Please wait a minute...
Shopping Cart Email List Chinese
Advanced Search Fig/Tab
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Featured Articles  |  Most Downloaded  |  Most Reading
Online Submission Subscribe to Our RSS Content Feed
Front Biol    0, Vol. Issue () : 156-169    https://doi.org/10.1007/s11515-011-1112-z
REVIEW
Kinases and glutathione transferases: selective and sensitive targeting
Yasemin G. ISGOR, Belgin S. ISGOR()
Chemistry Group, Faculty of Engineering, Atilim University, Ankara 06836, Turkey
 Download: PDF(697 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Kinases, representing almost 500 proteins in the human genome, are responsible for catalyzing the phosphorylation reaction of amino acid residues at their targets. As the largest family of kinases, the protein tyrosine kinases (PTKs) have roles in controlling the essential cellular activities, and their deregulation is generally related to pathologic conditions. The recent efforts on identifying their signal transducer or mediator role in cellular signaling revealed the interaction of PTKs with numerous enzymes of different classes, such as Ser/Thr kinases (STKs), glutathione transferases (GSTs), and receptor tyrosine kinases (RTKs). In either regulation or enhancing the signaling, PTKs are determined in close interaction with these enzymes, under specific cellular conditions, such as oxidative stress and inflammation. In this concept, intensive research on thiol metabolizing enzymes recently showed their involvement in the physiologic functions in cellular signaling besides their well known traditional role in antioxidant defense. The shared signaling components between PTK and GST family enzymes will be discussed in depth in this research review to evaluate the results of recent studies important in drug targeting for therapeutic intervention, such as cell viability, migration, differentiation and proliferation.
Keywords glutathione transferase      protein tyrosine kinase      small molecule inhibitors      c-Src      signal transduction      drug targeting     
Corresponding Author(s): ISGOR Belgin S.,Email:bisgor@atilim.edu.tr   
Issue Date: 01 April 2011
 Cite this article:   
Yasemin G. ISGOR,Belgin S. ISGOR. Kinases and glutathione transferases: selective and sensitive targeting[J]. Front Biol, 0, (): 156-169.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-011-1112-z
https://academic.hep.com.cn/fib/EN/Y0/V/I/156
Fig.1  The ribbon diagram for the crystal structure of human c-Src complexed with anticancer drug imatinib (A) is adapted from Protein DataBank Accession No: 1Y57. The linear representation of functional domains of c-Src with opposing regulatory Tyr(Y) residues is shown (B). The inactive (C) and active (D) conformational change is illustrated. The cartoon also shows the membrane attachment through N-myristoylated tail (C and D).
Fig.1  The ribbon diagram for the crystal structure of human c-Src complexed with anticancer drug imatinib (A) is adapted from Protein DataBank Accession No: 1Y57. The linear representation of functional domains of c-Src with opposing regulatory Tyr(Y) residues is shown (B). The inactive (C) and active (D) conformational change is illustrated. The cartoon also shows the membrane attachment through N-myristoylated tail (C and D).
Fig.2  The ribbon diagram for crystal structure of the human GST A4 monomer (single subunit) representing secondary (hydrophobic) substrate and GSH binding sites. Adapted from Protein DataBank, accession number: 1GUL.
Fig.2  The ribbon diagram for crystal structure of the human GST A4 monomer (single subunit) representing secondary (hydrophobic) substrate and GSH binding sites. Adapted from Protein DataBank, accession number: 1GUL.
Fig.3  The ribbon diagrams for the crystal structures of human GSTs complexed with GSH and inhibitors. Except for MGST-1, all isoforms shown here are homodimers. The representations were adapted from Protein DataBank with accession numbers: 1PKW (GST A1-1), 11GS (GST P1-1), 1YJ6 (GST M1-1), 2C3N (GST T1-1), 1YZX (GST K1-1), 1EEM (GST O1-1), 1FW1 (GST Z1-1), and 2H8A (MGST-1).
Fig.3  The ribbon diagrams for the crystal structures of human GSTs complexed with GSH and inhibitors. Except for MGST-1, all isoforms shown here are homodimers. The representations were adapted from Protein DataBank with accession numbers: 1PKW (GST A1-1), 11GS (GST P1-1), 1YJ6 (GST M1-1), 2C3N (GST T1-1), 1YZX (GST K1-1), 1EEM (GST O1-1), 1FW1 (GST Z1-1), and 2H8A (MGST-1).
Fig.4  Recently published c-Src mediated signaling pathways. Under different physiological conditions some of the cellular reactions are presented, where c-Src is either signaling or regulatory component. A few phosphorylated proteins upon aberrant activation of c-Src are demonstrated to reflect the latest findings in the field. The c-Src activation summarized here with blue arrows are due to direct interaction with RTKs, except EGFR which is not shown for simplification. The black arrows correspond to the involvement of external or internal ROS in c-Src regulation. The downstream effects upon c-Src phosphorylation through RTKs or ROS are represented with green arrows. The purple arrows are used to demonstrate c-Src-FAK complex formation and related downstream effects. Here, E-Cad stands for E-cadherin and P for phosphorylation (upon c-Src action). The dashed line (red) stands for the direct inhibition of the target (PTEN), and solid lines correspond to the established interactions such as activation of enzymes, transcription factors (TFs) or initiation of translation, where the mechanism is almost clarified to date. Proteins with dark shades represent the enzymes critical for cell physiology for both normal and pathologic conditions.
