Inhibition of p38 mitogen-activated protein kinase alters microRNA expression and reverses epithelial-to-mesenchymal transition

International Journal of Oncology

Volumn 42, Issue 4, 2013, Pages 1139-1150

  Antoon, James W ^a   Nitzchke, Ashley M ^a   Martin, Elizabeth C ^a   Rhodes, Lyndsay V ^a   Nam, Seungyoon ^b   Wadsworth, Scott ^c   Salvo, Virgilo A ^a   Elliott, Steven ^a   Collins Burow, Bridgette ^a   Nephew, Kenneth P ^b   Burow, Matthew E ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

Breast cancer; Drug discovery; Epithelial to mesenchymal transition; P38 mitogen activated protein kinase

Indexed keywords

4 [4 (4 FLUOROPHENYL) 1 (3 PHENYLPROPYL) 5 (4 PYRIDINYL) 1H IMIDAZOL 2 YL] 3 BUTYN 1 OL; ACTIVATING TRANSCRIPTION FACTOR; DEATH RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 199; MICRORNA 200; MICRORNA 302; MICRORNA 303; MICRORNA 328; MITOGEN ACTIVATED PROTEIN KINASE P38; NERVE CELL ADHESION MOLECULE; PROTEIN; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; ZEB PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CANCER MODEL; CANCER RESISTANCE; CLONOGENESIS; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; GENE FUNCTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SURVIVAL TIME; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; HUMANS; IMIDAZOLES; MAP KINASE SIGNALING SYSTEM; MCF-7 CELLS; MICE; MICRORNAS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; TRANSCRIPTOME; TUMOR NECROSIS FACTOR-ALPHA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84874588628     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1814     Document Type: Article

References (90)

