Translational control of PML contributes to TNFα-induced apoptosis of MCF7 breast cancer cells and decreased angiogenesis in HUVECs

Cell Death and Differentiation

Volumn 23, Issue 3, 2016, Pages 469-483

  Hsu, K S ^a   Guan, B J ^a   Cheng, X ^a   Guan, D ^a   Lam, M ^b   Hatzoglou, M ^a   Kao, H Y ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIREFLY LUCIFERASE; HISTONE DEACETYLASE 7; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PROMYELOCYTIC LEUKEMIA PROTEIN; RENILLA LUCIFERIN 2 MONOOXYGENASE; STRESS ACTIVATED PROTEIN KINASE 1; STROMELYSIN 2; TUMOR NECROSIS FACTOR ALPHA; 5' UNTRANSLATED REGION; CCL2 PROTEIN, HUMAN; INTERNAL RIBOSOME ENTRY SITE; MKNK1 PROTEIN, HUMAN; MMP10 PROTEIN, HUMAN; NUCLEAR PROTEIN; PML PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TNF PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR; TUMOR SUPPRESSOR PROTEIN;

5' UNTRANSLATED REGION; ANGIOGENESIS; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BREAST CANCER; CELL FRACTIONATION; CELL MIGRATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; FEMALE; GENE CONTROL; HEK293 CELL LINE; HELA CELL LINE; HL 60 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; MCF 7 CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; TRANSLATION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; BREAST TUMOR; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; HL-60 CELL LINE; MCF-7 CELL LINE; METABOLISM; PHYSIOLOGY;

5' UNTRANSLATED REGIONS; APOPTOSIS; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CCL2; GENE EXPRESSION REGULATION, NEOPLASTIC; HL-60 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERNAL RIBOSOME ENTRY SITES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MATRIX METALLOPROTEINASE 10; MCF-7 CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; NUCLEAR PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEINS;

EID: 84957436723     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.114     Document Type: Article

References (80)

1. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci USA 1975; 72: 3666-3670.
2. Pasparakis M. Regulation of tissue homeostasis by NF-kappaB signalling: implications for inflammatory diseases. Nat Rev Immunol 2009; 9: 778-788.
3. Aggarwal BB, Gupta SC, Kim JH. Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood 2012; 119: 651-665.
4. Cheng X, Liu Y, Chu H, Kao HY. Promyelocytic leukemia protein (PML) regulates endothelial cell network formation and migration in response to tumor necrosis factor alpha (TNFalpha) and interferon alpha (IFNalpha). J Biol Chem 2012; 287: 23356-23367.
5. Gao C, Cheng X, Lam M, Liu Y, Liu Q, Chang KS et al. Signal-dependent regulation of transcription by histone deacetylase 7 involves recruitment to promyelocytic leukemia protein nuclear bodies. Mol Biol Cell 2008; 19: 3020-3027.
6. Zhang Y, Herbert BS, Rajashekhar G, Ingram DA, Yoder MC, Clauss M et al. Premature senescence of highly proliferative endothelial progenitor cells is induced by tumor necrosis factor-alpha via the p38 mitogen-activated protein kinase pathway. FASEB J 2009; 23: 1358-1365.
7. Janzen C, Sen S, Cuevas J, Reddy ST, Chaudhuri G. Protein phosphatase 2A promotes endothelial survival via stabilization of translational inhibitor 4E-BP1 following exposure to tumor necrosis factor-alpha. Arterioscler Thromb Vasc Biol 2011; 31: 2586-2594.
8. Wu W-S, Xu Z-X, Hittelman WN, Salomoni P, Pandolfi PP, Chang K-S. Promyelocytic leukemia protein sensitizes tumor necrosis factor-induced apoptosis by inhibiting the NF-B survival pathway. J Biol Chem 2003; 278: 12294-12304.
9. Jeffrey IW, Bushell M, Tilleray VJ, Morley S, Clemens MJ. Inhibition of protein synthesis in apoptosis: differential requirements by the tumor necrosis factor alpha family and a DNAdamaging agent for caspases and the double-stranded RNA-dependent protein kinase. Cancer Res 2002; 62: 2272-2280.
10. Bernardi R, Pandolfi PP. Role of PML and the PML-nuclear body in the control of programmed cell death. Oncogene 2003; 22: 9048-9057.
11. Wang ZG, Ruggero D, Ronchetti S, Zhong S, Gaboli M, Rivi R et al. PML is essential for multiple apoptotic pathways. Nat Genet 1998; 20: 266-272.
12. Clemens MJ, Bushell M, Jeffrey IW, Pain VM, Morley SJ. Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ 2000; 7: 603-615.
13. Quignon F, De Bels F, Koken M, Feunteun J, Ameisen JC, de The H. PML induces a novel caspase-independent death process. Nat Genet 1998; 20: 259-265.
14. Pages G, Lenormand P, L'Allemain G, Chambard JC, Meloche S, Pouyssegur J. Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc Natl Acad Sci USA 1993; 90: 8319-8323.
15. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9: 537-549.
16. Beg AA, Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 1996; 274: 782-784.
17. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res 2005; 15: 11-18.
18. Zhong S, Salomoni P, Pandolfi PP. The transcriptional role of PML and the nuclear body. Nat Cell Biol 2000; 2: E85-E90.
19. Lallemand-Breitenbach V, de Thé H. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2: a000661.
20. Lapi E, Di Agostino S, Donzelli S, Gal H, Domany E, Rechavi G et al. PML, YAP, and p73 are components of a proapoptotic autoregulatory feedback loop. Mol Cell 2008; 32: 803-814.
21. Van Damme E, Laukens K, Dang TH, Van Ostade X. A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. Int J Biol Sci 2010; 6: 51-67.
22. Pearson M, Carbone R, Sebastiani C, Cioce M, Fagioli M, Saito S et al. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 2000; 406: 207-210.
23. Mu ZM, Le XF, Vallian S, Glassman AB, Chang KS. Stable overexpression of PML alters regulation of cell cycle progression in HeLa cells. Carcinogenesis 1997; 18: 2063-2069.
24. Gurrieri C, Capodieci P, Bernardi R, Scaglioni PP, Nafa K, Rush LJ et al. Loss of the tumor suppressor PML in human cancers of multiple histologic origins. J Natl Cancer Inst 2004; 96: 269-279.
25. Cheng X, Kao HY. Microarray analysis revealing common and distinct functions of promyelocytic leukemia protein (PML) and tumor necrosis factor alpha (TNFalpha) signaling in endothelial cells. BMC Genomics 2012; 13: 453.
26. Gao C, Ho CC, Reineke E, Lam M, Cheng X, Stanya KJ et al. Histone deacetylase 7 promotes PML sumoylation and is essential for PML nuclear body formation. Mol Cell Biol 2008; 28: 5658-5667.
27. Reineke EL, Lam M, Liu Q, Liu Y, Stanya KJ, Chang KS et al. Degradation of the tumor suppressor PML by Pin1 contributes to the cancer phenotype of breast cancer MDAMB-231 cells. Mol Cell Biol 2008; 28: 997-1006.
28. Yuan WC, Lee YR, Huang SF, Lin YM, Chen TY, Chung HC et al. A Cullin3-KLHL20 ubiquitin ligase-dependent pathway targets PML to potentiate HIF-1 signaling and prostate cancer progression. Cancer Cell 2011; 20: 214-228.
