The Combination of the CIGB-300 Anticancer Peptide and Cisplatin Modulates Proteins Related to Cell Survival, DNA Repair and Metastasis in a Lung Cancer Cell Line Model

Author(s): Arielis Rodríguez-Ulloa*, Yassel Ramos*, Aniel Sánchez-Puente, Yasser Perera, Alexis Musacchio-Lasa , Jorge Fernández-de-Cossio, Gabriel Padrón, Luis J.G. López, Vladimir Besada, Silvio E. Perea.

Journal Name: Current Proteomics

Volume 16 , Issue 4 , 2019

Submit Manuscript
Submit Proposal

Graphical Abstract:


Background: CIGB-300 is a pro-apoptotic peptide that abrogates CK2-mediated phosphorylation, and can elicit synergistic interaction in vitro and in vivo when combined with certain anticancer drugs.

Objective: The combination of CIGB-300 with cisplatin is studied through data mining and expressionbased proteomics to reveal the molecular basis of this interaction. Cisplatin resistance-associated proteins, which have also been reported as CK2 substrates, were first identified by bioinformatic analyses.

Methods: Data from these analyses suggested that the cisplatin resistance phenotype could be directly improved by inhibiting CK2 phosphorylation on specific substrates. Furthermore, 157 proteins were differentially modulated on the NCI-H125 lung cancer cell line in response to CIGB-300, cisplatin or both drugs as determined by LC-MS/MS.

Results: The expression of 28 cisplatin resistance-associated proteins was changed when cisplatin was combined with CIGB-300. Overall, the proteins identified are also related to cell survival, cell proliferation and metastasis. Furthermore, the CIGB-300 regulated proteome revealed proteins that were initially involved in the mechanism of action of CIGB-300 and cisplatin as single agents.

Conclusion: This is the first report describing the protein array modulated by combining CIGB-300 and cisplatin that will support the rationale for future clinical settings based on a multi-target cancer therapy.

Keywords: Comparative proteomic analysis, CIGB-300, cisplatin, apoptosis, casein kinase 2, lung cancer.

