Tyrosine phosphorylation of HSC70 and its interaction with RFC mediates methotrexate resistance in murine L1210 leukemia cells

Cancer Letters

Volumn 357, Issue 1, 2015, Pages 231-241

  Liu, Tuoen ^a   Singh, Ratan ^b   Rios, Zechary ^b   Bhushan, Alok ^c   Li, Mengxiong ^d   Sheridan, Peter P ^b,e   Bearden, Shawn E ^b,e   Lai, James C K ^b   Agbenowu, Senyo ^b   Cao, Shousong ^f   Daniels, Christopher K ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b IDAHO STATE UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d THE THIRD AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^e Nucl Eng Idaho State University   (United States)

^f Chifeng Saliont Pharmaceutical Co Ltd   (China)

Author keywords

Cross resistance; Heat shock cognate protein 70; Methotrexate binding protein; Methotrexate transportation; Reduced folate carrier; Tyrosine phosphorylation

Indexed keywords

CISPLATIN; GENISTEIN; HEAT SHOCK COGNATE PROTEIN 70; METHOTREXATE; REDUCED FOLATE CARRIER; TYROSINE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CROSS RESISTANCE; DRUG PROTEIN BINDING; LEUKEMIA; LEUKEMIA CELL; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; ANIMAL; CONFOCAL MICROSCOPY; DRUG RESISTANCE; LEUKEMIA L1210; METABOLISM; MOUSE; PHOSPHORYLATION;

MURINAE;

ANIMALS; DRUG RESISTANCE, NEOPLASM; HSC70 HEAT-SHOCK PROTEINS; LEUKEMIA L1210; METHOTREXATE; MICE; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; REDUCED FOLATE CARRIER PROTEIN; TYROSINE;

EID: 84920456570     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.11.036     Document Type: Article

References (42)