Fig.4  Recently published c-Src mediated signaling pathways. Under different physiological conditions some of the cellular reactions are presented, where c-Src is either signaling or regulatory component. A few phosphorylated proteins upon aberrant activation of c-Src are demonstrated to reflect the latest findings in the field. The c-Src activation summarized here with blue arrows are due to direct interaction with RTKs, except EGFR which is not shown for simplification. The black arrows correspond to the involvement of external or internal ROS in c-Src regulation. The downstream effects upon c-Src phosphorylation through RTKs or ROS are represented with green arrows. The purple arrows are used to demonstrate c-Src-FAK complex formation and related downstream effects. Here, E-Cad stands for E-cadherin and P for phosphorylation (upon c-Src action). The dashed line (red) stands for the direct inhibition of the target (PTEN), and solid lines correspond to the established interactions such as activation of enzymes, transcription factors (TFs) or initiation of translation, where the mechanism is almost clarified to date. Proteins with dark shades represent the enzymes critical for cell physiology for both normal and pathologic conditions.
Fig.5  Recent advancements in GST involved signaling pathways. Under different physiological conditions, GST isozymes appear to function in regulation or in signaling as substrates for various kinases. The positive effect of RTKs on GST expression is shown but detail not given. The protein components interacting with GSTs or inducing their expression are shown with dark gray shades. The amino acid residues important in GST activation upon STK or PTK catalysis are given in light gray shades. GST stands for all soluble isozymes unless any symbol for specific isozyme was used with. In the figure, P corresponds to phosphorylation (after kinase action), and S (on the outside of shapes representing GSTs) stands for the thiol group of GST required for dimerization. It should be noted that the dimerization of GSTs, transferred from nucleus to cytosol, is not shown to simplify the presentation.
Fig.5  Recent advancements in GST involved signaling pathways. Under different physiological conditions, GST isozymes appear to function in regulation or in signaling as substrates for various kinases. The positive effect of RTKs on GST expression is shown but detail not given. The protein components interacting with GSTs or inducing their expression are shown with dark gray shades. The amino acid residues important in GST activation upon STK or PTK catalysis are given in light gray shades. GST stands for all soluble isozymes unless any symbol for specific isozyme was used with. In the figure, P corresponds to phosphorylation (after kinase action), and S (on the outside of shapes representing GSTs) stands for the thiol group of GST required for dimerization. It should be noted that the dimerization of GSTs, transferred from nucleus to cytosol, is not shown to simplify the presentation.
1 Abe J, Takahashi M, Ishida M, Lee J D, Berk B C (1997). c-Src is required for oxidative stress-mediated activation of big mitogen-activated protein kinase 1. J Biol Chem , 272(33): 20389–20394
doi: 10.1074/jbc.272.33.20389 pmid:9252345
2 Adler V, Pincus M R (2004). Effector peptides from glutathione-S-transferase-pi affect the activation of jun by jun-N-terminal kinase. Ann Clin Lab Sci , 34(1): 35–46
pmid:15038666
3 Adler V, Yin Z, Fuchs S Y, Benezra M, Rosario L, Tew K D, Pincus M R, Sardana M, Henderson C J, Wolf C R, Davis R J, Ronai Z (1999a). Regulation of JNK signaling by GSTp. EMBO J , 18(5): 1321–1334
doi: 10.1093/emboj/18.5.1321 pmid:10064598
4 Adler V, Yin Z, Tew K D, Ronai Z (1999b). Role of redox potential and reactive oxygen species in stress signaling. Oncogene , 18(45): 6104–6111
doi: 10.1038/sj.onc.1203128 pmid:10557101
5 Allan J M, Wild C P, Rollinson S, Willett E V, Moorman A V, Dovey G J, Roddam P L, Roman E, Cartwright R A, Morgan G J (2001). Polymorphism in glutathione S-transferase P1 is associated with susceptibility to chemotherapy-induced leukemia. Proc Natl Acad Sci USA , 98(20): 11592–11597