Trembley, J.H.; Wang, G.; Unger, G.; Slaton, J.; Ahmed, K. Protein kinase CK2 in health and disease: CK2: A key player in cancer biology. Cell. Mol. Life Sci., 2009, 66(11-12), 1858-1867.
Chon, H.J.; Bae, K.J.; Lee, Y.; Kim, J. The casein kinase 2 inhibitor, CX-4945, as an anti-cancer drug in treatment of human hematological malignancies. Front. Pharmacol., 2015, 31(6), 70.
Solares, A.M.; Santana, A.; Baladrón, I.; Valenzuela, C.; González, C.A.; Díaz, A.; Castillo, D.; Ramos, T.; Gómez, R.; Alonso, D.F.; Herrera, L.; Sigman, H.; Perea, S.E.; Acevedo, B.E.; López-Saura, P. Safety and preliminary efficacy data of a novel casein kinase 2 (CK2) peptide inhibitor administered intralesionally at four dose levels in patients with cervical malignancies. BMC Cancer, 2009, 9, 146.
Pierre, F.; Chua, P.C.; O’Brien, S.E.; Siddiqui-Jain, A.; Bourbon, P.; Haddach, M.; Michaux, J.; Nagasawa, J.; Schwaebe, M.K.; Stefan, E.; Vialettes, A.; Whitten, J.P.; Chen, T.K.; Darjania, L.; Stansfield, R.; Anderes, K.; Bliesath, J.; Drygin, D.; Ho, C.; Omori, M.; Proffitt, C.; Streiner, N.; Trent, K.; Rice, W.G.; Ryckman, D.M. Discovery and SAR of 5-(3-chlorophenylamino)benzo[c][2,6]naphthyridine-8-carboxylic acid (CX-4945), the first clinical stage inhibitor of protein kinase CK2 for the treatment of cancer. J. Med. Chem., 2011, 54(2), 635-654.
Perea, S.E.; Reyes, O.; Puchades, Y.; Mendoza, O.; Vispo, N.S.; Torrens, I.; Santos, A.; Silva, R.; Acevedo, B.; López, E.; Falcón, V.; Alonso, D.F. Antitumor effect of a novel proapoptotic peptide that impairs the phosphorylation by the protein kinase 2 (casein kinase 2). Cancer Res., 2004, 64(19), 7127-7129.
Martins, L.R.; Perera, Y.; Lúcio, P.; Silva, M.G.; Perea, S.E.; Barata, J.T. Targeting chronic lymphocytic leukemia using CIGB-300, a clinical-stage CK2-specific cell-permeable peptide inhibitor. Oncotarget, 2014, 5(1), 258-263.
Perera, Y.; Farina, H.G.; Hernández, I.; Mendoza, O.; Serrano, J.M.; Reyes, O.; Gómez, D.E.; Gómez, R.E.; Acevedo, B.E.; Alonso, D.F.; Perea, S.E. Systemic administration of a peptide that impairs the protein kinase (CK2) phosphorylation reduces solid tumor growth in mice. Int. J. Cancer, 2008, 122(1), 57-62.
Soriano-García, J.L.; López-Díaz, A.; Solares-Asteasuainzarra, M.; Baladrón-Castrillo, I.; Batista-Albuerne, N.; García-García, I.; González-Méndez, L.; Perera-Negrín, Y.; Valenzuela-Silva, C.M.; Pedro, A.P.; Quevedo-Sotolongo, L.S.; Hernández-González, I.; Silveira-Pablos, J.M.; Chong-López, A.; Alonso, D.F.; Gómez, R.E.; Renault, J.Y.; Perrin, P.; Sigman, H.; Gold, S.; Perea-Rodríguez, S.E.; Acevedo-Castro, B.E.; Herrera-Martínez, L.; López-Saura, P.A. Pharmacological and safety evaluation of CIGB-300, a casein kinase 2 inhibitor peptide, administered intralesionally to patients with cervical cancer stage IB2/II. J. Cancer Res. Ther., 2013, 1(6), 163-173.
Pommier, Y.; Sordet, O.; Antony, S.; Hayward, R.L.; Kohn, K.W. Apoptosis defects and chemotherapy resistance: Molecular interaction maps and networks. Oncogene, 2004, 23(16), 2934-2949.
Lehár, J.; Krueger, A.S.; Avery, W.; Heilbut, A.M.; Johansen, L.M.; Price, E.R.; Rickles, R.J.; Short, G.F., III; Staunton, J.E.; Jin, X.; Lee, M.S.; Zimmermann, G.R.; Borisy, A.A. Synergistic drug combinations tend to improve therapeutically relevant selectivity. Nat. Biotechnol., 2009, 27(7), 659-666.
