1360718
doi: 10.1042/BJ20050791
Li Z, Yu Z, Wang D, Ju W, Zhan X, Wu Q, et al. Influence of acetylsalicylate on plasma lysophosphatidic acid level in patients with ischemic cerebral vascular diseases. Neurol Res. 2008;30:366–9.
pubmed: 18544253
doi: 10.1179/174313208X300369
Block RC, Duff R, Lawrence P, Kakinami L, Brenna JT, Shearer GC, et al. The effects of EPA, DHA, and aspirin ingestion on plasma lysophospholipids and autotaxin. Prostaglandins Leukot Ess Fat Acids. 2010;82:87–95.
doi: 10.1016/j.plefa.2009.12.005
Kehlen A, Lauterbach R, Santos A, Thiele K, Kabisch U, Weber E, et al. IL-1 beta- and IL-4-induced down-regulation of autotaxin mRNA and PC-1 in fibroblast-like synoviocytes of patients with rheumatoid arthritis (RA). Clin Exp Immunol. 2001;123:147–54.
pubmed: 11168012
pmcid: 1905967
doi: 10.1046/j.1365-2249.2001.01432.x
Zhang P, Chen Y, Zhang T, Zhu J, Zhao L, Li J, et al. Deficiency of alkaline SMase enhances dextran sulfate sodium-induced colitis in mice with upregulation of autotaxin. J Lipid Res. 2018;59:1841–50.
pubmed: 30087205
pmcid: 6168310
doi: 10.1194/jlr.M084285
Lin S, Haque A, Raeman R, Guo L, He P, Denning TL, et al. Autotaxin determines colitis severity in mice and is secreted by B cells in the colon. FASEB J. 2019;33:3623–35.
pubmed: 30481488
doi: 10.1096/fj.201801415RR
Mills GB, Moolenaar WH. The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer. 2003;3:582–91.
pubmed: 12894246
doi: 10.1038/nrc1143
Thun M, Henley S, Patrono C. Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst. 2002;94:252–66.
pubmed: 11854387
doi: 10.1093/jnci/94.4.252
Hull MA, Gardner SH, Hawcroft G. Activity of the non-steroidal anti-inflammatory drug indomethacin against colorectal cancer. Cancer Treat Rev. 2003;29:309–20.
pubmed: 12927571
doi: 10.1016/S0305-7372(03)00014-8
Wong RSY. Role of nonsteroidal anti-inflammatory drugs (NSAIDs) in cancer prevention and cancer promotion. Adv Pharmacol Sci. 2019;2019:3418975.
pubmed: 30838040
pmcid: 6374867
Kent TH, Cardelli RM, Stamler FW. Small intestinal ulcers and intestinal flora in rats given indomethacin. Am J Pathol. 1969;54:237–49.
pubmed: 5765565
pmcid: 2013470
Watanabe T, Nishio H, Tanigawa T, Yamagami H, Okazaki H, Watanabe K, et al. Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: involvement of lactic acid. Am J Physiol Gastrointest Liver Physiol. 2009;297:G506–13.
pubmed: 19589943
doi: 10.1152/ajpgi.90553.2008
Zadori ZS, Kiraly K, Al-Khrasani M, Gyires K. Interactions between NSAIDs, opioids and the gut microbiota—future perspectives in the management of inflammation and pain. Pharmacol Ther. 2023;241:108327.
pubmed: 36473615
doi: 10.1016/j.pharmthera.2022.108327
Colucci R, Pellegrini C, Fornai M, Tirotta E, Antonioli L, Renzulli C, et al. Pathophysiology of NSAID-associated intestinal lesions in the rat: luminal bacteria and mucosal inflammation as targets for prevention. Front Pharmacol. 2018;9:1340.
pubmed: 30555323
pmcid: 6281992
doi: 10.3389/fphar.2018.01340
D’Antongiovanni V, Antonioli L, Benvenuti L, Pellegrini C, Di Salvo C, Calvigioni M, et al. Use of Saccharomyces boulardii CNCM I-745 as therapeutic strategy for prevention of nonsteroidal anti-inflammatory drug-induced intestinal injury. Br J Pharmacol. 2023; in press.
Lin S, Han Y, Jenkin K, Lee SJ, Sasaki M, Klapproth JM, et al. Lysophosphatidic acid receptor 1 is important for intestinal epithelial barrier function and susceptibility to colitis. Am J Pathol. 2018;188:353–66.
pubmed: 29128569
pmcid: 5785539
doi: 10.1016/j.ajpath.2017.10.006
Liang Z, He P, Han Y, Yun CC. Survival of stem cells and progenitors in the intestine is regulated by LPA
pubmed: 35390517
pmcid: 9120264
doi: 10.1016/j.jcmgh.2022.03.012
Kotarsky K, Boketoft A, Bristulf J, Nilsson NE, Norberg A, Hansson S, et al. Lysophosphatidic acid binds to and activates GPR92, a G protein-coupled receptor highly expressed in gastrointestinal lymphocytes. J Pharmacol Exp Ther. 2006;318:619–28.
pubmed: 16651401
doi: 10.1124/jpet.105.098848
Oda SK, Strauch P, Fujiwara Y, Al-Shami A, Oravecz T, Tigyi G, et al. Lysophosphatidic acid inhibits CD8 T cell activation and control of tumor progression. Cancer Immunol Res. 2013;1:245–55.
pubmed: 24455753
pmcid: 3893823
doi: 10.1158/2326-6066.CIR-13-0043-T
Liang Z, Yun CC. Compensatory upregulation of LPA