Cancer Letters
Volume 286, Issue 2 , Pages 206-216 , 28 December 2009

MKP1 repression is required for the chemosensitizing effects of NF-κB and PI3K inhibitors to cisplatin in non-small cell lung cancer

  • María Cortes-Sempere

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
    • CIBER de Enfermedades Raras (CIBERER) Valencia, C/Álvaro de Bazán, 10 Valencia, Spain
    • These authors contributed equally to this manuscript.
  • ,
  • Sharmila Chattopadhyay

      Affiliations

    • Department of Pathology, University of California, San Diego, CA, United States
    • These authors contributed equally to this manuscript.
  • ,
  • Ana Rovira

      Affiliations

    • Medical Oncology Department, Hospital del Mar-IMAS, Barcelona, Spain
    • Cancer Research Program, IMIM-Hospital del Mar, PRBB, Barcelona, Spain
  • ,
  • Vanessa Rodriguez-Fanjul

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
    • CIBER de Enfermedades Raras (CIBERER) Valencia, C/Álvaro de Bazán, 10 Valencia, Spain
  • ,
  • Cristobal Belda-Iniesta

      Affiliations

    • Medical Oncology Department, Hospital La Paz, Madrid, Spain
  • ,
  • Marian Tapia

      Affiliations

    • Medical Oncology Department, Hospital del Mar-IMAS, Barcelona, Spain
    • Cancer Research Program, IMIM-Hospital del Mar, PRBB, Barcelona, Spain
  • ,
  • Paloma Cejas

      Affiliations

    • Medical Oncology Department, Hospital La Paz, Madrid, Spain
  • ,
  • Rosario Machado-Pinilla

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
    • CIBER de Enfermedades Raras (CIBERER) Valencia, C/Álvaro de Bazán, 10 Valencia, Spain
  • ,
  • Cristina Manguan-García

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
    • CIBER de Enfermedades Raras (CIBERER) Valencia, C/Álvaro de Bazán, 10 Valencia, Spain
  • ,
  • Isabel Sánchez-Pérez

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
    • CIBER de Enfermedades Raras (CIBERER) Valencia, C/Álvaro de Bazán, 10 Valencia, Spain
  • ,
  • Manuel Nistal

      Affiliations

    • Pathology Department Hospital La Paz, Madrid, Spain
  • ,
  • Carmen Moratilla

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
  • ,
  • Javier de Castro-Carpeño

      Affiliations

    • Medical Oncology Department, Hospital La Paz, Madrid, Spain
  • ,
  • Manuel Gonzalez-Barón

      Affiliations

    • Medical Oncology Department, Hospital La Paz, Madrid, Spain
  • ,
  • Joan Albanell

      Affiliations

    • Medical Oncology Department, Hospital del Mar-IMAS, Barcelona, Spain
    • Cancer Research Program, IMIM-Hospital del Mar, PRBB, Barcelona, Spain
  • ,
  • Rosario Perona

      Affiliations

    • Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain
    • CIBER de Enfermedades Raras (CIBERER) Valencia, C/Álvaro de Bazán, 10 Valencia, Spain
    • Corresponding Author InformationCorresponding author. Address: Translational Oncology Unit C.S.I.C./U.A.M: Instituto de Investigaciones Biomédicas C.S.I.C./U.A.M., C/Arturo Duperier, 4, Madrid 28029, Spain. Tel.: +34 91 5854463; fax: +34 91 5854401.

Received 12 January 2009 ,Revised 21 May 2009 ,Accepted 25 May 2009.