Winter, G.E.; Rix, U.; Carlson, S.M.; Gleixner, K.V.; Grebien, F.; Gridling, M.; Müller, A.C.; Breitwieser, F.P.; Bilban, M.; Colinge, J.; Valent, P.; Bennett, K.L.; White, F.M.; Superti-Furga, G. Systems-pharmacology dissection of a drug synergy in imatinib-resistant CML. Nat. Chem. Biol., 2012, 8(11), 905-912.
Perera, Y.; Toro, N.D.; Gorovaya, L.; Fernandez-de-Cossio, J.; Farina, H.G.; Perea, S.E. Synergistic interactions of the anti-casein kinase 2 CIGB-300 peptide and chemotherapeutic agents in lung and cervical preclinical cancer models. Mol. Clin. Oncol., 2014, 2(6), 935-944.
Rodríguez-Ulloa, A.; Ramos, Y.; Gil, J.; Perera, Y.; Castellanos-Serra, L.; García, Y.; Betancourt, L.; Besada, V.; González, L.J.; Fernández-de-Cossio, J.; Sanchez, A.; Serrano, J.M.; Farina, H.; Alonso, D.F.; Acevedo, B.E.; Padrón, G.; Musacchio, A.; Perea, S.E. Proteomic profile regulated by the anticancer peptide CIGB-300 in Non-Small Cell Lung Cancer (NSCLC) cells. J. Proteome Res., 2010, 9(10), 5473-5483.
Cirigliano, S.M.; Díaz Bessone, M.I.; Berardi, D.E.; Flumian, C.; Bal de Kier Joffé, E.D.; Perea, S.E.; Farina, H.G.; Todaro, L.B.; Urtreger, A.J. The synthetic peptide CIGB-300 modulates CK2-dependent signaling pathways affecting the survival and chemoresistance of non-small cell lung cancer cell lines. Cancer Cell Int., 2017, 17, 42.
Fields, G.B.; Noble, R.L. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res., 1990, 35(3), 161-214.
Klose, J.; Kobalz, U. Two-dimensional electrophoresis of proteins: an updated protocol and implications for a functional analysis of the genome. Electrophoresis, 1995, 16(6), 1034-1059.
Sánchez, A.; González, L.J.; Betancourt, L.; Gil, J.; Besada, V.; Fernández-de-Cossío, J.; Rodríguez-Ulloa, A.; Marrero, K.; Alvarez, F.; Fando, R.; Padrón, G. Selective isolation of multiple positively charged peptides for 2-DE-free quantitative proteomics. Proteomics, 2006, 6(16), 4444-4455.
Fernandez-de-Cossio, J.; Gonzalez, L.J.; Satomi, Y.; Betancourt, L.; Ramos, Y.; Huerta, V.; Amaro, A.; Besada, V.; Padron, G.; Minamino, N.; Takao, T. Isotopica: A tool for the calculation and viewing of complex isotopic envelopes. Nucleic Acids Res, 2004. 32(Web Server issue), W674-W678.
Fernández-de-Cossio, J.; Gonzalez, L.J.; Satomi, Y.; Betancourt, L.; Ramos, Y.; Huerta, V.; Besada, V.; Padron, G.; Minamino, N.; Takao, T. Automated interpretation of mass spectra of complex mixtures by matching of isotope peak distributions. Rapid Commun. Mass Spectrom., 2004, 18(20), 2465-2472.
Huang da W.; Sherman, B.T.; Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 2009, 4(1), 44-57.
Yeung, K.Y.; Haynor, D.R.; Ruzzo, W.L. Validating clustering for gene expression data. Bioinformatics, 2001, 17(4), 309-318.
Pavlidis, P.; Noble, W.S. Matrix2png: A utility for visualizing matrix data. Bioinformatics, 2003, 19(2), 295-296.
Meggio, F.; Pinna, L.A. One-thousand-and-one substrates of protein kinase CK2? FASEB J., 2003, 17(3), 349-368.
Dinkel, H.; Chica, C.; Via, A.; Gould, C.M.; Jensen, L.J.; Gibson, T.J.; Diella, F. Phospho.ELM: A database of phosphorylation sites--update 2011. Nucleic Acids Res., 2011, 39, D261-D267.
Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res., 2003, 13(11), 2498-2504.
Kitano, H. Cancer as a robust system: Implications for anticancer therapy. Nat. Rev. Cancer, 2004, 4(3), 227-235.