1. Vickers P.J., Dickson R.B., Shoemaker R., Cowan K.H. A multidrug-resistant MCF-7 human breast cancer cell line which exhibits cross-resistance to antiestrogens and hormone-independent tumor growth in vivo. Mol. Endocrinol 1988, 2:886-892.
2. Volk E.L., Rohde K., Rhee M., McGuire J.J., Doyle L.A., Ross D.D., et al. Methotrexate cross-resistance in a mitoxantrone-selected multidrug-resistant MCF7 breast cancer cell line is attributable to enhanced energy-dependent drug efflux. Cancer Res 2000, 160:3514-3521.
3. Gore M.E., Fryatt I., Wiltshaw E., Dawson T., Robinson B.A., Calvert A.H. Cisplatin/carboplatin cross-resistance in ovarian cancer. Br. J. Cancer 1989, 60:767-769.
4. Hamaguchi K., Godwin A.K., Yakushiji M., O'Dwyer P.J., Ozols R.F., Hamilton T.C. Cross-resistance to diverse drugs is associated with primary cisplatin resistance in ovarian cancer cell lines. Cancer Res 1993, 53:5225-5232.
5. Wroblewski H.D., Bhushan A., Xuan Y., Brinton B.T., Tritton T.R., Hacker M.P. Investigations on the mechanisms of methotrexate resistance in a cisplatin-resistant L1210 murine leukemia cell subline. Cancer Chemother. Pharmacol 1996, 37:337-342.
6. Price E.M., Freisheim J.H. Photoaffinity analogues of methotrexate as folate antagonist binding probes. 2. Transport studies, photoaffinity labeling, and identification of the membrane carrier protein for methotrexate from murine L1210 cells. Biochemistry 1987, 26:4757-4763.
7. Price E.M., Ratnam M., Rodeman K.M., Freisheim J.H. Characterization of the methotrexate transport pathway in murine L1210 leukemia cells: involvement of a membrane receptor and a cytosolic protein. Biochemistry 1988, 27:7853-7858.
8. Bhushan A., Wroblewski D., Xuan Y., Tritton T.R., Hacker M.P. Correlation of altered tyrosine phosphorylation with methotrexate resistance in a cisplatin-resistant subline of L1210 cells. Biochem. Pharmacol 1996, 51:477-482.
9. Bhushan A., Hacker M.P., Tritton T.R. Collateral methotrexate resistance in cisplatin-selected murine leukemia cells. Braz. J. Med. Biol. Res 1999, 32:827-833.
10. Liu T., Dean A., Ashwini S., Sheridan P.P., Bhushan A., Lai J.C.K., et al. Identification and characterization of a 66-68-kDa protein as a methotrexate-binding protein in murine leukemia L1210 cells. Cell Stress Chaperones 2013, 18:223-234.
11. Place S.P., Hofmann G.E. Comparison of Hsc70 orthologs from polar and temperate notothenioid fishes: differences in prevention of aggregation and refolding of denatured proteins. Am. J. Physiol. Regul. Integr. Comp. Physiol 2005, 288:R1195-R1202.
12. Arispe N., De Maio A. ATP and ADP modulate a cation channel formed by Hsc70 in acidic phospholipid membranes. J. Biol. Chem 2000, 275:30839-30843.
13. Kose S., Furuta M., Koike M., Yoneda Y., Imamoto N. The 70-kD heat shock cognate protein (hsc70) facilitates the nuclear export of the import receptors. J. Cell Biol 2005, 171:19-25.
14. Kodiha M., Chu A., Lazrak O., Stochaj U. Stress inhibits nucleocytoplasmic shuttling of heat shock protein hsc70. Am. J. Physiol. Cell Physiol 2005, 289:C1034-C1041.
15. Gebauer M., Melki R., Gehring U. The chaperone cofactor Hop/p60 interacts with the cytosolic chaperonin-containing TCP-1 and affects its nucleotide exchange and protein folding activities. J. Biol. Chem 1998, 273:29475-29480.
16. Höfeld J., Minami Y., Hartl F.U. Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell 1995, 83:589-598.
17. Minam Y., Höhfeld J., Ohtsuka K., Hart F.U. Regulation of the heat-shock protein 70 reaction cycle by the mammalian DnaJ homolog, Hsp40. J. Biol. Chem 1996, 927:19617-19624.
18. Liu T., Daniels C.K., Cao S. Comprehensive review on the HSC70 functions, interactions with related molecules and involvement in clinical diseases and therapeutic potential. Pharmacol. Ther 2012, 136:354-374.
19. Liu M., Ge Y., Cabelof D.C., Aboukamee A., Heydari A.R., Mohammad R., et al. Structure and regulation of the murine reduced folate carrier gene: identification of four noncoding exons and promoters and regulation by dietary folates. J. Biol. Chem 2005, 280:5588-5597.
20. Matherly L.H., Hou Z., Deng Y. Human reduced folate carrier: translation of basic biology to cancer etiology and therapy. Cancer Metastasis Rev 2007, 26:111-128.
21. Kaufman Y., Drori S., Cole P.D., Kamen B.A., Sirota J., Ifergan I., et al. Reduced folate carrier mutations are not the mechanism underlying methotrexate resistance in childhood acute lymphoblastic leukemia. Cancer 2004, 100:773-782.
22. Trippett T.M., Garcia S., Manova K., Mody R., Cohen-Gould L., Flintoff W., et al. Localization of a human reduced folate carrier protein in the mitochondrial as well as the cell membrane of leukemia cells. Cancer Res 2001, 61:1941-1947.
23. Zhao R., Gao F., Liu L., Goldman I.D. The reduced folate carrier in L1210 murine leukemia cells is a 58-kDa protein. Biochim. Biophys. Acta 2000, 1466:7-10.
24. Leung S.M., Hightower L.E. A 16-kDa protein functions as a new regulatory protein for Hsc70 molecular chaperone and is identified as a member of the Nm23/nucleoside diphosphate kinase family. J. Biol. Chem 1997, 272:2607-2614.
25. Otto H., Dreger M., Bengtsson L., Hucho F. Identification of tyrosine-phosphorylated proteins with the nuclear envelope. Eur. J. Biochem 2001, 268:420-428.
26. Egerton M., Moritz R.L., Druker B., Kelso A., Simpson R.J. Identification of the 70kD heat shock cognate protein (Hsc70) and alpha-actinin-1 as novel phosphotyrosine-containing proteins in T lymphocytes. Biochem. Biophys. Res. Commun 1996, 224:666-674.
27. Obenauer J.C., Cantley L.C., Yaffe M.B. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 2003, 31:3635-3641.
28. Yaffe M.B., Leparc G.G., Lai J., Obata T., Volinia S., Cantley L.C. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol 2001, 19:348-353.
29. Huang H.D., Lee T.Y., Tzeng S.W., Horng J.T. KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites. Nucleic Acids Res 2005, 33:W226-W229.
30. Blom N., Gammeltoft S., Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol 1999, 294:1351-1362.
31. Oheim M., Li D. Imaging cellular and molecular biological functions: principles and practice. Quantitative Colocalisation Imaging: Concepts, Measurements, and Pitfalls 2007, 117-155. Springer, Berlin, Heidelberg. S.L. Shorte, F. Frischknecht (Eds.).
32. Söderberg O., Gullberg M., Jarvius M., Ridderstråle K., Leuchowius K.J., Jarvius J., et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 2006, 3:995-1000.
33. Zinchuk V., Grossenbacher-Zinchuk O. Quantitative colocalization analysis of confocal fluorescence microscopy images. Curr. Protoc. Cell Biol 2011, Chapter 4.
34. Sadlish H., Williams F.M.R., Flintoff W.F. Cytoplasmic domains of the reduced folate carrier are essential for trafficking, but not function. Biochem. J. 2002, 364:777-786.
35. Gorlick R., Goker E., Trippett T., Steinherz P., Elisseyeff Y., Mazumdar M., et al. Defective transport is a common mechanism of acquired methotrexate resistance in acute lymphocytic leukemia and is associated with decreased reduced folate carrier expression. Blood 1997, 89:1013-1018.
36. Chen H.S., Jia J., Su H.F., Lin H.D., Chen J.W., Lin S.J., et al. Downregulation of the constitutively expressed Hsc70 in diabetic myocardium is mediated by insulin deficiency. J. Endocrinol 2006, 190:433-440.
37. Hou Z., Stapels S.E., Haska C.L., Matherly L.H. Localization of a substrate binding domain of the human reduced folate carrier to transmembrane domain 11 by radioaffinity labeling and cysteine-substituted accessibility methods. J. Biol. Chem 2005, 280:36206-36213.
38. Nabokina S.M., Ma T.Y., Said H.M. Mechanism and regulation of folate uptake by human pancreatic epithelial MIA PaCa-2 cells. Am. J. Physiol. Cell Physiol 1999, 287:C142-C148.
39. Frank N.Y., Pendse S.S., Lapchak P.H., Margaryan A., Shlain D., Doeing C., et al. Regulation of progenitor cell fusion by ABCB5 P-glycoprotein, a novel human ATP-binding cassette transporter. J. Biol. Chem 2003, 278:47156-47165.
40. Choi C.H. ABC transporters as multidrug resistance mechanisms and the development of chemosensitizers for their reversal. Cancer Cell Int 2005, 5:30.
41. Lehne G. P-glycoprotein as a drug target in the treatment of multidrug resistant cancer. Curr. Drug Targets 2000, 1:85-99.
42. Loo T.W., Clarke D.M. P-glycoprotein. Associations between domains and between domains and molecular chaperones. J. Biol. Chem 1995, 270:21839-21844.