doi: 10.1073/pnas.191211198 pmid:11553769
6 Alvarez R H, Kantarjian H M, Cortes J E (2006). The role of Src in solid and hematologic malignancies: development of new-generation Src inhibitors. Cancer , 107(8): 1918–1929
doi: 10.1002/cncr.22215 pmid:16986126
7 Ayd?n D, Isgor B S, Isgor Y G, Olgen S, (2010). Evaluation of Novel Indole-3-Imine-2-On Derivatives As Src Kinase and Mammalian Glutathione S-Transferase Inhibitors. 3rd International Meeting on Pharmacy and Pharmaceutical Sciences. Istanbul, Turkey : 119
8 Baez S, Segura-Aguilar J, Widersten M, Johansson A S, Mannervik B (1997). Glutathione transferases catalyse the detoxication of oxidized metabolites (o-quinones) of catecholamines and may serve as an antioxidant system preventing degenerative cellular processes. Biochem J , 324(Pt 1): 25–28
pmid:9164836
9 Ben-Bassat H, Klein B Y (2000). Inhibitors of tyrosine kinases in the treatment of psoriasis. Curr Pharm Des , 6(9): 933–942
doi: 10.2174/1381612003400182 pmid:10828317
10 Berrier A L, Yamada K M (2007). Cell-matrix adhesion. J Cell Physiol , 213(3): 565–573
doi: 10.1002/jcp.21237 pmid:17680633
11 Bjorge J D, Jakymiw A, Fujita D J (2000). Selected glimpses into the activation and function of Src kinase. Oncogene , 19(49): 5620–5635
doi: 10.1038/sj.onc.1203923 pmid:11114743
12 Board P G, Coggan M, Chelvanayagam G, Easteal S, Jermiin L S, Schulte G K, Danley D E, Hoth L R, Griffor M C, Kamath A V, Rosner M H, Chrunyk B A, Perregaux D E, Gabel C A, Geoghegan K F, Pandit J (2000). Identification, characterization, and crystal structure of the Omega class glutathione transferases. J Biol Chem , 275(32): 24798–24806
doi: 10.1074/jbc.M001706200 pmid:10783391
13 Bordeleau F, Galarneau L, Gilbert S, Loranger A, Marceau N (2010). Keratin 8/18 modulation of protein kinase C-mediated integrin-dependent adhesion and migration of liver epithelial cells. Mol Biol Cell , 21(10): 1698–1713
doi: 10.1091/mbc.E09-05-0373 pmid:20357007
14 Carlucci A, Gedressi C, Lignitto L, Nezi L, Villa-Moruzzi E, Avvedimento E V, Gottesman M, Garbi C, Feliciello A (2008). Protein-tyrosine phosphatase PTPD1 regulates focal adhesion kinase autophosphorylation and cell migration. J Biol Chem , 283(16): 10919–10929
doi: 10.1074/jbc.M707248200 pmid:18223254
15 Chiarugi P, Pani G, Giannoni E, Taddei L, Colavitti R, Raugei G, Symons M, Borrello S, Galeotti T, Ramponi G (2003). Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J Cell Biol , 161(5): 933–944
doi: 10.1083/jcb.200211118 pmid:12796479
16 Cohen P (2000). The regulation of protein function by multisite phosphorylation—a 25 year update. Trends Biochem Sci , 25(12): 596–601
doi: 10.1016/S0968-0004(00)01712-6 pmid:11116185
17 Cohen S, Fleischmann R (2010). Kinase inhibitors: a new approach to rheumatoid arthritis treatment. Curr Opin Rheumatol , 22(3): 330–335
doi: 10.1097/BOR.0b013e3283378e6f pmid:20164774
18 Cowan-Jacob S W, Fendrich G, Manley P W, Jahnke W, Fabbro D, Liebetanz J, Meyer T (2005). The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation. Structure , 13(6): 861–871
doi: 10.1016/j.str.2005.03.012 pmid:15939018
19 Crout C A, Koh L P, Gockerman J P, Moore J O, Decastro C, Long G D, Diehl L, Gasparetto C, Niedzwiecki D, Edwards J, Prosnitz L, Horwitz M, Chute J, Morris A, Davis P, Beaven A, Chao N J, Ali-Osman F, Rizzieri D A (2010). Overcoming drug resistance in mantle cell lymphoma using a combination of dose-dense and intense therapy. Cancer Invest , 28(6): 654–660
doi: 10.3109/07357901003631015 pmid:20521909
20 Desmots F, Rissel M, Gilot D, Lagadic-Gossmann D, Morel F, Guguen-Guillouzo C, Guillouzo A, Loyer P (2002). Pro-inflammatory cytokines tumor necrosis factor alpha and interleukin-6 and survival factor epidermal growth factor positively regulate the murine GSTA4 enzyme in hepatocytes. J Biol Chem , 277(20): 17892–17900
doi: 10.1074/jbc.M112351200 pmid:11884396
21 Di Pietro G, Magno L A, Rios-Santos F (2010). Glutathione S-transferases: an overview in cancer research. Expert Opin Drug Metab Toxicol , 6(2): 153–170
doi: 10.1517/17425250903427980 pmid:20078251
