Dose-dependent inhibitory effects of proton pump inhibitors on human osteoclastic and osteoblastic cell activity

FEBS Journal

Volumn 280, Issue 20, 2013, Pages 5052-5064

  Costa Rodrigues, João ^a   Reis, Sara ^a,b   Teixeira, Sónia ^a,b   Lopes, Sandra ^a   Fernandes, Maria H ^a  

^a Portugal   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

bone metabolism; intracellular signaling pathways; osteoblastic cells; osteoclastic cells; proton pump inhibitors

Indexed keywords

ESOMEPRAZOLE; LANSOPRAZOLE; OMEPRAZOLE; PROTON PUMP INHIBITOR;

APOPTOSIS; ARTICLE; BLOOD CELL; BONE MINERALIZATION; BONE TURNOVER; CELL ACTIVITY; CELL DENSITY; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; CELL TYPE; CONCENTRATION RESPONSE; DOSE RESPONSE; GENE EXPRESSION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MESENCHYMAL STEM CELL; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; STEM CELL CULTURE;

BONE METABOLISM; INTRACELLULAR SIGNALING PATHWAYS; OSTEOBLASTIC CELLS; OSTEOCLASTIC CELLS; PROTON PUMP INHIBITORS;

ADULT; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MALE; MONOCYTES; OSTEOBLASTS; OSTEOCLASTS; PROTON PUMP INHIBITORS; SIGNAL TRANSDUCTION;

EID: 84885320235     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12478     Document Type: Article

References (44)

