Shotgun proteomics analysis reveals new unsuspected molecular effectors of nitrogen-containing bisphosphonates in osteocytes

Journal of Proteomics

Volumn 74, Issue 7, 2011, Pages 1113-1122

  Bivi, Nicoletta ^a   Picotti, Paola ^b   Müller, Lukas N ^b   Romanello, Milena ^a   Moro, Luigi ^c   Quadrifoglio, Franco ^a   Tell, Gianluca ^a  

^a UNIVERSITY OF UDINE   (Italy)

^b Institute of Molecular Systems Biology   (Switzerland)

^c UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Bisphosphonates; Osteocytes; Proteomics; Shot gun

Indexed keywords

DJ 1 PROTEIN; PROGRANULIN; PROTEIN KINASE B; RISEDRONIC ACID;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; LOW DRUG DOSE; MOUSE; NONHUMAN; OSTEOCYTE; OSTEOPOROSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PRENYLATION; PROTEOMICS;

ANIMALS; BLOTTING, WESTERN; BONE DENSITY CONSERVATION AGENTS; DIPHOSPHONATES; ETIDRONIC ACID; GENE EXPRESSION PROFILING; MICE; OSTEOCYTES; PROTEIN PRENYLATION; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; TANDEM MASS SPECTROMETRY;

EID: 79957636548     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.04.002     Document Type: Article

References (44)