29. Jeanne M, Lallemand-Breitenbach V, Ferhi O, Koken M, Le Bras M, Duffort S et al. PML/RARA oxidation and arsenic binding initiate the antileukemia response of As2O3. Cancer Cell 2010; 18: 88-98.
30. Li W, Thakor N, Xu EY, Huang Y, Chen C, Yu R et al. An internal ribosomal entry site mediates redox-sensitive translation of Nrf2. Nucleic Acids Res 2010; 38: 778-788.
31. Yang DQ, Halaby MJ, Zhang Y. The identification of an internal ribosomal entry site in the 5'-untranslated region of p53 mRNA provides a novel mechanism for the regulation of its translation following DNA damage. Oncogene 2006; 25: 4613-4619.
32. Coldwell MJ, Mitchell SA, Stoneley M, MacFarlane M, Willis AE. Initiation of Apaf-1 translation by internal ribosome entry. Oncogene 2000; 19: 899-905.
33. Holcik M, Lefebvre C, Yeh C, Chow T, Korneluk RG. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat Cell Biol 1999; 1: 190-192.
34. Henis-Korenblit S, Strumpf NL, Goldstaub D, Kimchi A. A novel form of DAP5 protein accumulates in apoptotic cells as a result of caspase cleavage and internal ribosome entry site-mediated translation. Mol Cell Biol 2000; 20: 496-506.
35. Stoneley M, Chappell SA, Jopling CL, Dickens M, MacFarlane M, Willis AE. c-Myc protein synthesis is initiated from the internal ribosome entry segment during apoptosis. Mol Cell Biol 2000; 20: 1162-1169.
36. Shi Y, Frost P, Hoang B, Yang Y, Fukunaga R, Gera J et al. MNK kinases facilitate c-myc IRES activity in rapamycin-treated multiple myeloma cells. Oncogene 2013; 32: 190-197.
37. Shi Y, Sharma A, Wu H, Lichtenstein A, Gera J. Cyclin D1 and c-myc internal ribosome entry site (IRES)-dependent translation is regulated by AKT activity and enhanced by rapamycin through a p38 MAPK-and ERK-dependent pathway. J Biol Chem 2005; 280: 10964-10973.
38. de Nadal E, Ammerer G, Posas F. Controlling gene expression in response to stress. Nat Rev Genet 2011; 12: 833-845.
39. Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 2004; 68: 320-344.
40. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, Lebiedzinska M et al. PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 2010; 330: 1247-1251.
41. Scaglioni PP, Yung TM, Cai LF, Erdjument-Bromage H, Kaufman AJ, Singh B et al. A CK2-dependent mechanism for degradation of the PML tumor suppressor. Cell 2006; 126: 269-283.
42. Brown MC, Bryant JD, Dobrikova EY, Shveygert M, Bradrick SS, Chandramohan V et al. Induction of viral, m7G-cap-independent translation and oncolysis by MAPK interacting kinase (MNK)-mediated effects on the Ser-Arg rich protein kinase, SRPK. J Virol 2014; 88: 13135-13148.
43. Thompson SR. So you want to know if your message has an IRES Wiley Interdiscip Rev RNA 2012; 3: 697-705.
44. Van Eden ME, Byrd MP, Sherrill KW, Lloyd RE. Demonstrating internal ribosome entry sites in eukaryotic mRNAs using stringent RNA test procedures. RNA 2004; 10: 720-730.
45. Holcik M, Graber T, Lewis SM, Lefebvre CA, Lacasse E, Baird S. Spurious splicing within the XIAP 5' UTR occurs in the Rluc/Fluc but not the betagal/CAT bicistronic reporter system. RNA 2005; 11: 1605-1609.
46. Rapley J, Oshiro N, Ortiz-Vega S, Avruch J. The mechanism of insulin-stimulated 4E-BP protein binding to mammalian target of rapamycin (mTOR) complex 1 and its contribution to mTOR complex 1 signaling. J Biol Chem 2011; 286: 38043-38053.
47. Mothe-Satney I, Yang D, Fadden P, Haystead TA, Lawrence JC Jr. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol Cell Biol 2000; 20: 3558-3567.
48. Pohlman TH, Harlan JM. Human endothelial cell response to lipopolysaccharide, interleukin-1, and tumor necrosis factor is regulated by protein synthesis. Cell Immunol 1989; 119: 41-52.
49. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 2006; 126: 321-334.
50. Saunders WB, Bayless KJ, Davis GE. MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci 2005; 118: 2325-2340.
51. Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV. Potential role of MCP-1 in endothelial cell tight junction 'opening': signaling via Rho and Rho kinase. J Cell Sci 2003; 116: 4615-4628.
52. Martin M, Kettmann R, Dequiedt F. Class IIa histone deacetylases: regulating the regulators. Oncogene 2007; 26: 5450-5467.
53. Burow ME, Weldon CB, Tang Y, Navar GL, Krajewski S, Reed JC et al. Differences in susceptibility to tumor necrosis factor alpha-induced apoptosis among MCF-7 breast cancer cell variants. Cancer Res 1998; 58: 4940-4946.
54. Munker R, Koeffler P. In vitro action of tumor necrosis factor on myeloid leukemia cells. Blood 1987; 69: 1102-1108.
55. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 1999; 19: 1871-1880.