1. Savarino V, Di Mario F, &, Scarpignato C, (2009) Proton pump inhibitors in GORD. An overview of their pharmacology, efficacy and safety. Pharmacol Res 59, 135-153.
2. Besancon M, Simon A, Sachs G, &, Shin JM, (1997) Sites of reaction of the gastric H, K-ATPase with extracytoplasmic thiol reagents. J Biol Chem 272, 22438-22446.
3. Lodato F, Azzaroli F, Turco L, Mazzella N, Buonfiglioli F, Zoli M, &, Mazzella G, (2010) Adverse effects of proton pump inhibitors. Best Pract Res Clin Gastroenterol 24, 193-201.
4. Martin RM, Dunn NR, Freemantle S, &, Shakir S, (2000) The rates of common adverse events reported during treatment with proton pump inhibitors used in general practice in England: Cohort studies. Br J Clin Pharmacol 50, 366-372.
5. Ye X, Liu H, Wu C, Qin Y, Zang J, Gao Q, Zhang X, &, He J, (2011) Proton pump inhibitor therapy and risk of hip fracture: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 23, 794-800.
6. Voelker R, (2010) Proton pump inhibitors linked to fracture risk. JAMA 304, 29.
7. Yang YX, Lewis JD, Epstein S, &, Metz DC, (2006) Long-term proton pump inhibitor therapy and risk of hip fracture. JAMA 296, 2947-2953.
8. Vestergaard P, Rejnmark L, &, Mosekilde L, (2006) Proton pump inhibitors, histamine H2 receptor antagonists, and other antacid medications and the risk of fracture. Calc Tissue Int 79, 76-83.
9. Targownik LE, Lix LM, Metge CJ, Prior HJ, Leung S, &, Leslie WD, (2008) Use of proton pump inhibitors and risk of osteoporosis-related fractures. CMAJ 179, 319-326.
10. Corley DA, Kubo A, Zhao W, &, Quesenberry C, (2010) Proton pump inhibitors and histamine-2 receptor antagonists are associated with hip fractures among at-risk patients. Gastroenterology 139, 93-101.
11. Yu EW, Blackwell T, Ensrud KE, Hillier TA, Lane NE, Orwoll E, &, Bauer DC, (2008) Acid-suppressive medications and risk of bone loss and fracture in older adults. Calc Tissue Int 83, 251-259.
12. Targownik LE, Lix LM, Leung S, &, Leslie WD, (2010) Proton-pump inhibitor use is not associated with osteoporosis or accelerated bone mineral density loss. Gastroenterology 138, 896-904.
13. O'Connell MB, Madden DM, Murray AM, Heaney RP, &, Kerzner LJ, (2005) Effects of proton pump inhibitors on calcium carbonate absorption in women: a randomized crossover trial. Am J Med 118, 778-781.
14. Hansen KE, Jones AN, Lindstrom MJ, Davis LA, Ziegler TE, Penniston KL, Alvig AL, &, Shafer MM, (2010) Do proton pump inhibitors decrease calcium absorption? J Bone Miner Res 25, 2786-2795.
15. Wright MJ, Sullivan RR, Gaffney-Stomberg E, Caseria DM, O'Brien KO, Proctor DD, Simpson CA, Kerstetter JE, &, Insogna KL, (2010) Inhibiting gastric acid production does not affect intestinal calcium absorption in young, healthy individuals: a randomized, crossover, controlled clinical trial. J Bone Miner Res 25, 2205-2211.
16. Zaidi M, (2007) Skeletal remodeling in health and disease. Nat Med 13, 791-801.
17. Datta HK, Ng WF, Walker JA, Tuck SP, &, Varanasi SS, (2008) The cell biology of bone metabolism. J Clin Pathol 61, 577-587.
18. +-ATPase, inhibits bone resorption in vitro. Calc Tissue Int 38, 123-125.
19. Zaidi M, (1990) Modularity of osteoclast behaviour and 'mode-specific' inhibition of osteoclast function. Biosci Rep 10, 547-556.
20. Mattsson JP, Vaananen K, Wallmark B, &, Lorentzon P, (1991) Omeprazole and bafilomycin, two proton pump inhibitors: differentiation of their effects on gastric, kidney and bone H(+)-translocating ATPases. Biochim Biophys Acta 1065, 261-268.
21. Hyun JJ, Chun HJ, Keum B, Seo YS, Kim YS, Jeen YT, Lee HS, Um SH, Kim CD, Ryu HS, et al,. (2010) Effect of omeprazole on the expression of transcription factors in osteoclasts and osteoblasts. Int J Mol Med 26, 877-883.
22. Sheraly AR, Lickorish D, Sarraf F, &, Davies JE, (2009) Use of gastrointestinal proton pump inhibitors to regulate osteoclast-mediated resorption of calcium phosphate cements in vivo. Curr Drug Deliv 6, 192-198.
23. Rzeszutek K, Sarraf F, &, Davies JE, (2003) Proton pump inhibitors control osteoclastic resorption of calcium phosphate implants and stimulate increased local reparative bone growth. J Craniofac Surg 14, 301-307.
24. Cottrell JA, Vales FM, Schachter D, Wadsworth S, Gundlapalli R, Kapadia R, &, O'Connor JP, (2010) Osteogenic activity of locally applied small molecule drugs in a rat femur defect model. J Biomed Biotechnol 2010, 597641.
25. Narisawa S, Harmey D, Yadav MC, O'Neill WC, Hoylaerts MF, &, Millan JL, (2007) Novel inhibitors of alkaline phosphatase suppress vascular smooth muscle cell calcification. J Bone Miner Res 22, 1700-1710.
26. Delomenede M, Buchet R, &, Mebarek S, (2009) Lansoprazole is an uncompetitive inhibitor of tissue-nonspecific alkaline phosphatase. Acta Biochim Pol 56, 301-305.
27. Roberts S, Narisawa S, Harmey D, Millan JL, &, Farquharson C, (2007) Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization. J Bone Miner Res 22, 617-627.
28. Andersson T, Holmberg J, Rohss K, &, Walan A, (1998) Pharmacokinetics and effect on caffeine metabolism of the proton pump inhibitors, omeprazole, lansoprazole, and pantoprazole. Br J Clin Pharmacol 45, 369-375.
29. Junghard O, Hassan-Alin M, &, Hasselgren G, (2002) The effect of the area under the plasma concentration vs time curve and the maximum plasma concentration of esomeprazole on intragastric pH. Eur J Clin Pharmacol 58, 453-458.
30. Zhao Q, Shao J, Chen W, &, Li YP, (2007) Osteoclast differentiation and gene regulation. Front Biosci 12, 2519-2529.
31. Costa-Rodrigues J, Fernandes A, &, Fernandes MH, (2011) Spontaneous and induced osteoclastogenic behaviour of human peripheral blood mononuclear cells and their CD14(+) and CD14(-) cell fractions. Cell Proliferat 44, 410-419.
32. Mizunashi K, Furukawa Y, Katano K, &, Abe K, (1993) Effect of omeprazole, an inhibitor of H+, K + -ATPase, on bone resorption in humans. Calc Tissue Int 53, 21-25.
33. Coelho MJ, &, Fernandes MH, (2000) Human bone cell cultures in biocompatibility testing. Part II: effect of ascorbic acid, beta- glycerophosphate and dexamethasone on osteoblastic differentiation. Biomaterials 21, 1095-1102.
34. Matsuo K, &, Irie N, (2008) Osteoclast-osteoblast communication. Arch Biochem Biophys 473, 201-209.
35. Baron R, &, Horne CW, (2005) Regulation of osteoclast activity. In Bone Resorption (, Bronner F, Farach-Carson MC, &, Rubin J, eds), pp. 34-46. Springer Science, London, UK.
36. Xiao G, Jiang D, Thomas P, Benson MD, Guan K, Karsenty G, &, Franceschi RT, (2000) MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J Biol Chem 275, 4453-4459.
37. Udelnow A, Kreyes A, Ellinger S, Landfester K, Walther P, Klapperstueck T, Wohlrab J, Henne-Bruns D, Knippschild U, &, Würl P, (2011) Omeprazole inhibits proliferation and modulates autophagy in pancreatic cancer cells. PLoS ONE 6, e20143.
38. Yeo M, Kim DK, Kim YB, Oh TY, Lee JE, Cho SW, Kim HC, &, Hahm KB, (2004) Selective induction of apoptosis with proton pump inhibitor in gastric cancer cells. Clin Cancer Res 10, 8687-8696.
39. Hall TJ, (1994) Cytotoxicity of vacuolar H(+)-ATPase inhibitors to UMR-106 rat osteoblasts: an effect on iron uptake into cells? Cell Biol Int 18, 189-193.
40. Francis MJ, Lees RL, Trujillo E, Martín-Vasallo P, Heersche JNM, &, Mobasheri A, (2002) ATPase pumps in osteoclasts and osteoblasts. Int J Biochem Cell Biol 34, 459-476.
41. Rodan GA, &, Martin TJ, (2000) Therapeutic approaches to bone diseases. Science 289, 1508-1514.
42. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
43. Vaananen HK, &, Laitala-Leinonen T, (2008) Osteoclast lineage and function. Arch Biochem Biophys 473, 132-138.
44. Lian JB, Stein GS, Javed A, van Wijnen AJ, Stein JL, Montecino M, Hassan MQ, Gaur T, Lengner CJ, &, Young DW, (2006) Networks and hubs for the transcriptional control of osteoblastogenesis. Rev Endocr Metab Disord 7, 1-16.