1. Dunford J.E., Kwaasi A.A., Rogers M.J., Barnett B.L., Ebetino F.H., Russell R.G., et al. Structure-activity relationships among the nitrogen containing bisphosphonates in clinical use and other analogues: time-dependent inhibition of human farnesyl pyrophosphate synthase. J Med Chem 2008, 51:2187-2195.
2. Coxon F.P., Thompson K., Rogers M.J. Recent advances in understanding the mechanism of action of bisphosphonates. Curr Opin Pharmacol 2006, 6:307-312.
3. Luckman S.P., Hughes D.E., Coxon F.P., Graham R., Russell G., Rogers M.J. Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras. J Bone Miner Res 1998, 13:581-589.
4. Kavanagh K.L., Guo K., Dunford J.E., Wu X., Knapp S., Ebetino F.H., et al. The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs. Proc Natl Acad Sci USA 2006, 103:7829-7834.
5. Dunford J.E., Rogers M.J., Ebetino F.H., Phipps R.J., Coxon F.P. Inhibition of protein prenylation by bisphosphonates causes sustained activation of Rac, Cdc42, and Rho GTPases. J Bone Miner Res 2006, 21:684-694.
6. Coxon F.P., Thompson K., Roelofs A.J., Ebetino F.H., Rogers M.J. Visualizing mineral binding and uptake of bisphosphonate by osteoclasts and non-resorbing cells. Bone 2008, 42:848-860.
7. Plotkin L.I., Weinstein R.S., Parfitt A.M., Roberson P.K., Manolagas S.C., Bellido T. Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest 1999, 104:1363-1374.
8. Plotkin L.I., Lezcano V., Thostenson J., Weinstein R.S., Manolagas S.C., Bellido T. Connexin 43 is required for the anti-apoptotic effect of bisphosphonates on osteocytes and osteoblasts in vivo. J Bone Miner Res 2008, 23:1712-1721.
9. Plotkin L.I., Aguirre J.I., Kousteni S., Manolagas S.C., Bellido T. Bisphosphonates and estrogens inhibit osteocyte apoptosis via distinct molecular mechanisms downstream of extracellular signal-regulated kinase activation. J Biol Chem 2005, 280:7317-7325.
10. Romanello M., Bivi N., Pines A., Deganuto M., Quadrifoglio F., Moro L., et al. Bisphosphonates activate nucleotide receptors signaling and induce the expression of Hsp90 in osteoblast-like cell lines. Bone 2006, 39:739-753.
11. Noble B.S., Reeve J. Osteocyte function, osteocyte death and bone fracture resistance. Mol Cell Endocrinol 2000, 159:7-13.
12. Tatsumi S., Ishii K., Amizuka N., Li M., Kobayashi T., Kohno K., et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 2007, 5:464-475.
13. Aebersold R., Mann M. Mass spectrometry-based proteomics. Nature 2003, 422:198-207.
14. Aebersold R. Quantitative proteome analysis: methods and applications. J Infect Dis 2003, 187(Suppl 2):S315-S320.
15. Kato Y., Windle J.J., Koop B.A., Mundy G.R., Bonewald L.F. Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res 1997, 12:2014-2023.
16. Picotti P., Aebersold R. The implications of proteolytic background for shotgun proteomics. Mol Cell Proteomics 2007, 6:1589-1598.
17. Link A.J., Eng J., Schieltz D.M., Carmack E., Mize G.J., Morris D.R., et al. Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 1999, 17:676-682.
18. Mueller L.N., Rinner O., Schmidt A., Letarte S., Bodenmiller B., Brusniak M.Y., et al. SuperHirn - a novel tool for high resolution LC-MS-based peptide/protein profiling. Proteomics 2007, 7:3470-3480.
19. Higdon R., Hogan J.M., Kolker N., van Belle G., Kolker E. Experiment-specific estimation of peptide identification probabilities using a randomized database. OMICS 2007, 11:351-365.
20. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392.
21. Deutsch E.W. A guided tour of the trans-proteomic pipeline. Proteomics 2010, 10:1150-1159.
22. Elias J.E., Gygi S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 2007, 4:207-214.
23. Bivi N., Bereszczak J.Z., Romanello M., Zeef L.A., Delneri D., Quadrifoglio F., et al. Transcriptome and proteome analysis of osteocytes treated with nitrogen-containing bisphosphonates. J Proteome Res 2009, 8:1131-1142.
24. Hengst U., Albrecht H., Hess D., Monard D. The phosphatidylethanolamine-binding protein is the prototype of a novel family of serine protease inhibitors. J Biol Chem 2001, 276:535-540.
25. Bornhauser B.C., Olsson P.A., Lindholm D. MSAP is a novel MIR-interacting protein that enhances neurite outgrowth and increases myosin regulatory light chain. J Biol Chem 2003, 278:35412-35420.
26. Coxon F.P., Helfrich M.H., Larijani B., Muzylak M., Dunford J.E., Marshall D., et al. Identification of a novel phosphonocarboxylate inhibitor of Rab geranylgeranyl transferase that specifically prevents Rab prenylation in osteoclasts and macrophages. J Biol Chem 2001, 276:48213-48222.
27. Frith J.C., Monkkonen J., Auriola S., Monkkonen H., Rogers M.J. The molecular mechanism of action of the antiresorptive and antiinflammatory drug clodronate: evidence for the formation in vivo of a metabolite that inhibits bone resorption and causes osteoclast and macrophage apoptosis. Arthritis Rheum 2001, 44:2201-2210.
28. Kim R.H., Peters M., Jang Y., Shi W., Pintilie M., Fletcher G.C., et al. DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 2005, 7:263-273.
29. Paez J., Sellers W.R. PI3K/PTEN/AKT pathway. A critical mediator of oncogenic signaling. Cancer Treat Res 2003, 115:145-167.
30. Wang W., Hayashi J., Kim W.E., Serrero G. PC cell-derived growth factor (granulin precursor) expression and action in human multiple myeloma. Clin Cancer Res 2003, 9:2221-2228.
31. Plotkin L.I., Manolagas S.C., Bellido T. Dissociation of the pro-apoptotic effects of bisphosphonates on osteoclasts from their anti-apoptotic effects on osteoblasts/osteocytes with novel analogs. Bone 2006, 39:443-452.
32. Guo D., Keightley A., Guthrie J., Veno P.A., Harris S.E., Bonewald L.F. Identification of osteocyte-selective proteins. Proteomics 2010, 10:3688-3698.
33. Gomes F.C., Paulin D., Moura Neto V. Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz J Med Biol Res 1999, 32:619-631.
34. Kasantikul V., Shuangshoti S. Positivity to glial fibrillary acidic protein in bone, cartilage, and chondroma. J Surg Oncol 1989, 41:22-26.
35. Chipoy C., Berreur M., Couillaud S., Pradal G., Vallette F., Colombeix C., et al. Downregulation of osteoblast markers and induction of the glial fibrillary acidic protein by oncostatin M in osteosarcoma cells require PKCdelta and STAT3. J Bone Miner Res 2004, 19:1850-1861.
36. Stresing V., Fournier P.G., Bellahcène A., Benzaïd I., Mönkkönen H., Colombel M., et al. Nitrogen-containing bisphosphonates can inhibit angiogenesis in vivo without the involvement of farnesyl pyrophosphate synthase. Bone 2011, 48(2):259-266.
37. Tang X., Zhang Q., Shi S., Yen Y., Li X., Zhang Y., et al. Bisphosphonates suppress insulin-like growth factor 1-induced angiogenesis via the HIF-1alpha/VEGF signaling pathways in human breast cancer cells. Int J Cancer 2010, 126(1):90-103.
38. Inoue R., Matsuki N.A., Jing G., Kanematsu T., Abe K., Hirata M. The inhibitory effect of alendronate, a nitrogen-containing bisphosphonate on the PI3K-Akt-NFkappaB pathway in osteosarcoma cells. Br J Pharmacol 2005, 146(5):633-641.
39. Bivi N., Romanello M., Harrison R., Clarke I., Hoyle D.C., Moro L., et al. Identification of secondary targets of N-containing bisphosphonates in mammalian cells via parallel competition analysis of the barcoded yeast deletion collection. Genome Biol 2009, 10(9):R93.
40. He Z., Bateman A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J Mol Med 2003, 81:600-612.
41. Monami G., Gonzalez E.M., Hellman M., Gomella L.G., Baffa R., Iozzo R.V., et al. Proepithelin promotes migration and invasion of 5637 bladder cancer cells through the activation of ERK1/2 and the formation of a paxillin/FAK/ERK complex. Cancer Res 2006, 66:7103-7110.
42. Zanocco-Marani T., Bateman A., Romano G., Valentinis B., He Z.H., Baserga R. Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res 1999, 59:5331-5340.
43. Zhu J., Nathan C., Jin W., Sim D., Ashcroft G.S., Wahl S.M., et al. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 2002, 111:867-878.
44. Bai X.H., Wang D.W., Kong L., Zhang Y., Luan Y., Kobayashi T., et al. ADAMTS-7. a direct target of PTHrP, adversely regulates endochondral bone growth by associating with and inactivating GEP growth factor. Mol Cell Biol 2009, 29:4201-4219.