1. Kaufmann SH and Earnshaw WC: Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256:42-49, 2000.
2. Seidman AD: Chemotherapy for advanced breast cancer: a current perspective. Semin Oncol 23:55-59, 1996.
3. Hsu H, Xiong J and Goeddel DV: The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81:495-504, 1995.
4. Herrnring C, Reimer T, Jeschke U, et al: Expression of the apoptosis-inducing ligands FasL and TRAIL in malignant and benign human breast tumors. Histochem Cell Biol 113:189-194, 2000.
5. Zyad A, Benard J, Tursz T, Clarke R and Chouaib S: Resistance to TNF-alpha and adriamycin in the human breast cancer MCF-7 cell line: relationship to MDR1, MnSOD, and TNF gene expression. Cancer Res 54:825-831, 1994.
6. Zyad A, Branellec D, Mahe Y, Tursz T and Chouaib S: The development of human tumor-cell resistance to TNF-alpha does not confer resistance to cytokine-induced cellular cytotoxic mechanisms. Int J Cancer 52:953-958, 1992.
7. Gatti L and Zunino F: Overview of tumor cell chemoresistance mechanisms. Methods Mol Med 111:127-148, 2005.
8. Gottesman MM: Mechanisms of cancer drug resistance. Annu Rev Med 53:615-627, 2002.
9. Huber MA, Azoitei N, Baumann B, et al: NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 114:569-581, 2004.
10. Radisky DC and Bissell MJ: NF-kappaB links oestrogen receptor signalling and EMT. Nat Cell Biol 9:361-363, 2007.
11. Park S, Song J, Joe CO and Shin I: Akt stabilizes estrogen receptor alpha with the concomitant reduction in its transcriptional activity. Cell Signal 20:1368-1374, 2008.
12. Frigo DE, Vigh KA, Struckhoff AP, et al: Xenobiotic-induced TNF-alpha expression and apoptosis through the p38 MAPK signaling pathway. Toxicol Lett 155:227-238, 2005.
13. Thomas RS, Sarwar N, Phoenix F, Coombes RC and Ali S: Phosphorylation at serines 104 and 106 by Erk1/2 MAPK is important for estrogen receptor-alpha activity. J Mol Endocrinol 40:173-184, 2008.
14. Santen RJ, Song RX, McPherson R, et al: The role of mitogen-activated protein (MAP) kinase in breast cancer. J Steroid Biochem Mol Biol 80:239-256, 2002.
15. Ballif BA and Blenis J: Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ 12:397-408, 2001.
16. Geh E, Meng Q, Mongan M, et al: Mitogen-activated protein kinase kinase kinase 1 (MAP3K1) integrates developmental signals for eyelid closure. Proc Natl Acad Sci USA 108:17349-17354, 2011.
17. Kyriakis JM and Avruch J: Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807-869, 2001.
18. Guo YL, Kang B, Han J and Williamson JR: p38beta MAP kinase protects rat mesangial cells from TNF-alpha-induced apoptosis. J Cell Biochem 82:556-565, 2001.
19. Bulavin DV, Saito S, Hollander MC, et al: Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 18:6845-6854, 1999.
20. Driggers PH, Segars JH and Rubino DM: The proto-oncoprotein Brx activates estrogen receptor beta by a p38 mitogen-activated protein kinase pathway. J Biol Chem 276:46792-46797, 2001.
21. Madrid LV, Mayo MW, Reuther JY and Baldwin AS Jr: Akt stimulates the transactivation potential of the RelA/p65 subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J Biol Chem 276:18934-18940, 2001.
22. Zimmermann J, Lamerant N, Grossenbacher R and Furst P: Proteasome-and p38-dependent regulation of ERK3 expression. J Biol Chem 276:10759-10766, 2001.
23. Waas WF, Lo HH and Dalby KN: The kinetic mechanism of the dual phosphorylation of the ATF2 transcription factor by p38 mitogen-activated protein (MAP) kinase alpha. Implications for signal/response profiles of MAP kinase pathways. J Biol Chem 276:5676-5684, 2001.
24. Bradham C and McClay DR: p38 MAPK in development and cancer. Cell Cycle 5:824-828, 2006.
25. Maemura M, Iino Y, Koibuchi Y, Yokoe T and Morishita Y: Mitogen-activated protein kinase cascade in breast cancer. Oncology 57(Suppl 2):37-44, 1999.
26. Weldon CB, Burow ME, Rolfe KW, Clayton JL, Jaffe BM and Beckman BS: NF-kappa B-mediated chemoresistance in breast cancer cells. Surgery 130:143-150, 2001.
27. Weldon CB, Parker AP, Patten D, et al: Sensitization of apoptotically-resistant breast carcinoma cells to TNF and TRAIL by inhibition of p38 mitogen-activated protein kinase signaling. Int J Oncol 24:1473-1480, 2004.
28. Weldon CB, Scandurro AB, Rolfe KW, et al: Identification of mitogen-activated protein kinase kinase as a chemoresistant pathway in MCF-7 cells by using gene expression microarray. Surgery 132:293-301, 2002.
29. Frigo DE, Tang Y, Beckman BS, et al: Mechanism of AP-1-mediated gene expression by select organochlorines through the p38 MAPK pathway. Carcinogenesis 25:249-261, 2004.
30. Ma L, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449:682-688, 2007.
31. Si ML, Zhu S, Wu H, Lu Z, Wu F and Mo YY: miR-21-mediated tumor growth. Oncogene 26:2799-2803, 2007.
32. Chen GQ, Zhao ZW, Zhou HY, Liu YJ and Yang HJ: Systematic analysis of microRNA involved in resistance of the MCF-7 human breast cancer cell to doxorubicin. Med Oncol 27:406-415, 2010.
33. Park SM, Gaur AB, Lengyel E and Peter ME: The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22:894-907, 2008.
