Functional impact of PTP1B-mediated Src regulation on oxidative phosphorylation in rat brain mitochondria
Tóm tắt
Given the presence of Src and PTP1B within rat brain mitochondria, we have investigated whether PTP1B regulates Src activity in mitochondria as in the cytosol. Results showed that Src was stimulated by in vitro addition of ATP to mitochondria, and this stimulation was reversed by a membrane-permeable allosteric inhibitor of PTP1B and by a potent selective Src inhibitor. They also indicated a direct action of PTP1B on phosphorylated tyrosine 527 residue of Src, thus implicating a role for PTP1B in the modulation of Src activity in mitochondria. Putative Src and PTP1B substrates were identified by liquid chromatography tandem mass spectrometry and two-dimensional blue native/SDS-PAGE. Both inhibitors inhibited ADP-stimulated respirations concurrently with Src activation and complex IV activation by ATP, while having no effect or increasing the activity of the other complexes. Our analysis emphasizes the regulatory function of Src and its modulation by PTP1B on oxidative phosphorylation in mitochondria.
Tài liệu tham khảo
Navarro A, Boveris A (2007) The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292:C670–C686
Huttemann M, Lee I, Samavati L, Yu H, Doan JW (2007) Regulation of mitochondrial oxidative phosphorylation through cell signaling. Biochim Biophys Acta 1773:1701–1720
Horbinski C, Chu CT (2005) Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic Biol Med 38:2–11
Pagliarini DJ, Dixon JE (2006) Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem Sci 31:26–34
Salvi M, Brunati AM, Toninello A (2005) Tyrosine phosphorylation in mitochondria: a new frontier in mitochondrial signaling. Free Radic Biol Med 38:1267–1277
Miyazaki T, Neff L, Tanaka S, Horne WC, Baron R (2003) Regulation of cytochrome c oxidase activity by c-Src in osteoclasts. J Cell Biol 160:709–718
Miyazaki T, Tanaka S, Sanjay A, Baron R (2006) The role of c-Src kinase in the regulation of osteoclast function. Mod Rheumatol 16:68–74
Samavati L, Lee I, Mathes I, Lottspeich F, Huttemann M (2008) Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J Biol Chem 283:21134–21144
Salvi M, Morrice NA, Brunati AM, Toninello A (2007) Identification of the flavoprotein of succinate dehydrogenase and aconitase as in vitro mitochondrial substrates of Fgr tyrosine kinase. FEBS Lett 581:5579–5585
Di Pancrazio F, Bisetto E, Alverdi V, Mavelli I, Esposito G, Lippe G (2006) Differential steady-state tyrosine phosphorylation of two oligomeric forms of mitochondrial F0F1ATPsynthase: a structural proteomic analysis. Proteomics 6:921–926
Yu H, Lee I, Salomon AR, Yu K, Huttemann M (2008) Mammalian liver cytochrome c is tyrosine-48 phosphorylated in vivo, inhibiting mitochondrial respiration. Biochim Biophys Acta 1777:1066–1071
Feng J, Lucchinetti E, Enkavi G, Wang Y, Gehrig P, Roschitzki B, Schaub MC, Tajkhorshid E, Zaugg K, Zaugg M (2010) Tyrosine phosphorylation by Src within the cavity of the adenine nucleotide translocase 1 regulates ADP/ATP exchange in mitochondria. Am J Physiol Cell Physiol 298:C740–C748
Salvi M, Brunati AM, Bordin L, La Rocca N, Clari G, Toninello A (2002) Characterization and location of Src-dependent tyrosine phosphorylation in rat brain mitochondria. Biochim Biophys Acta 1589:181–195
Tibaldi E, Brunati AM, Massimino ML, Stringaro A, Colone M, Agostinelli E, Arancia G, Toninello A (2008) Src-Tyrosine kinases are major agents in mitochondrial tyrosine phosphorylation. J Cell Biochem 104:840–849
Augereau O, Claverol S, Boudes N, Basurko MJ, Bonneu M, Rossignol R, Mazat JP, Letellier T, Dachary-Prigent J (2005) Identification of tyrosine-phosphorylated proteins of the mitochondrial oxidative phosphorylation machinery. Cell Mol Life Sci 62:1478–1488
Salvi M, Stringaro A, Brunati AM, Agostinelli E, Arancia G, Clari G, Toninello A (2004) Tyrosine phosphatase activity in mitochondria: presence of Shp-2 phosphatase in mitochondria. Cell Mol Life Sci 61:2393–2404