References 

  1. Eastman A. Interstrand cross-links and sequence specificity in the reaction of cis-dichloro(ethylenediamine)platinum(II) with DNA. Biochemistry. 1985;24:27–32
  2. Sanchez-Perez I, Martinez-Gomariz M, Williams D, Keyse SM, Perona R. CL100/MKP-1 modulates JNK activation and apoptosis in response to cisplatin. Oncogene. 2000;19:5142–5152
  3. Sanchez-Perez I, Murguia JR, Perona R. Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene. 1998;16:533–540
  4. Sanchez-Perez I, Perona R. Lack of c-Jun activity increases survival to cisplatin. FEBS Lett. 1999;453:151–158
  5. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer. 2002;2:489–501
  6. Baldwin AS. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J. Clin. Invest. 2001;107:241–246
  7. Lau LF, Nathans D. Identification of a set of genes expressed during the G0/G1 transition of cultured mouse cells. EMBO J. 1985;4:3145–3151
  8. Charles CH, Abler AS, Lau LF. cDNA sequence of a growth factor-inducible immediate early gene and characterization of its encoded protein. Oncogene. 1992;7:187–190
  9. Chattopadhyay S, Machado-Pinilla R, Manguan-Garcia C, et al. MKP1/CL100 controls tumor growth and sensitivity to cisplatin in non-small-cell lung cancer. Oncogene. 2006;25:3335–3345
  10. Toker A, Newton AC. Cellular signaling: pivoting around PDK-1. Cell. 2000;103:185–188
  11. Wymann MP, Pirola L. Structure and function of phosphoinositide 3-kinases. Biochim. Biophys. Acta. 1998;1436:127–150
  12. Di Cristofano A, Pandolfi PP. The multiple roles of PTEN in tumor suppression. Cell. 2000;100:387–390
  13. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91:231–241
  14. Cardone MH, Roy N, Stennicke HR, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science. 1998;282:1318–1321
  15. Chun KH, Kosmeder JW, Sun S, et al. Effects of deguelin on the phosphatidylinositol 3-kinase/Akt pathway and apoptosis in premalignant human bronchial epithelial cells. J. Natl. Cancer Inst. 2003;95:291–302
  16. Lee HY, Srinivas H, Xia D, et al. Evidence that phosphatidylinositol 3-kinase- and mitogen-activated protein kinase kinase-4/c-Jun NH2-terminal kinase-dependent pathways cooperate to maintain lung cancer cell survival. J. Biol. Chem. 2003;278:23630–23638
  17. Brognard J, Clark AS, Ni Y, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res. 2001;61:3986–3997
  18. Lee HY, Oh SH, Suh YA, et al. Response of non-small cell lung cancer cells to the inhibitors of phosphatidylinositol 3-kinase/Akt- and MAPK kinase 4/c-Jun NH2-terminal kinase pathways: an effective therapeutic strategy for lung cancer. Clin. Cancer Res. 2005;11:6065–60674
  19. Wang CY, Guttridge DC, Mayo MW, Baldwin AS. NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 1999;19:5923–5929
  20. Finco TS, Baldwin AS. Mechanistic aspects of NF-kappa B regulation: the emerging role of phosphorylation and proteolysis. Immunity. 1995;3:263–272
  21. Matthews JR, Hay RT. Regulation of the DNA binding activity of NF-kappa B. Int. J. Biochem. Cell Biol. 1995;27:865–879
  22. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004;25:280–288
  23. Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science. 1995;267:1485–1488
  24. Traenckner EB, Pahl HL, Henkel T, Schmidt KN, Wilk S, Baeuerle PA. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J. 1995;14:2876–28783
  25. DiDonato J, Mercurio F, Rosette C, et al. Mapping of the inducible IkappaB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 1996;16:1295–1304
  26. Dejardin E, Droin NM, Delhase M, et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity. 2002;17:525–535
  27. Sanchez-Perez I, Benitah SA, Martinez-Gomariz M, Lacal JC, Perona R. Cell stress and MEKK1-mediated c-Jun activation modulate NF-κB activity and cell viability. Mol. Biol. Cell. 2002;13:2933–2945
  28. Devary Y, Rosette C, DiDonato JA, Karin M. NF-kappa B activation by ultraviolet light not dependent on a nuclear signal. Science. 1993;261:1442–1445
  29. Russo A, Fratto ME, Bazan V, Schiró V, Agnese V, Cicero G, et al. Targeting apoptosis in solid tumors: the role of Bortezomib from preclinical to clinical evidence. Expert. Opin. Ther. Targets. 2007;11:1571–1586
  30. Perona R, Montaner S, Saniger L, Sanchez-Perez I, Bravo R, Lacal JC. Activation of the nuclear factor-kappaB by Rho, CDC42, and Rac-1 proteins. Genes Dev. 1997;11:463–475
  31. Schmitz ML, dos Santos Silva MA, Baeuerle PA. Transactivation domain 2 (TA2) of p65 NF-kappa B. Similarity to TA1 and phorbol ester-stimulated activity and phosphorylation in intact cells. J. Biol. Chem. 1995;270:15576–15584
  32. Tichelaar JW, Zhang Y, leRiche JC, Biddinger PW, Lam S, Anderson MW. Increased staining for phospho-Akt, p65/RELA and cIAP-2 in pre-neoplastic human bronchial biopsies. BMC Cancer. 2005;5:155–159
  33. Tsurutani J, Steinberg SM, Ballas M, et al. Prognostic significance of clinical factors and Akt activation in patients with bronchioloalveolar carcinoma. Lung Cancer. 2007;55:115–121
  34. Tsurutani J, Castillo SS, Brognard J, et al. Tobacco components stimulate Akt-dependent proliferation and NFkappaB-dependent survival in lung cancer cells. Carcinogenesis. 2005;26:1182–1195
  35. Mabuchi S, Ohmichi M, Nishio Y, et al. Inhibition of NFkappaB increases the efficacy of cisplatin in in vitro and in vivo ovarian cancer models. J. Biol. Chem. 2004;279:23477–23485
  36. Dejardin E. The alternative NF-kappaB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochem. Pharmacol. 2006;72:1161–1179
  37. Voboril R, Hochwald SN, Li J, et al. Inhibition of NF-kappa B augments sensitivity to 5-fluorouracil/folinic acid in colon cancer. J. Surg. Res. 2004;120:178–188
  38. Montagut C, Tusquets I, Ferrer B, et al. Activation of nuclear factor-kappa B is linked to resistance to neoadjuvant chemotherapy in breast cancer patients. Endocr. Relat. Cancer. 2006;13:607–616
  39. Wang X, Ju W, Renouard J, Aden J, Belinsky SA, Lin Y. 17-allylamino-17-demethoxygeldanamycin synergistically potentiates tumor necrosis factor-induced lung cancer cell death by blocking the nuclear factor-kappaB pathway. Cancer Res. 2006;66:1089–1095
  40. Fanucchi MP, Fossella FV, Belt R, Natale R, Fidias P, Carbone DP, et al. Randomized phase II study of Bortezomib alone and Bortezomib in combination with docetaxel in previously treated advanced non-small-cell lung cancer. J. Clin. Oncol. 2006;24:5025–5033

PII: S0304-3835(09)00376-0

doi: 10.1016/j.canlet.2009.05.029

Cancer Letters
Volume 286, Issue 2 , Pages 206-216 , 28 December 2009