34. Antoon JW, Liu J, Gestaut MM, Burow ME, Beckman BS and Foroozesh M: Design, synthesis, and biological activity of a family of novel ceramide analogues in chemoresistant breast cancer cells. J Med Chem 52:5748-5752, 2009.
35. Struckhoff AP, Bittman R, Burow ME, et al: Novel ceramide analogs as potential chemotherapeutic agents in breast cancer. J Pharmacol Exp Ther 309:523-532, 2004.
36. Zhou C, Nitschke AM, Xiong W, et al: Proteomic analysis of tumor necrosis factor-alpha resistant human breast cancer cells reveals a MEK5/Erk5-mediated epithelial-mesenchymal transition phenotype. Breast Cancer Res 10:R105, 2008.
37. Antoon JW, Lai R, Struckhoff AP, et al: Altered death receptor signaling promotes epithelial-to-mesenchymal transition and acquired chemoresistance. Sci Rep 2:539, 2012.
38. Antoon JW, White MD, Burow ME and Beckman BS: Dual inhibition of sphingosine kinase isoforms ablates TNF-induced drug resistance. Oncol Rep 27:1779-1786, 2012.
39. Antoon JW, White MD, Slaughter EM, et al: Targeting NF. B mediated breast cancer chemoresistance through selective inhibition of sphingosine kinase-2. Cancer Biol Ther 11:678-689, 2011.
40. Wadsworth SA, Cavender DE, Beers SA, et al: RWJ 67657, a potent, orally active inhibitor of p38 mitogen-activated protein kinase. J Pharmacol Exp Ther 291:680-687, 1999.
41. Antoon JW, Bratton MR, Guillot LM, et al: Pharmacology and anti-tumor activity of RWJ67657, a novel inhibitor of p38 mitogen activated protein kinase. Am J Cancer Res 2:446-458, 2012.
42. Antoon JW, Bratton MR, Guillot LM, Wadsworth S, Salvo VA and Burow ME: Inhibition of p38-MAPK alters SRC coactivation and estrogen receptor phosphorylation. Cancer Biol Ther 13:1026-1033, 2012.
43. Antoon JW, Liu J, Ponnapakkam AP, Gestaut MM, Foroozesh M and Beckman BS: Novel D: -erythro N-octanoyl sphingosine analogs as chemo-and endocrine-resistant breast cancer therapeutics. Cancer Chemother Pharmacol 65:1191-1195, 2010.
44. Antoon JW and Beckman BS: Anti-proliferative effects of the novel ceramide analog (S)-2-(benzylideneamino)-3-hydroxy-N-tetrade-cylpropanamide in chemoresistant cancer. Bioorg Med Chem Lett 22:2624-2628, 2012.
45. Rhodes LV, Nitschke AM, Segar HC, et al: The histone deacetylase inhibitor trichostatin A alters microRNA expression profiles in apoptosis-resistant breast cancer cells. Oncol Rep 27:10-16, 2012.
46. Antoon JW, White MD, Driver JL, Burow ME and Beckman BS: Sphingosine kinase isoforms as a therapeutic target in endocrine therapy resistant luminal and basal-A breast cancer. Exp Biol Med (Maywood) 237:832-844, 2012.
47. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ and Reed MW: Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285:194-204, 2000.
48. Antoon JW, Meacham WD, Bratton MR, et al: Pharmacological inhibition of sphingosine kinase isoforms alters estrogen receptor signaling in human breast cancer. J Mol Endocrinol 46:205-216, 2011.
49. Bratton MR, Antoon JW, Duong BN, et al: Gao potentiates estrogen receptor a activity via the ERK signaling pathway. J Endocrinol 214:45-54, 2012.
50. Collins-Burow BM, Antoon JW, Frigo DE, et al: Antiestrogenic activity of flavonoid phytochemicals mediated via the c-Jun. N-terminal protein kinase pathway. Cell-type specific regulation of estrogen receptor alpha. Journal Steroid Biochem Mol Biol 132:186-193, 2012.
51. Antoon JW, White MD, Meacham WD, et al: Antiestrogenic effects of the novel sphingosine kinase-2 inhibitor ABC294640. Endocrinology 151:5124-5135, 2010.
52. Payton-Stewart F, Schoene NW, Kim YS, et al: Molecular effects of soy phytoalexin glyceollins in human prostate cancer cells LNCaP. Mol Carcinog 48:862-871, 2009.
53. Rhodes LV, Antoon JW, Muir SE, Elliott S, Beckman BS and Burow ME: Effects of human mesenchymal stem cells on ER-positive human breast carcinoma cells mediated through ER-SDF-1/CXCR4 crosstalk. Mol Cancer 9:295, 2010.
54. Rhodes LV, Short SP, Neel NF, et al: Cytokine receptor CXCR4 mediates estrogen-independent tumorigenesis, metastasis, and resistance to endocrine therapy in human breast cancer. Cancer Res 71:603-613, 2011.
55. Walker CH, Drew BA, Antoon JW, Kalueff AV and Beckman BS: Neurocognitive effects of chemotherapy and endocrine therapies in the treatment of breast cancer: recent perspectives. Cancer Invest 30:135-148, 2011.
56. Clarke R, Thompson EW, Leonessa F, et al: Hormone resistance, invasiveness, and metastatic potential in breast cancer. Breast Cancer Res Treat 24:227-239, 1993.
57. Nakanishi H, Taylor RM, Chrest FJ, et al: Progression of hormone-dependent adenocarcinoma cells to hormone-independent spindle carcinoma cells in vitro in a clonal spontaneous rat mammary tumor cell line. Cancer Res 55:399-407, 1995.
58. Murphy LC and Dotzlaw H: Variant estrogen receptor mRNA species detected in human breast cancer biopsy samples. Mol Endocrinol 3:687-693, 1989.
59. Rhodes LV, Muir SE, Elliott S, et al: Adult human mesenchymal stem cells enhance breast tumorigenesis and promote hormone independence. Breast Cancer Res Treat 121:293-300, 2010.
