Role of GSH/GSSG redox couple in osteogenic activity and osteoclastogenic markers of human osteoblast-like SaOS-2 cells

FEBS Journal

Volumn 280, Issue 3, 2013, Pages 867-879

  Romagnoli, Cecilia ^a   Marcucci, Gemma ^a   Favilli, Fabio ^a   Zonefrati, Roberto ^a   Mavilia, Carmelo ^a   Galli, Gianna ^a   Tanini, Annalisa ^a   Iantomasi, Teresa ^a   Brandi, Maria L ^a   Vincenzini, Maria T ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

bone remodeling; GSH GSSH redox couple; human osteoblast like cell line SaOS 2; osteoclastogenic markers; osteogenic differentiation

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TRANSCRIPTION FACTOR RUNX2;

ARTICLE; BONE MINERALIZATION; CALCIFICATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; OSTEOBLAST; OSTEOCLASTOGENESIS; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REGULATOR GENE; RUNX 2 GENE;

ACETYLCYSTEINE; BLOTTING, WESTERN; BUTHIONINE SULFOXIMINE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CORE BINDING FACTOR ALPHA 1 SUBUNIT; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; OSTEOPROTEGERIN; OXIDATION-REDUCTION; RANK LIGAND; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84873139186     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12075     Document Type: Article

References (55)

1. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, &, Telser J, (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44-84.
2. Catarzi S, Favilli F, Romagnoli C, Marcucci T, Picariello L, Tonelli F, Vincenzini MT, &, Iantomasi T, (2011) Oxidative state and IL-6 production in intestinal myofibroblasts of Crohn's disease patients. Inflamm Bowel Dis 17, 1674-1684.
3. 2. Biochem Biophys Res Commun 280, 1279-1285.
4. Rahman I, Biswas SK, Jimenez LA, Torres M, &, Forman HJ, (2005) Glutathione, stress responses, and redox signaling in lung inflammation. Antioxid Redox Signal 7, 42-59.
5. Townsend DM, Tew KD, &, Tapiero H, (2003) The importance of glutathione in human disease. Biomed Pharmacother 57, 145-155.
6. Biswas SK, &, Rahman I, (2009) Environmental toxicity, redox signaling and lung inflammation: the role of glutathione. Mol Aspects Med 30, 60-76.
7. 2 in the platelet-derived growth factor-induced transcription of the γ-glutamylcysteine synthetase heavy subunit. Cell Mol Life Sci 59, 1388-1394.
8. Jones DP, (2002) Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol 348, 93-112.
9. Mody N, Parhami F, Sarafian TA, &, Demer LL, (2001) Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med 31, 509-519.
10. Bai XC, Lu D, Bai J, Zheng H, Ke ZY, Li XM, &, Luo SQ, (2004) Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-κB. Biochem Biophys Res Commun 314, 197-207.
11. Lean JM, Jagger CJ, Kirstein B, Fuller K, &, Chambers TJ, (2005) Hydrogen peroxide is essential for estrogen-deficiency bone loss and osteoclast formation. Endocrinology 146, 728-735.
12. Huh YJ, Kim JM, Kim H, Song H, So H, Lee SY, Kwon SB, Kim HJ, Kim HH, Lee SH, et al,. (2006) Regulation of osteoclast differentiation by the redox-dependent modulation of nuclear import of transcription factors. Cell Death Differ 13, 1138-1146.
13. 2) on alkaline phosphatase activity and matrix mineralization of odontoblast and osteoblast cell lines. Cell Biol Toxicol 22, 39-46.
14. Jun JH, Lee SH, Kwak HB, Lee ZH, Seo SB, Woo KM, Ryoo HM, Kim GS, &, Baek JH, (2008) N-acetylcysteine stimulates osteoblastic differentiation of mouse calvarial cells. J Cell Biochem 103, 1246-1255.
15. Jagger CJ, Lean JM, Davies JT, &, Chambers TJ, (2005) Tumor necrosis factor-α mediates osteopenia caused by depletion of antioxidants. Endocrinology 146, 113-118.
16. Trost Z, Trebse R, Prezelj J, Komadina R, Logar DB, &, Marc J, (2010) A microarray based identification of osteoporosis-related genes in primary culture of human osteoblasts. Bone 46, 72-80.
17. Lean JM, Davies JT, Fuller K, Jagger CJ, Kirstein B, Partington GA, Urry ZL, &, Chambers TJ, (2003) A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J Clin Invest 112, 915-923.
18. Sendur OF, Turan Y, Tastaban E, &, Serter M, (2009) Antioxidant status in patients with osteoporosis: a controlled study. Joint Bone Spine 76, 514-518.
19. Tilg H, Moschen AR, Kaser A, Pines A, &, Dotan I, (2008) Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57, 684-694.
20. Bjelakovic̈ G, Beninati S, Pavlovic̈ D, Kocic̈ G, Jevtovic̈ T, Kamenov B, Saranac LJ, Bjelakovic̈ B, Stojanovic̈ I, &, Basic̈ J, (2007) Glucocorticoids and oxidative stress. J Basic Clin Physiol Pharmacol 18, 115-127.
21. Rodan SB, Imai Y, Thiede MA, Wesolowski G, Thompson D, Bar-Shavit Z, Shull S, Mann K, &, Rodan GA, (1987) Characterization of a human osteosarcoma cell line (Saos-2) with osteoblastic properties. Cancer Res 47, 4961-4966.
22. Boskey AL, &, Roy R, (2008) Cell culture systems for studies of bone and tooth mineralization. Chem Rev 108, 4716-4733.
23. Mamaeva SE, (1998) Karyotypic evolution of cells in culture: a new concept. Int Rev Cytol 178, 1-40.
24. McQuillan DJ, Richardson MD, &, Bateman JF, (1995) Matrix deposition by a calcifying human osteogenic sarcoma cell line (SAOS-2). Bone 16, 415-426.
25. Gundle R, &, Beresford JN, (1995) The isolation and culture of cells from explants of human trabecular bobe. Calcif Tissue Int 56, S8-S10.
26. Hausser HJ, &, Brenner RE, (2005) Phenotypic instability of Saos-2 cells in long-term culture. Biochem Biophys Res Commun 333, 216-222.
27. Fariss MW, &, Reed DJ, (1987) High-performance liquid chromatography of thiols and disulfides: dinitrophenol derivatives. Methods Enzymol 143, 101-109.
28. Kotobuki N, Matsushima A, Kato Y, Kubo Y, Hirose M, &, Ohgushi H, (2008) Small interfering RNA of alkaline phosphatase inhibits matrix mineralization. Cell Tissue Res 332, 279-288.
29. Komori T, (2006) Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 99, 1233-1239.
30. Coffman JA, (2003) Runx transcription factors and the developmental balance between cell proliferation and differentiation. Cell Biol Int 27, 315-324.