22 Dincer S, Isgor B S, Isgor Y G, Olgen S (2010). Evaluation of Benzimidazole Derivatives as Src Kinase and Mammalian Glutathione S-Transferase Inhibitors. Joint Meeting of 4th International Meeting on Medicinal and Pharmaceutical Chemistry (IMMPC-4) and 6th International Symposium on Pharmaceutical Chemistry (ISPC-6). Ankara, Turkey
23 Eaton D L, Bammler T K (1999). Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol Sci , 49(2): 156–164
doi: 10.1093/toxsci/49.2.156 pmid:10416260
24 Edelman A M, Blumenthal D K, Krebs E G (1987). Protein serine/threonine kinases. Annu Rev Biochem , 56: 567–613
pmid:2956925
25 Frame M C (2002). Src in cancer: deregulation and consequences for cell behaviour. Biochim Biophys Acta , 1602(2): 114–130
pmid:12020799
26 Gate L, Majumdar R S, Lunk A, Tew K D (2004). Increased myeloproliferation in glutathione S-transferase pi-deficient mice is associated with a deregulation of JNK and Janus kinase/STAT pathways. J Biol Chem , 279(10): 8608–8616
doi: 10.1074/jbc.M308613200 pmid:14684749
27 Giamas G, Man Y L, Hirner H, Bischof J, Kramer K, Khan K, Ahmed S S, Stebbing J, Knippschild U (2010). Kinases as targets in the treatment of solid tumors. Cell Signal , 22(7): 984–1002
doi: 10.1016/j.cellsig.2010.01.011 pmid:20096351
28 Giannoni E, Buricchi F, Raugei G, Ramponi G, Chiarugi P (2005). Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol , 25(15): 6391–6403
doi: 10.1128/MCB.25.15.6391-6403.2005 pmid:16024778
29 Grahn E, Novotny M, Jakobsson E, Gustafsson A, Grehn L, Olin B, Madsen D, Wahlberg M, Mannervik B, Kleywegt G J (2006). New crystal structures of human glutathione transferase A1-1 shed light on glutathione binding and the conformation of the C-terminal helix. Acta Crystallogr D Biol Crystallogr , 62(Pt 2): 197–207
doi: 10.1107/S0907444905039296 pmid:16421451
30 Griffith D, Parker J P, Marmion C J (2010). Enzyme inhibition as a key target for the development of novel metal-based anti-cancer therapeutics. Anticancer Agents Med Chem , 10(5): 354–370
pmid:20380633
31 Gulick A M, Fahl W E (1995). Forced evolution of glutathione S-transferase to create a more efficient drug detoxication enzyme. Proc Natl Acad Sci USA , 92(18): 8140–8144
doi: 10.1073/pnas.92.18.8140 pmid:7667259
32 Ha C H, Bennett A M, Jin Z G (2008). A novel role of vascular endothelial cadherin in modulating c-Src activation and downstream signaling of vascular endothelial growth factor. J Biol Chem , 283(11): 7261–7270
doi: 10.1074/jbc.M702881200 pmid:18180305
33 Hao Q, Rutherford S A, Low B, Tang H (2006). Suppression of the phosphorylation of receptor tyrosine phosphatase-alpha on the Src-independent site tyrosine 789 by reactive oxygen species. Mol Pharmacol , 69(6): 1938–1944
doi: 10.1124/mol.105.020115 pmid:16505154
34 Harir N, Pecquet C, Kerenyi M, Sonneck K, Kovacic B, Nyga R, Brevet M, Dhennin I, Gouilleux-Gruart V, Beug H, Valent P, Lassoued K, Moriggl R, Gouilleux F (2007). Constitutive activation of Stat5 promotes its cytoplasmic localization and association with PI3-kinase in myeloid leukemias. Blood , 109(4): 1678–1686
doi: 10.1182/blood-2006-01-029918 pmid:17038539
35 Hayes J D, Flanagan J U, Jowsey I R (2005). Glutathione transferases. Annu Rev Pharmacol Toxicol , 45(1): 51–88
doi: 10.1146/annurev.pharmtox.45.120403.095857 pmid:15822171
36 Hayes J D, Pulford D J (1995). The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol , 30(6): 445–600
doi: 10.3109/10409239509083491 pmid:8770536
37 Holm P J, Bhakat P, Jegersch?ld C, Gyobu N, Mitsuoka K, Fujiyoshi Y, Morgenstern R, Hebert H (2006). Structural basis for detoxification and oxidative stress protection in membranes. J Mol Biol , 360(5): 934–945
doi: 10.1016/j.jmb.2006.05.056 pmid:16806268
38 Hosono N, Kishi S, Iho S, Urasaki Y, Yoshida A, Kurooka H, Yokota Y, Ueda T (2010). Glutathione S-transferase M1 inhibits dexamethasone-induced apoptosis in association with the suppression of Bim through dual mechanisms in a lymphoblastic leukemia cell line. Cancer Sci , 101(3): 767–773
doi: 10.1111/j.1349-7006.2009.01432.x pmid:20067466
39 Hsu C H, Chen C L, Hong R L, Chen K L, Lin J F, Cheng A L (2002). Prognostic value of multidrug resistance 1, glutathione-S-transferase-pi and p53 in advanced nasopharyngeal carcinoma treated with systemic chemotherapy. Oncology , 62(4): 305–312
doi: 10.1159/000065061 pmid:12138237