Perea, S.E.; Reyes, O.; Baladron, I.; Perera, Y.; Farina, H.; Gil, J.; Rodriguez, A.; Bacardi, D.; Marcelo, J.L.; Cosme, K.; Cruz, M.; Valenzuela, C.; López-Saura, P.A.; Puchades, Y.; Serrano, J.M.; Mendoza, O.; Castellanos, L.; Sanchez, A.; Betancourt, L.; Besada, V.; Silva, R.; López, E.; Falcón, V.; Hernández, I.; Solares, M.; Santana, A.; Díaz, A.; Ramos, T.; López, C.; Ariosa, J.; González, L.J.; Garay, H.; Gómez, D.; Gómez, R.; Alonso, D.F.; Sigman, H.; Herrera, L.; Acevedo, B. CIGB-300, a novel proapoptotic peptide that impairs the CK2 phosphorylation and exhibits anticancer properties both in vitro and in vivo. Mol. Cell. Biochem., 2008, 316(1-2), 163-167.
Brown, M.S.; Diallo, O.T.; Hu, M.; Ehsanian, R.; Yang, X.; Arun, P.; Lu, H.; Korman, V.; Unger, G.; Ahmed, K.; Van Waes, C.; Chen, Z. CK2 modulation of NF-kappaB, TP53, and the malignant phenotype in head and neck cancer by anti-CK2 oligonucleotides in vitro or in vivo via sub-50-nm nanocapsules. Clin. Cancer Res., 2010, 16(8), 2295-2307.
Siddiqui-Jain, A.; Bliesath, J.; Macalino, D.; Omori, M.; Huser, N.; Streiner, N.; Ho, C.B.; Anderes, K.; Proffitt, C.; O’Brien, S.E.; Lim, J.K.; Von Hoff, D.D.; Ryckman, D.M.; Rice, W.G.; Drygin, D. CK2 inhibitor CX-4945 suppresses DNA repair response triggered by DNA-targeted anticancer drugs and augments efficacy: Mechanistic rationale for drug combination therapy. Mol. Cancer Ther., 2012, 11(4), 994-1005.
So, K.S.; Rho, J.K.; Choi, Y.J.; Kim, S.Y.; Choi, C.M.; Chun, Y.J.; Lee, J.C. AKT/mTOR down-regulation by CX-4945, a CK2 inhibitor, promotes apoptosis in chemo-refractory non-small cell lung cancer cells. Anticancer Res., 2015, 35(3), 1537-1542.
Galluzzi, L.; Vitale, I.; Michels, J.; Brenner, C.; Szabadkai, G.; Harel-Bellan, A.; Castedo, M.; Kroemer, G. Systems biology of cisplatin resistance: Past, present and future. Cell Death Dis., 2014, 5, e1257.
Perera, Y.; Farina, H.G.; Gil, J.; Rodriguez, A.; Benavent, F.; Castellanos, L.; Gómez, R.E.; Acevedo, B.E.; Alonso, D.F.; Perea, S.E. Anticancer peptide CIGB-300 binds to nucleophosmin/B23, impairs its CK2-mediated phosphorylation, and leads to apoptosis through its nucleolar disassembly activity. Mol. Cancer Ther., 2009, 8(5), 1189-1196.
Salvi, M.; Sarno, S.; Cesaro, L.; Nakamura, H.; Pinna, L.A. Extraordinary pleiotropy of protein kinase CK2 revealed by weblogo phosphoproteome analysis. Biochim. Biophys. Acta, 2009, 1793(5), 847-859.
Bian, Y.; Ye, M.; Wang, C.; Cheng, K.; Song, C.; Dong, M.; Pan, Y.; Qin, H.; Zou, H. Global screening of CK2 kinase substrates by an integrated phosphoproteomics workflow. Sci. Rep., 2013, 3, 3460.
Ruzzene, M.; Pinna, L.A. Addiction to protein kinase CK2: a common denominator of diverse cancer cells? Biochim. Biophys. Acta, 2010, 1804(3), 499-504.
Fitzpatrick, D.P.; You, J.S.; Bemis, K.G.; Wery, J.P.; Ludwig, J.R.; Wang, M. Searching for potential biomarkers of cisplatin resistance in human ovarian cancer using a label-free LC/MS-based protein quantification method. Proteomics Clin. Appl., 2007, 1(3), 246-263.
Desagher, S.; Osen-Sand, A.; Montessuit, S.; Magnenat, E.; Vilbois, F.; Hochmann, A.; Journot, L.; Antonsson, B.; Martinou, J.C. Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol. Cell, 2001, 8(3), 601-611.