60. Di Leva G, Gasparini P, Piovan C, et al: MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J Natl Cancer Inst 102:706-721, 2010.
61. Sonkoly E, Lovén J, Xu N, et al: MicroRNA-203 functions as a tumor suppressor in basal cell carcinoma. Oncogenesis 1:e3, 2012.
62. Burk U, Schubert J, Wellner U, et al: A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9:582-589, 2008.
63. le Sage C, Nagel R, Egan DA, et al: Regulation of the p27 (Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 26:3699-3708, 2007.
64. Massarweh S, Osborne CK, Creighton CJ, et al: Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res 68:826-833, 2008.
65. Massarweh S and Schiff R: Unraveling the mechanisms of endocrine resistance in breast cancer: new therapeutic opportunities. Clin Cancer Res 13:1950-1954, 2007.
66. Obrero M, Yu DV and Shapiro DJ: Estrogen receptor-dependent and estrogen receptor-independent pathways for tamoxifen and 4-hydroxytamoxifen-induced programmed cell death. J Biol Chem 277:45695-45703, 2002.
67. St-Laurent V, Sanchez M, Charbonneau C and Tremblay A: Selective hormone-dependent repression of estrogen receptor beta by a p38-activated ErbB2/ErbB3 pathway. J Steroid Biochem Mol Biol 94:23-37, 2005.
68. Cannell IG, Kong YW, Johnston SJ, et al: p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci USA 107:5375-5380, 2010.
69. Yang F, Yin Y, Wang F, et al: miR-17-5p promotes migration of human hepatocellular carcinoma cells through the p38 mitogen-activated protein kinase-heat shock protein 27 pathway. Hepatology 51:1614-1623, 2010.
70. Rajaram MV, Ni B, Morris JD, et al: Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc Natl Acad Sci USA 108:17408-17413, 2011.
71. Akhtar N, Rasheed Z, Ramamurthy S, Anbazhagan AN, Voss FR and Haqqi TM: MicroRNA-27b regulates the expression of matrix metalloproteinase 13 in human osteoarthritis chondrocytes. Arthritis Rheum 62:1361-1371, 2010.
72. Ben-Hamo R and Efroni S: Gene expression and network-based analysis reveals a novel role for hsa-miR-9 and drug control over the p38 network in glioblastoma multiforme progression. Genome Med 3:77, 2011.
73. Zaman MS, Shahryari V, Deng G, et al: Up-regulation of microRNA-21 correlates with lower kidney cancer survival. PloS One 7:e31060, 2012.
74. Alam J, Wicks C, Stewart D, et al: Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J Biol Chem 275:27694-27702, 2000.
75. Liu Z, Zhu J, Cao H, Ren H and Fang X: miR-10b promotes cell invasion through RhoC-AKT signaling pathway by targeting HOXD10 in gastric cancer. Int J Oncol 40:1553-1560, 2012.
76. Li G, Wu Z, Peng Y, et al: MicroRNA-10b induced by Epstein-Barr virus-encoded latent membrane protein-1 promotes the metastasis of human nasopharyngeal carcinoma cells. Cancer Lett 299:29-36, 2010.
77. Ng YH, Zhu H and Leung PC: Twist modulates human trophoblastic cell invasion via regulation of N-cadherin. Endocrinology 153:925-936, 2012.
78. Alexander NR, Tran NL, Rekapally H, Summers CE, Glackin C and Heimark RL: N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res 66:3365-3369, 2006.
79. Kovalchuk O, Filkowski J, Meservy J, et al: Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther 7:2152-2159, 2008.
80. Yang H, Kong W, He L, et al: MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res 68:425-433, 2008.
81. Ma J, Dong C and Ji C: MicroRNA and drug resistance. Cancer Gene Ther 17:523-531, 2010.
82. Xin F, Li M, Balch C, et al: Computational analysis of microRNA profiles and their target genes suggests significant involvement in breast cancer antiestrogen resistance. Bioinformatics 25:430-434, 2009.
83. Burow ME, Weldon CB, Melnik LI, et al: PI3-K/AKT regulation of NF-kappaB signaling events in suppression of TNF-induced apoptosis. Biochem Biophys Res Commun 271:342-345, 2000.
84. Frigo DE, Basu A, Nierth-Simpson EN, et al: p38 mitogen-activated protein kinase stimulates estrogen-mediated transcription and proliferation through the phosphorylation and potentiation of the p160 coactivator glucocorticoid receptor-interacting protein 1. Mol Endocrinol 20:971-983, 2006.
85. Bourguignon LY, Wong G, Earle C, Krueger K and Spevak CC: Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion. J Biol Chem 285:36721-36735, 2010.
86. Croce CM: Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10:704-714, 2009.
87. Zhu S, Wu H, Wu F, Nie D, Sheng S and Mo YY: MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18:350-359, 2008.
88. Grund EM, Kagan D, Tran CA, et al: Tumor necrosis factor-alpha regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor kappaB in human endometriotic epithelial cells. Mol Pharmacol 73:1394-1404, 2008.
89. Kolosova I, Nethery D and Kern JA: Role of Smad2/3 and p38 MAP kinase in TGF-β1-induced epithelial-mesenchymal transition of pulmonary epithelial cells. J Cell Physiol 226:1248-1254, 2011.
90. Strippoli R, Benedicto I, Foronda M, et al: p38 maintains E-cadherin expression by modulating TAK1-NF-kappa B during epithelial-to-mesenchymal transition. J Cell Sci 123:4321-4331, 2010.