40 Hunter T, Cooper J A (1985). Protein-tyrosine kinases. Annu Rev Biochem , 54: 897–930
pmid:2992362
41 Huveneers S, Danen E H (2009). Adhesion signaling- crosstalk between integrins, Src and Rho. J Cell Sci , 122(Pt 8): 1059–1069
doi: 10.1242/jcs.039446 pmid:19339545
42 Igarashi T, Tomihari N, Ohmori S, Ueno K, Kitagawa H, Satoh T (1986). Comparison of glutathione S-transferases in mouse, guinea pig, rabbit and hamster liver cytosol to those in rat liver. Biochem Int , 13(4): 641–648
pmid:3801038
43 Ingley E (2008). Src family kinases: regulation of their activities, levels and identification of new pathways. Biochim Biophys Acta , 1784(1): 56–65
pmid:17905674
44 Isgor B S, Coruh N, Iscan M (2010a). Soluble glutathione s-transferases in bovine liver: existence of GST T2. J Biol Sci , 10: 667–675
45 Isgor B S, Isgor Y G, Kurt-K?l?c Z, Olgen S (2010b). The Effect of Novel pp60c-src Inhibitors on Mammalian Glutathione S-Transferase Activity. 240th ACS National Meeting & Exposition on “Chemistry of Preventing and Combatting Disease”, Boston, Massachusetts, USA
46 Jope R S, Zhang L, Song L (2000). Peroxynitrite modulates the activation of p38 and extracellular regulated kinases in PC12 cells. Arch Biochem Biophys , 376(2): 365–370
doi: 10.1006/abbi.2000.1728 pmid:10775424
47 Kemble D J, Sun G (2009). Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation. Proc Natl Acad Sci USA , 106(13): 5070–5075
doi: 10.1073/pnas.0806117106 pmid:19273857
48 Khadaroo R G, He R, Parodo J, Powers K A, Marshall J C, Kapus A, Rotstein O D (2004). The role of the Src family of tyrosine kinases after oxidant-induced lung injury in vivo. Surgery , 136(2): 483–488
doi: 10.1016/j.surg.2004.05.029 pmid:15300219
49 Kilic Z, Sener F, Isgor Y G, Coban T, Olgen S (2009). Investigating Antioxidant and Src Kinase Inhibitory Effects of Aminomethylindole Derivatives. 1st Turkish-Russian Joint Meeting on Organic and Medicinal Chemistry. Antalya, Turkey : 51
50 Kilic-Kurt Z, Isgor Y G, Isgor B S, Olgen S (2010). The Effect Of Novel Indole Derivatives As Inhibitors Of Src Kinase and Mammalian Glutathione S-Transferase. Joint Meeting of 4th International Meeting on Medicinal and Pharmaceutical Chemistry (IMMPC-4) and 6th International Symposium on Pharmaceutical Chemistry (ISPC-6). Ankara, Turkey
51 Kim S G, Lee S J (2007). PI3K, RSK, and mTOR signal networks for the GST gene regulation. Toxicol Sci , 96(2): 206–213
doi: 10.1093/toxsci/kfl175 pmid:17122411
52 Kim S K, Abdelmegeed M A, Novak R F (2006). Identification of the insulin signaling cascade in the regulation of alpha-class glutathione S-transferase expression in primary cultured rat hepatocytes. J Pharmacol Exp Ther , 316(3): 1255–1261
doi: 10.1124/jpet.105.096065 pmid:16293713
53 Kim S K, Novak R F (2007). The role of intracellular signaling in insulin-mediated regulation of drug metabolizing enzyme gene and protein expression. Pharmacol Ther , 113(1): 88–120
doi: 10.1016/j.pharmthera.2006.07.004 pmid:17097148
54 Kim S K, Woodcroft K J, Novak R F (2003). Insulin and glucagon regulation of glutathione S-transferase expression in primary cultured rat hepatocytes. J Pharmacol Exp Ther , 305(1): 353–361
doi: 10.1124/jpet.102.045153 pmid:12649389
55 Kostyuk V A, Potapovich A I (2009). Mechanisms of the suppression of free radical overproduction by antioxidants. Front Biosci (Elite Ed) , 1: 179–188 (Elite Ed)
pmid:19482635
56 Kostyuk V A, Potapovich A I, Cesareo E, Brescia S, Guerra L, Valacchi G, Pecorelli A, Deeva I B, Raskovic D, De Luca C, Pastore S, Korkina L G (2010). Dysfunction of glutathione S-transferase leads to excess 4-hydroxy-2-nonenal and H2O2 and impaired cytokine pattern in cultured keratinocytes and blood of vitiligo patients. Antioxid Redox Signal , 13(5): 607–620
doi: 10.1089/ars.2009.2976 pmid:20070240
57 LaPensee E W, Schwemberger S J, LaPensee C R, Bahassi M, Afton S E, Ben-Jonathan N (2009). Prolactin confers resistance against cisplatin in breast cancer cells by activating glutathione-S-transferase. Carcinogenesis , 30(8): 1298–1304
doi: 10.1093/carcin/bgp120 pmid:19443905