Ruzzene, M.; Penzo, D.; Pinna, L.A. Protein kinase CK2 inhibitor 4,5,6,7-tetrabromobenzotriazole (TBB) induces apoptosis and caspase-dependent degradation of haematopoietic lineage cell-specific protein 1 (HS1) in Jurkat cells. Biochem. J., 2002, 364(Pt 1), 41-47.
Miller, S.J.; Lou, D.Y.; Seldin, D.C.; Lane, W.S.; Neel, B.G. Direct identification of PTEN phosphorylation sites. FEBS Lett., 2002, 528(1-3), 145-153.
Nguyen, E.V.; Huhtinen, K.; Goo, Y.A.; Kaipio, K.; Andersson, N.; Rantanen, V.; Hynninen, J.; Lahesmaa, R.; Carpen, O.; Goodlett, D.R. Hyper-phosphorylation of sequestosome-1 distinguishes resistance to cisplatin in patient derived high grade serous ovarian cancer cells. Mol. Cell. Proteomics, 2017, 16(7), 1377-1392.
Borgo, C.; Franchin, C.; Salizzato, V.; Cesaro, L.; Arrigoni, G.; Matricardi, L.; Pinna, L.A.; Donella-Deana, A. Protein kinase CK2 potentiates translation efficiency by phosphorylating eIF3j at Ser127. Biochim. Biophys. Acta, 2015, 1853(7), 1693-1701.
Homma, M.K.; Wada, I.; Suzuki, T.; Yamaki, J.; Krebs, E.G.; Homma, Y. CK2 phosphorylation of eukaryotic translation initiation factor 5 potentiates cell cycle progression. Proc. Natl. Acad. Sci. USA, 2005, 102(43), 15688-15693.
Olsen, J.V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell, 2006, 127(3), 635-648.
Jones, D.R.; Broad, R.M.; Madrid, L.V.; Baldwin, A.S. Jr.; Mayo, M.W. Inhibition of NF-kappa B sensitizes non-small cell lung cancer cells to chemotherapy-induced apoptosis. Ann. Thorac. Surg., 2000, 70(3), 930-937.
Sun, Y.; Guan, Z.; Liang, L.; Cheng, Y.; Zhou, J.; Li, J.; Xu, Y. NF-κB signaling plays irreplaceable roles in cisplatin-induced bladder cancer chemoresistance and tumor progression. Int. J. Oncol., 2016, 48(1), 225-234.
Heavey, S.; Godwin, P.; Baird, A.M.; Barr, M.P.; Umezawa, K.; Cuffe, S.; Finn, S.P.; O’Byrne, K.J.; Gately, K. Strategic targeting of the PI3K-NFκB axis in cisplatin-resistant NSCLC. Cancer Biol. Ther., 2014, 15(10), 1367-1377.
Barneda-Zahonero, B.; Parra, M. Histone deacetylases and cancer. Mol. Oncol., 2012, 6(6), 579-589.
Ashburner, B.P.; Westerheide, S.D.; Baldwin, A.S. Jr. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol., 2001, 21(20), 7065-7077.
Gueugnon, F.; Cartron, P.F.; Charrier, C.; Bertrand, P.; Fonteneau, J.F.; Gregoire, M.; Blanquart, C. New histone deacetylase inhibitors improve cisplatin antitumor properties against thoracic cancer cells. Oncotarget, 2014, 5(12), 4504-4515.
Piskareva, O.; Harvey, H.; Nolan, J.; Conlon, R.; Alcock, L.; Buckley, P.; Dowling, P.; Henry, M.; O’Sullivan, F.; Bray, I.; Stallings, R.L. The development of cisplatin resistance in neuroblastoma is accompanied by epithelial to mesenchymal transition in vitro. Cancer Lett., 2015, 364(2), 142-155.
Barcia, M.G.; Castro, J.M.; Jullien, C.D.; González, C.G.; Freire, M. Prothymosin alpha is phosphorylated by casein kinase-2. FEBS Lett., 1992, 312(2-3), 152-156.
Pérez-Estévez, A.; Díaz-Jullien, C.; Covelo, G.; Salgueiro, M.T.; Freire, M.A. 180-kDa protein kinase seems to be responsible for the phosphorylation of prothymosin alpha observed in proliferating cells. J. Biol. Chem., 1997, 272(16), 10506-10513.
Jin, L.; Huo, Y.; Zheng, Z.; Jiang, X.; Deng, H.; Chen, Y.; Lian, Q.; Ge, R.; Deng, H. Down-regulation of Ras-related protein Rab 5C-dependent endocytosis and glycolysis in cisplatin-resistant ovarian cancer cell lines. Mol. Cell. Proteomics, 2014, 13(11), 3138-3151.