Roskoski R Jr (2005) Src kinase regulation by phosphorylation and dephosphorylation. Biochem Biophys Res Commun 331:1–14
Roskoski R Jr (2004) Src protein-tyrosine kinase structure and regulation. Biochem Biophys Res Commun 324:1155–1164
Brown MT, Cooper JA (1996) Regulation, substrates and functions of Src. Biochim Biophys Acta 1287:121–149
Arachiche A, Augereau O, Decossas M, Pertuiset C, Gontier E, Letellier T, Dachary-Prigent J (2008) Localization of PTP-1B, SHP-2, and Src exclusively in rat brain mitochondria and functional consequences. J Biol Chem 283:24406–24411
Wiesmann C, Barr KJ, Kung J, Zhu J, Erlanson DA, Shen W, Fahr BJ, Zhong M, Taylor L, Randal M, McDowell RS, Hansen SK (2004) Allosteric inhibition of protein tyrosine phosphatase 1B. Nat Struct Mol Biol 11:730–737
Bain J, McLauchlan H, Elliott M, Cohen P (2003) The specificities of protein kinase inhibitors: an update. Biochem J 371:199–204
Clark JB, Nicklas WJ (1970) The metabolism of rat brain mitochondria. Preparation and characterization. J Biol Chem 245:4724–4731
Wittig I, Braun HP, Schagger H (2006) Blue native PAGE. Nat Protoc 1:418–428
Williams SL, Valnot I, Rustin P, Taanman JW (2004) Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1, or SURF1. J Biol Chem 279:7462–7469
Pocaly M, Lagarde V, Etienne G, Dupouy M, Lapaillerie D, Claverol S, Vilain S, Bonneu M, Turcq B, Mahon FX, Pasquet JM (2008) Proteomic analysis of an imatinib-resistant K562 cell line highlights opposing roles of heat shock cognate 70 and heat shock 70 proteins in resistance. Proteomics 8:2394–2406
Nishikawa Y, Ohi N, Yagisawa A, Doi Y, Yamamoto Y, Yoshida M, Tokairin T, Yoshioka T, Omori Y, Enomoto K (2009) Suppressive effect of orthovanadate on hepatic stellate cell activation and liver fibrosis in rats. Am J Pathol 174:881–890
Shani V, Bromberg Y, Sperling O, Zoref-Shani E (2009) Involvement of Src tyrosine kinases (SFKs) and of focal adhesion kinase (FAK) in the injurious mechanism in rat primary neuronal cultures exposed to chemical ischemia. J Mol Neurosci 37:50–59
Mohamed AS, Rivas-Plata KA, Kraas JR, Saleh SM, Swope SL (2001) Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J Neurosci 21:3806–3818
Newman DK (2009) The Y’s that bind: negative regulators of Src family kinase activity in platelets. J Thromb Haemost 7(Suppl 1):195–199
Stover DR, Furet P, Lydon NB (1996) Modulation of the SH2 binding specificity and kinase activity of Src by tyrosine phosphorylation within its SH2 domain. J Biol Chem 271:12481–12487
Yamaguchi H, Hendrickson WA (1996) Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384:484–489
Sondhi D, Xu W, Songyang Z, Eck MJ, Cole PA (1998) Peptide and protein phosphorylation by protein tyrosine kinase Csk: insights into specificity and mechanism. Biochemistry 37:165–172
Bjorge JD, Pang A, Fujita DJ (2000) Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J Biol Chem 275:41439–41446
Zhu S, Bjorge JD, Fujita DJ (2007) PTP1B contributes to the oncogenic properties of colon cancer cells through Src activation. Cancer Res 67:10129–10137
Harrison SC (2003) Variation on an Src-like theme. Cell 112:737–740
Villani G, Attardi G (1997) In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc Natl Acad Sci USA 94:1166–1171
Villani G, Greco M, Papa S, Attardi G (1998) Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J Biol Chem 273:31829–31836
D’Aurelio M, Pallotti F, Barrientos A, Gajewski CD, Kwong JQ, Bruno C, Beal MF, Manfredi G (2001) In vivo regulation of oxidative phosphorylation in cells harboring a stop-codon mutation in mitochondrial DNA-encoded cytochrome c oxidase subunit I. J Biol Chem 276:46925–46932
Hopper RK, Carroll S, Aponte AM, Johnson DT, French S, Shen RF, Witzmann FA, Harris RA, Balaban RS (2006) Mitochondrial matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry 45:2524–2536