58 Li J, Xia Z, Ding J (2005). Thioredoxin-like domain of human kappa class glutathione transferase reveals sequence homology and structure similarity to the theta class enzyme. Protein Sci , 14(9): 2361–2369
doi: 10.1110/ps.051463905 pmid:16081649
59 Lindberg R A, Quinn A M, Hunter T (1992). Dual-specificity protein kinases: will any hydroxyl do? Trends Biochem Sci , 17(3): 114–119
doi: 10.1016/0968-0004(92)90248-8 pmid:1412695
60 Lo H W, Antoun G R, Ali-Osman F (2004). The human glutathione S-transferase P1 protein is phosphorylated and its metabolic function enhanced by the Ser/Thr protein kinases, cAMP-dependent protein kinase and protein kinase C, in glioblastoma cells. Cancer Res , 64(24): 9131–9138
doi: 10.1158/0008-5472.CAN-04-0283 pmid:15604283
61 Lu Y, Yu Q, Liu J H, Zhang J, Wang H, Koul D, McMurray J S, Fang X, Yung W K, Siminovitch K A, Mills G B (2003). Src family protein-tyrosine kinases alter the function of PTEN to regulate phosphatidylinositol 3-kinase/AKT cascades. J Biol Chem , 278(41): 40057–40066
doi: 10.1074/jbc.M303621200 pmid:12869565
62 Manal M E T, Hanachi P, Patimah I, Siddig I A, Fauziah O (2007). The effect of neem (Azadirachta indica) leaves extract on alpha-fetoprotein serum concentration, glutathione s-transferase and glutathione peroxidase activity in hepatocarcinogenesis induced rats. Int J Cancer Res , 3: 111–118
doi: 10.3923/ijcr.2007.111.118
63 Manning G, Whyte D B, Martinez R, Hunter T, Sudarsanam S (2002). The protein kinase complement of the human genome. Science , 298(5600): 1912–1934
doi: 10.1126/science.1075762 pmid:12471243
64 Martin G S (2004). The road to Src. Oncogene , 23(48): 7910–7917
doi: 10.1038/sj.onc.1208077 pmid:15489909
65 McIlwain C C, Townsend D M, Tew K D (2006). Glutathione S-transferase polymorphisms: cancer incidence and therapy. Oncogene , 25(11): 1639–1648
doi: 10.1038/sj.onc.1209373 pmid:16550164
66 McLachlan R W, Kraemer A, Helwani F M, Kovacs E M, Yap A S (2007). E-cadherin adhesion activates c-Src signaling at cell-cell contacts. Mol Biol Cell , 18(8): 3214–3223
doi: 10.1091/mbc.E06-12-1154 pmid:17553930
67 McLean G W, Carragher N O, Avizienyte E, Evans J, Brunton V G, Frame M C (2005). The role of focal-adhesion kinase in cancer- a new therapeutic opportunity. Nat Rev Cancer , 5(7): 505–515
68 Nordberg J, Arnér E S (2001). Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med , 31(11): 1287–1312
doi: 10.1016/S0891-5849(01)00724-9 pmid:11728801
69 Nyga R, Pecquet C, Harir N, Gu H, Dhennin-Duthille I, Régnier A, Gouilleux-Gruart V, Lassoued K, Gouilleux F (2005). Activated STAT5 proteins induce activation of the PI 3-kinase/Akt and Ras/MAPK pathways via the Gab2 scaffolding adapter. Biochem J , 390(Pt 1): 359–366
doi: 10.1042/BJ20041523 pmid:15833084
70 Oakley A J, Lo Bello M, Mazzetti A P, Federici G, Parker M W (1997). The glutathione conjugate of ethacrynic acid can bind to human pi class glutathione transferase P1-1 in two different modes. FEBS Lett , 419(1): 32–36
doi: 10.1016/S0014-5793(97)01424-5 pmid:9426214
71 Okamura T, Singh S, Buolamwini J, Haystead T, Friedman H, Bigner D, Ali-Osman F (2009a). Tyrosine phosphorylation of the human glutathione S-transferase P1 by epidermal growth factor receptor. J Biol Chem , 284(25): 16979–16989
doi: 10.1074/jbc.M808153200 pmid:19254954
72 Okamura T, Singh S, Buolamwini J K, Friedman H S, Bigner D D, Ali-Osman F (2009b). EGF receptor tyrosine kinase mediates a novel pathway of drug resistance in malignant gliomas via tyrosine phosphorylation and functional activation of GST P1. Neuro-oncol , 11(2): 218–218
73 Okutani Y, Kitanaka A, Tanaka T, Kamano H, Ohnishi H, Kubota Y, Ishida T, Takahara J (2001). Src directly tyrosine-phosphorylates STAT5 on its activation site and is involved in erythropoietin-induced signaling pathway. Oncogene , 20(45): 6643–6650
doi: 10.1038/sj.onc.1204807 pmid:11641791
74 Pani G, Giannoni E, Galeotti T, Chiarugi P (2009). Redox-based escape mechanism from death: the cancer lesson. Antioxid Redox Signal , 11(11): 2791–2806
doi: 10.1089/ars.2009.2739 pmid:19686053
75 Patskovsky Y V, Patskovska L N, Listowsky I, Almo S C(2009, Last Update on 24 February, 2009). Human Glutathione S-Transferase M1A–1A Catalyzes Formation of GSH-Metal Complexes. Retrieved 20 June, 2010 , from http://www.pdb.org.