Chavez, J.D.; Hoopmann, M.R.; Weisbrod, C.R.; Takara, K.; Bruce, J.E. Quantitative proteomic and interaction network analysis of cisplatin resistance in HeLa cells. PLoS One, 2011, 6(5), e19892.
Seger, D.; Gechtman, Z.; Shaltiel, S. Phosphorylation of vitronectin by casein kinase II. Identification of the sites and their promotion of cell adhesion and spreading. J. Biol. Chem., 1998, 273(38), 24805-24813.
Formby, B.; Stern, R. Phosphorylation stabilizes alternatively spliced CD44 mRNA transcripts in breast cancer cells: inhibition by antisense complementary to casein kinase II mRNA. Mol. Cell. Biochem., 1998, 187(1-2), 23-31.
Yanagawa, T.; Watanabe, H.; Takeuchi, T.; Fujimoto, S.; Kurihara, H.; Takagishi, K. Overexpression of autocrine motility factor in metastatic tumor cells: Possible association with augmented expression of KIF3A and GDI-beta. Lab. Invest., 2004, 84(4), 513-522.
Haga, A.; Niinaka, Y.; Raz, A. Phosphohexose isomerase/autocrine motility factor/neuroleukin/maturation factor is a multifunctional phosphoprotein. Biochim. Biophys. Acta, 2000, 1480(1-2), 235-244.
Kim, S.W.; Hasanuzzaman, M.; Cho, M.; Heo, Y.R.; Ryu, M.J.; Ha, N.Y.; Park, H.J.; Park, H.Y.; Shin, J.G. Casein kinase 2 (CK2)-mediated phosphorylation of Hsp90β as a novel mechanism of rifampin-induced MDR1 expression. J. Biol. Chem., 2015, 290(27), 17029-17040.
Tufo, G.; Jones, A.W.; Wang, Z.; Hamelin, J.; Tajeddine, N.; Esposti, D.D.; Martel, C.; Boursier, C.; Gallerne, C.; Migdal, C.; Lemaire, C.; Szabadkai, G.; Lemoine, A.; Kroemer, G.; Brenner, C. The protein disulfide isomerases PDIA4 and PDIA6 mediate resistance to cisplatin-induced cell death in lung adenocarcinoma. Cell Death Differ., 2014, 21(5), 685-695.
Castagna, A.; Antonioli, P.; Astner, H.; Hamdan, M.; Righetti, S.C.; Perego, P.; Zunino, F.; Righetti, P.G. A proteomic approach to cisplatin resistance in the cervix squamous cell carcinoma cell line A431. Proteomics, 2004, 4(10), 3246-3267.
Masters, S.C.; Subramanian, R.R.; Truong, A.; Yang, H.; Fujii, K.; Zhang, H.; Fu, H. Survival-promoting functions of 14-3-3 proteins. Biochem. Soc. Trans., 2002, 30(4), 360-365.
Sahara, S.; Aoto, M.; Eguchi, Y.; Imamoto, N.; Yoneda, Y.; Tsujimoto, Y. Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature, 1999, 401(6749), 168-173.
Hu, Y.; Yao, J.; Liu, Z.; Liu, X.; Fu, H.; Ye, K. Akt phosphorylates acinus and inhibits its proteolytic cleavage, preventing chromatin condensation. EMBO J., 2005, 24(20), 3543-3554.
Valiente, M.; Andrés-Pons, A.; Gomar, B.; Torres, J.; Gil, A.; Tapparel, C.; Antonarakis, S.E.; Pulido, R. Binding of PTEN to specific PDZ domains contributes to PTEN protein stability and phosphorylation by microtubule-associated serine/threonine kinases. J. Biol. Chem., 2005, 280(32), 28936-28943.
Nylandsted, J.; Rohde, M.; Brand, K.; Bastholm, L.; Elling, F.; Jäättelä, M. Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses BCl-2. Proc. Natl. Acad. Sci. USA, 2000, 97(14), 7871-7876.
Takayama, S.; Bimston, D.N.; Matsuzawa, S.; Freeman, B.C.; Aime-Sempe, C.; Xie, Z.; Morimoto, R.I.; Reed, J.C. BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J., 1997, 16(16), 4887-4896.
Saleh, A.; Srinivasula, S.M.; Balkir, L.; Robbins, P.D.; Alnemri, E.S. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol., 2000, 2(8), 476-483.