31. Javed A, Barnes GL, Pratap J, Antkowiak T, Gerstenfeld LC, van Wijnen AJ, Stein JL, Lian JB, &, Stein GS, (2005) Impaired intranuclear trafficking of Runx2 (AML3/CBFA1) transcription factors in breast cancer cells inhibits osteolysis in vivo. Proc Natl Acad Sci USA 102, 1454-1459.
32. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, Kennedy MB, Pockwinse S, Lian JB, &, Stein GS, (1990) Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143, 420-430.
33. Poser JW, Esch FS, Ling NC, &, Price PA, (1980) Isolation and sequence of the vitamin K-dependent protein from human bone. Undercarboxylation of the first glutamic acid residue. J Biol Chem 255, 8685-8691.
34. Catarzi S, Romagnoli C, Marcucci G, Favilli F, Iantomasi T, &, Vincenzini MT, (2011) Redox regulation of ERK1/2 activation induced by sphingosine 1-phosphate in fibroblasts: involvement of NADPH oxidase and platelet-derived growth factor receptor. Biochim Biophys Acta 1810, 446-456.
35. Ge C, Xiao G, Jiang D, &, Franceschi RT, (2007) Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol 176, 709-718.
36. Thomas GP, Baker SU, Eisman JA, &, Gardiner EM, (2001) Changing RANKL/OPG mRNA expression in differentiating murine primary osteoblasts. J Endocrinol 170, 451-460.
37. Nagai M, &, Sato N, (1999) Reciprocal gene expression of osteoclastogenesis inhibitory factor and osteoclast differentiation factor regulates osteoclast formation. Biochem Biophys Res Commun 257, 719-723.
38. Vincenzini MT, Favilli F, &, Iantomasi T, (1992) Intestinal uptake and transmembrane transport systems of intact GSH; characteristics and possible biological role. Biochim Biophys Acta 1113, 13-23.
39. Lu SC, Sun WM, Yi J, Ookhtens M, Sze G, &, Kaplowitz N, (1996) Role of two recently cloned rat liver GSH transporters in the ubiquitous transport of GSH in mammalian cells. J Clin Invest 97, 1488-1496.
40. Circu LM, &, Aw TY, (2012) Intestinal redox biology and oxidative stress. Semin Cell Dev Biol 23, 729-737.
41. Lash LH, (2009) Renal glutathione transport: identification of carriers, physiological functions, and controversies. BioFactors 35, 500-508.
42. Lu SC, (2009) Regulation of glutathione synthesis. Mol Aspects Med 30, 42-59.
43. Postiglione L, Domenico GD, Montagnani S, Spigna GD, Salzano S, Castaldo C, Ramaglia L, Sbordone L, &, Rossi G, (2003) Granulocyte-macrophage colony-stimulating factor (GM-CSF) induces the osteoblastic differentiation of the human osteosarcoma cell line SaOS-2. Calcif Tissue Int 72, 85-97.
44. Andela VB, Sheu TJ, Puzas EJ, Schwarz EM, O'Keefe RJ, &, Rosier RN, (2002) Malignant reversion of a human osteosarcoma cell line, Saos-2, by inhibition of NFκB. Biochem Biophys Res Commun 297, 237-241.
45. Uno K, Takarada T, Takarada-Iemata M, Nakamura Y, Fujita H, Hinoi E, &, Yoneda Y, (2011) Negative regulation of osteoblastogenesis through downregulation of runt-related transcription factor-2 in osteoblastic MC3T3-E1 cells with stable overexpression of the cystine/glutamate antiporter xCT subunit. Cell Physiol 226, 2953-2964.
46. Imhoff BR, &, Hansen JM, (2011) Differential redox potential profiles during adipogenesis and osteogenesis. Cell Mol Biol Lett 16, 149-161.
47. Deyama Y, Takeyama S, Suzuki K, Yoshimura Y, Nishikata M, &, Matsumoto A, (2001) Inactivation of NF-κB involved in osteoblast development through interleukin-6. Biochem Biophys Res Commun 282, 1080-1084.
48. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, &, Karsenty G, (1999) A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13, 1025-1036.
49. Du Y, Zhang H, Lu J, &, Holmgren A, (2012) Glutathione and glutaredoxin act as a backup of human thioredoxin reductase 1 to reduce thioredoxin 1 preventing cell death by aurothioglucose. J Biol Chem 287, 38210-38219.
50. Powis G, &, Kirkpatrick DL, (2007) Thioredoxin signaling as a target for cancer therapy. Curr Opin Pharmacol 7, 392-397.
51. Robinson JA, Harris SA, Riggs BL, &, Spelsberg TC, (1997) Estrogen regulation of human osteoblastic cell proliferation and differentiation. Endocrinology 138, 2919-2927.
52. Dalle Donne I, Rossi R, Giustarini D, Colombo R, &, Milzani A, (2007) S-glutathionylation in protein redox regulation. Free Radic Biol Med 43, 883-898.
53. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, &, Klenk DC, (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150, 76-85.
54. Bessey OA, Lowry OH, &, Brock MJ, (1946) A method for the rapid determination of alkaline phosphates with five cubic millimeters of serum. J Biol Chem 164, 321-329.
55. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.