76 Planchon S M, Waite K A, Eng C (2008). The nuclear affairs of PTEN. J Cell Sci , 121(Pt 3): 249–253
doi: 10.1242/jcs.022459 pmid:18216329
77 Playford M P, Schaller M D (2004). The interplay between Src and integrins in normal and tumor biology. Oncogene , 23(48): 7928–7946
doi: 10.1038/sj.onc.1208080 pmid:15489911
78 Polekhina G, Board P G, Blackburn A C, Parker M W (2001). Crystal structure of maleylacetoacetate isomerase/glutathione transferase zeta reveals the molecular basis for its remarkable catalytic promiscuity. Biochemistry , 40(6): 1567–1576
doi: 10.1021/bi002249z pmid:11327815
79 Ricono J M, Huang M, Barnes L A, Lau S K, Weis S M, Schlaepfer D D, Hanks S K, Cheresh D A (2009). Specific cross-talk between epidermal growth factor receptor and integrin alphavbeta5 promotes carcinoma cell invasion and metastasis. Cancer Res , 69(4): 1383–1391
doi: 10.1158/0008-5472.CAN-08-3612 pmid:19208836
80 Rodriguez P, Mitton B, Kranias E G (2005). Phosphorylation of glutathione-S-transferase by protein kinase C-alpha implications for affinity-tag purification. Biotechnol Lett , 27(23-24): 1869–1873
doi: 10.1007/s10529-005-3895-y pmid:16328982
81 Rucci N, Susa M, Teti A (2008). Inhibition of protein kinase c-Src as a therapeutic approach for cancer and bone metastases. Anticancer Agents Med Chem , 8(3): 342–349
doi: 10.2174/187152008783961905 pmid:18393792
82 Schlaepfer D D, Hanks S K, Hunter T, van der Geer P (1994). Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature , 372(6508): 786–791
pmid:7997267
83 Scodelaro Bilbao P, Boland R, Santillán G (2010). ATP modulates transcription factors through P2Y2 and P2Y4 receptors via PKC/MAPKs and PKC/Src pathways in MCF-7 cells. Arch Biochem Biophys , 494(1): 7–14
doi: 10.1016/j.abb.2009.11.002 pmid:19900397
84 Shah O J, Kimball S R, Jefferson L S (2002). The Src-family tyrosine kinase inhibitor PP1 interferes with the activation of ribosomal protein S6 kinases. Biochem J , 366(Pt 1): 57–62
pmid:12014987
85 Singh S, Okamura T, Ali-Osman F (2010). Serine phosphorylation of glutathione S-transferase P1 (GSTP1) by PKCα enhances GSTP1-dependent cisplatin metabolism and resistance in human glioma cells. Biochem Pharmacol , 80(9): 1343–1355
doi: 10.1016/j.bcp.2010.07.019 pmid:20654585
86 Smeyne M, Boyd J, Raviie Shepherd K, Jiao Y, Pond B B, Hatler M, Wolf R, Henderson C, Smeyne R J (2007). GSTpi expression mediates dopaminergic neuron sensitivity in experimental parkinsonism. Proc Natl Acad Sci U S A , 104(6): 1977–1982
doi: 10.1073/pnas.0610978104 pmid:17267597
87 Sun G, Kemble D J (2009). To C or not to C: direct and indirect redox regulation of Src protein tyrosine kinase. Cell Cycle , 8(15): 2353–2355
pmid:19571676
88 Tars K, Larsson A K, Shokeer A, Olin B, Mannervik B, Kleywegt G J (2006). Structural basis of the suppressed catalytic activity of wild-type human glutathione transferase T1-1 compared to its W234R mutant. J Mol Biol , 355(1): 96–105
doi: 10.1016/j.jmb.2005.10.049 pmid:16298388
89 Thomas S M, Brugge J S (1997). Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol , 13(1): 513–609
doi: 10.1146/annurev.cellbio.13.1.513 pmid:9442882
90 Tice D A, Biscardi J S, Nickles A L, Parsons S J (1999). Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci U S A , 96(4): 1415–1420
doi: 10.1073/pnas.96.4.1415 pmid:9990038
91 Townsend D M, Findlay V J, Fazilev F, Ogle M, Fraser J, Saavedra J E, Ji X, Keefer L K, Tew K D (2006). A glutathione S-transferase pi-activated prodrug causes kinase activation concurrent with S-glutathionylation of proteins. Mol Pharmacol , 69(2): 501–508
doi: 10.1124/mol.105.018523 pmid:16288082