56. Ueda T, Watanabe-Fukunaga R, Fukuyama H, Nagata S, Fukunaga R. Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol Cell Biol 2004; 24: 6539-6549.
57. Brown MC, Dobrikov MI, Gromeier M. MAPK-interacting kinase regulates mTOR/AKT signaling and controls SRPK-responsive type 1 IRES-mediated translation and viral oncolysis. J Virol 2014; 88: 13149-13160.
58. Knauf U, Tschopp C, Gram H. Negative regulation of protein translation by mitogen-activated protein kinase-interacting kinases 1 and 2. Mol Cell Biol 2001; 21: 5500-5511.
59. Culjkovic B, Topisirovic I, Skrabanek L, Ruiz-Gutierrez M, Borden KL. eIF4E is a central node of an RNA regulon that governs cellular proliferation. J Cell Biol 2006; 175: 415-426.
60. Cohen N, Sharma M, Kentsis A, Perez JM, Strudwick S, Borden KL. PML RING suppresses oncogenic transformation by reducing the affinity of eIF4E for mRNA. EMBO J 2001; 20: 4547-4559.
61. Buxade M, Parra JL, Rousseau S, Shpiro N, Marquez R, Morrice N et al. The Mnks are novel components in the control of TNF alpha biosynthesis and phosphorylate and regulate hnRNP A1. Immunity 2005; 23: 177-189.
62. Gingras AC, Raught B, Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 1999; 68: 913-963.
63. Scaglioni PP, Rabellino A, Yung TM, Bernardi R, Choi S, Konstantinidou G et al. Translationdependent mechanisms lead to PML upregulation and mediate oncogenic K-RAS-induced cellular senescence. EMBO Mol Med 2012; 4: 594-602.
64. Komar AA, Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 2011; 10: 229-240.
65. Baird SD, Turcotte M, Korneluk RG, Holcik M. Searching for IRES. RNA 2006; 12: 1755-1785.
66. Cheng X, Kao HY. Post-translational modifications of PML: consequences and implications. Front Oncol 2013; 2: 210.
67. Young RM, Wang SJ, Gordan JD, Ji X, Liebhaber SA, Simon MC. Hypoxia-mediated selective mRNA translation by an internal ribosome entry site-independent mechanism. J Biol Chem 2008; 283: 16309-16319.
68. Wheater MJ, Johnson PW, Blaydes JP. The role of MNK proteins and eIF4E phosphorylation in breast cancer cell proliferation and survival. Cancer Biol Ther 2010; 10: 728-735.
69. Lim S, Saw TY, Zhang M, Janes MR, Nacro K, Hill J et al. Targeting of the MNK-eIF4E axis in blast crisis chronic myeloid leukemia inhibits leukemia stem cell function. Proc Natl Acad Sci USA 2013; 110: E2298-E2307.
70. Ramalingam S, Gediya L, Kwegyir-Afful AK, Ramamurthy VP, Purushottamachar P, Mbatia H et al. First MNKs degrading agents block phosphorylation of eIF4E, induce apoptosis, inhibit cell growth, migration and invasion in triple negative and Her2-overexpressing breast cancer cell lines. Oncotarget 2014; 5: 530-543.
71. Joshi S, Kaur S, Redig AJ, Goldsborough K, David K, Ueda T et al. Type I interferon (IFN)-dependent activation of Mnk1 and its role in the generation of growth inhibitory responses. Proc Natl Acad Sci USA 2009; 106: 12097-12102.
72. Testa U, Grignani F, Samoggia P, Zanetti C, Riccioni R, Lo Coco F et al. The PML/RARalpha fusion protein inhibits tumor necrosis factor-alpha-induced apoptosis in U937 cells and acute promyelocytic leukemia blasts. J Clin Invest 1998; 101: 2278-2289.
73. Dolniak B, Katsoulidis E, Carayol N, Altman JK, Redig AJ, Tallman MS et al. Regulation of arsenic trioxide-induced cellular responses by Mnk1 and Mnk2. J Biol Chem 2008; 283: 12034-12042.
74. Sedger LM, McDermott MF. TNF and TNF-receptors: from mediators of cell death and inflammation to therapeutic giants-past, present and future. Cytokine Growth Factor Rev 2014; 25: 453-472.
75. Gerszten RE, Garcia-Zepeda EA, Lim YC, Yoshida M, Ding HA, Gimbrone Jr MA et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 1999; 398: 718-723.
76. Yang J, Park Y, Zhang H, Gao X,Wilson E, Zimmer W et al. Role of MCP-1 in tumor necrosis factor-alpha-induced endothelial dysfunction in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 2009; 297: H1208-H1216.
77. Basu A, Das P, Chaudhuri S, Bevilacqua E, Andrews J, Barik S et al. Requirement of rRNA methylation for 80S ribosome assembly on a cohort of cellular internal ribosome entry sites. Mol Cell Biol 2011; 31: 4482-4499.
78. Ray PS, Grover R, Das S. Two internal ribosome entry sites mediate the translation of p53 isoforms. EMBO Rep 2006; 7: 404-410.
79. Hsu KS, Kao HY. beta-Transducin repeat-containing protein 1 (beta-TrCP1)-mediated silencing mediator of retinoic acid and thyroid hormone receptor (SMRT) protein degradation promotes tumor necrosis factor alpha (TNFalpha)-induced inflammatory gene expression. J Biol Chem 2013; 288: 25375-25386.
80. Guan BJ, Krokowski D, Majumder M, Schmotzer CL, Kimball SR, Merrick WC et al. Translational control during endoplasmic reticulum stress beyond phosphorylation of the translation initiation factor eIF2alpha. J Biol Chem 2014; 289: 12593-12611.