Ravagnan, L.; Gurbuxani, S.; Susin, S.A.; Maisse, C.; Daugas, E.; Zamzami, N.; Mak, T.; Jäättelä, M.; Penninger, J.M.; Garrido, C.; Kroemer, G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol., 2001, 3(9), 839-843.
Popanda, O.; Fox, G.; Thielmann, H.W. Modulation of DNA polymerases alpha, delta and epsilon by lactate dehydrogenase and 3-phosphoglycerate kinase. Biochim. Biophys. Acta, 1998, 1397(1), 102-117.
Widlak, P.; Pietrowska, M.; Lanuszewska, J. The role of chromatin proteins in DNA damage recognition and repair. Histochem. Cell Biol., 2006, 125(1-2), 119-126.
Lange, S.S.; Vasquez, K.M. HMGB1: The jack-of-all-trades protein is a master DNA repair mechanic. Mol. Carcinog., 2009, 48(7), 571-580.
Nagatani, G.; Nomoto, M.; Takano, H.; Ise, T.; Kato, K.; Imamura, T.; Izumi, H.; Makishima, K.; Kohno, K. Transcriptional activation of the human HMG1 gene in cisplatin-resistant human cancer cells. Cancer Res., 2001, 61(4), 1592-1597.
Li, S.L.; Ye, F.; Cai, W.J.; Hu, H.D.; Hu, P.; Ren, H.; Zhu, F.F.; Zhang, D.Z. Quantitative proteome analysis of multidrug resistance in human ovarian cancer cell line. J. Cell. Biochem., 2010, 109(4), 625-633.
Zeng, H.Z.; Qu, Y.Q.; Zhang, W.J.; Xiu, B.; Deng, A.M.; Liang, A.B. Proteomic analysis identified DJ-1 as a cisplatin resistant marker in non-small cell lung cancer. Int. J. Mol. Sci., 2011, 12(6), 3489-3499.
Stone, J.R.; Maki, J.L.; Collins, T. Basal and hydrogen peroxide stimulated sites of phosphorylation in heterogeneous nuclear ribonucleoprotein C1/C2. Biochemistry, 2003, 42(5), 1301-1308.
Kim, J.H.; Paek, K.Y.; Choi, K.; Kim, T.D.; Hahm, B.; Kim, K.T.; Jang, S.K. Heterogeneous nuclear ribonucleoprotein C modulates translation of C-myc mRNA in a cell cycle phase-dependent manner. Mol. Cell. Biol., 2003, 23(2), 708-720.
Holcík, M.; Gordon, B.W.; Korneluk, R.G. The internal ribosome entry site-mediated translation of antiapoptotic protein XIAP is modulated by the heterogeneous nuclear ribonucleoproteins C1 and C2. Mol. Cell. Biol., 2003, 23(1), 280-288.
Patry, C.; Bouchard, L.; Labrecque, P.; Gendron, D.; Lemieux, B.; Toutant, J.; Lapointe, E.; Wellinger, R.; Chabot, B. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res., 2003, 63(22), 7679-7688.
Zhang, J.; Ren, H.; Yuan, P.; Lang, W.; Zhang, L.; Mao, L. Down-regulation of hepatoma-derived growth factor inhibits anchorage-independent growth and invasion of non-small cell lung cancer cells. Cancer Res., 2006, 66(1), 18-23.
D’Aguanno, S.; D’Alessandro, A.; Pieroni, L.; Roveri, A.; Zaccarin, M.; Marzano, V.; De Canio, M.; Bernardini, S.; Federici, G.; Urbani, A. New insights into neuroblastoma cisplatin resistance: A comparative proteomic and meta-mining investigation. J. Proteome Res., 2011, 10(2), 416-428.
Ren, H.; Tang, X.; Lee, J.J.; Feng, L.; Everett, A.D.; Hong, W.K.; Khuri, F.R.; Mao, L. Expression of hepatoma-derived growth factor is a strong prognostic predictor for patients with early-stage non-small-cell lung cancer. J. Clin. Oncol., 2004, 22(16), 3230-3237.
Iwasaki, T.; Nakagawa, K.; Nakamura, H.; Takada, Y.; Matsui, K.; Kawahara, K. Hepatoma-derived growth factor as a prognostic marker in completely resected non-small-cell lung cancer. Oncol. Rep., 2005, 13(6), 1075-1080.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [338 - 349]
Pages: 12
DOI: 10.2174/1570164616666190126104325
Price: $58

Article Metrics

PDF: 13