92 Townsend D M, He L, Hutchens S, Garrett T E, Pazoles C J, Tew K D (2008). NOV-002, a glutathione disulfide mimetic, as a modulator of cellular redox balance. Cancer Res , 68(8): 2870–2877
doi: 10.1158/0008-5472.CAN-07-5957 pmid:18413755
93 Townsend D M, Shen H, Staros A L, Gaté L, Tew K D (2002). Efficacy of a glutathione S-transferase pi-activated prodrug in platinum-resistant ovarian cancer cells. Mol Cancer Ther , 1(12): 1089–1095
pmid:12481432
94 Uys J D, Manevich Y, Devane L C, He L, Garret T E, Pazoles C J, Tew K D, Townsend D M (2010). Preclinical pharmacokinetic analysis of NOV-002, a glutathione disulfide mimetic. Biomed Pharmacother , 64(7): 493–498
doi: 10.1016/j.biopha.2010.01.003 pmid:20359856
95 Villafania A, Anwar K, Amar S, Chie L, Way D, Chung D L, Adler V, Ronai Z, Brandt-Rauf P W, Yamaizumii Z, Kung H F, Pincus M R (2000). Glutathione-S-Transferase as a selective inhibitor of oncogenic ras-p21-induced mitogenic signaling through blockade of activation of jun by jun-N-terminal kinase. Ann Clin Lab Sci , 30(1): 57–64
pmid:10678584
96 Vosler P S, Chen J (2009). Potential molecular targets for translational stroke research. Stroke , 40(3 Suppl): S119–S120
doi: 10.1161/STROKEAHA.108.533109 pmid:19064800
97 Waldmann H, Levitzki A (2001). Protein tyrosine kinase inhibitors as therapeutic agents. Bioorganic Chemistry of Biological Signal Transduction , 211: 1–15
98 Waldron R T, Rey O, Zhukova E, Rozengurt E (2004). Oxidative stress induces protein kinase C-mediated activation loop phosphorylation and nuclear redistribution of protein kinase D. J Biol Chem , 279(26): 27482–27493
doi: 10.1074/jbc.M402875200 pmid:15084589
99 Wallez Y, Cand F, Cruzalegui F, Wernstedt C, Souchelnytskyi S, Vilgrain I, Huber P (2007). Src kinase phosphorylates vascular endothelial-cadherin in response to vascular endothelial growth factor: identification of tyrosine 685 as the unique target site. Oncogene , 26(7): 1067–1077
doi: 10.1038/sj.onc.1209855 pmid:16909109
100 Wallez Y, Vilgrain I, Huber P (2006). Angiogenesis: the VE-cadherin switch. Trends Cardiovasc Med , 16(2): 55–59
doi: 10.1016/j.tcm.2005.11.008 pmid:16473763
[1] Kai Jiang,Jianhang Jia. Smoothened regulation in response to Hedgehog stimulation[J]. Front. Biol., 2015, 10(6): 475-486.
[2] Gahana Advani,Anderly C. Chueh,Ya Chee Lim,Amardeep Dhillon,Heung-Chin Cheng. Csk-homologous kinase (Chk/Matk): a molecular policeman suppressing cancer formation and progression[J]. Front. Biol., 2015, 10(3): 195-202.
[3] Chaohong LIU, Margaret K. FALLEN, Heather MILLER, Arpita UPADHYAYA, Wenxia SONG. The actin cytoskeleton coordinates the signal transduction and antigen processing functions of the B cell antigen receptor[J]. Front Biol, 2013, 8(5): 475-485.
[4] Yonggang ZHANG, Wenhui HU. NFκB signaling regulates embryonic and adult neurogenesis[J]. Front Biol, 2012, 7(4): 277-291.
[5] Saijun MO, Shengli YANG, Zongbin CUI. New glimpses of caveolin-1 functions in embryonic development and human diseases[J]. Front Biol, 2011, 6(5): 367-376.
[6] Wenjing ZHANG, Qilai HUANG, Zi-Chun HUA. Oridonin: A promising anticancer drug from China[J]. Front Biol, 2010, 5(6): 540-545.
[7] Fang-Fang WANG, Li WANG, Wei QIAN. Two-component signal transduction systems and regulation of virulence factors in Xanthomonas: a perspective[J]. Front Biol, 2010, 5(6): 495-506.
[8] Yinghui HUANG, Xiaoxue QIU, Ji-Long CHEN. Identification of cancer stem cells: from leukemia to solid cancers[J]. Front Biol, 2010, 5(5): 407-416.
[9] Jinbiao MA, Ying HUANG, . Post-transcriptional regulation of miRNA biogenesis and functions[J]. Front. Biol., 2010, 5(1): 32-40.
[10] YU Guanghui, CHEN Yan. The language of GABA in pollen tube growth and guidance[J]. Front. Biol., 2008, 3(4): 439-442.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed