Depletion of histone N-terminal-acetyltransferase Naa40 induces p53-independent apoptosis in colorectal cancer cells via the mitochondrial pathway

Apoptosis

Volumn 21, Issue 3, 2016, Pages 298-311

  Pavlou, Demetria ^a   Kirmizis, Antonis ^a  

^a UNIVERSITY OF CYPRUS   (Cyprus)

Author keywords

Apoptosis; Colorectal cancer; Epigenetics; Histone N terminal acetylation; Naa40; NatD

Indexed keywords

ACYLTRANSFERASE; CASPASE 9; HISTONE; HISTONE N TERMINAL ACETYLTRANSFERASE NAA40; PROTEIN P53; UNCLASSIFIED DRUG; CASP9 PROTEIN, HUMAN; CASPASE INHIBITOR; NAA40 PROTEIN, HUMAN; PEPTIDE ALPHA N ACETYLTRANSFERASE D; SMALL INTERFERING RNA; TP53 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL ACTIVATION; CELL VIABILITY; COLORECTAL CANCER; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN PROCESSING; ACETYLATION; ANIMAL; CARCINOGENESIS; CELL SURVIVAL; COLORECTAL TUMOR; GENE SILENCING; GENETICS; HCT 116 CELL LINE; HT-29 CELL LINE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACETYLATION; ANIMALS; APOPTOSIS; CARCINOGENESIS; CASPASE 9; CASPASE INHIBITORS; CELL SURVIVAL; COLORECTAL NEOPLASMS; GENE KNOCKDOWN TECHNIQUES; HCT116 CELLS; HISTONES; HT29 CELLS; HUMANS; MICE; MITOCHONDRIA; N-TERMINAL ACETYLTRANSFERASE D; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84957439440     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-015-1207-0     Document Type: Article

References (66)

1. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693-705
2. Seo J, Lee KJ (2004) Post-translational modifications and their biological functions: proteomic analysis and systematic approaches. J Biochem Mol Biol 37:35-44
3. Arnesen T, Van Damme P, Polevoda B, Helsens K, Evjenth R, Colaert N et al (2009) Proteomics analyses reveal the evolutionary conservation and divergence of N-terminal acetyltransferases from yeast and humans. Proc Natl Acad Sci USA 106:8157-8162
4. Brown JL, Roberts WK (1976) Evidence that approximately eighty per cent of the soluble proteins from Ehrlich ascites cells are Nalpha-acetylated. J Biol Chem 251:1009-1014
5. Hershko A, Heller H, Eytan E, Kaklij G, Rose IA (1984) Role of the alpha-amino group of protein in ubiquitin-mediated protein breakdown. Proc Natl Acad Sci USA 81:7021-7025
6. Jornvall H (1975) Acetylation of protein N-terminal amino groups structural observations on alpha-amino acetylated proteins. J Theor Biol 55:1-12
7. Hwang CS, Shemorry A, Varshavsky A (2010) N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327:973-977
8. Park SE, Kim JM, Seok OH, Cho H, Wadas B, Kim SY et al (2015) Control of mammalian G protein signaling by N-terminal acetylation and the N-end rule pathway. Science 347:1249-1252
9. Arnesen T (2011) Towards a functional understanding of protein N-terminal acetylation. PLoS Biol 9:e1001074
10. Forte GM, Pool MR, Stirling CJ (2011) N-terminal acetylation inhibits protein targeting to the endoplasmic reticulum. PLoS Biol 9:e1001073
11. Hollebeke J, Van Damme P, Gevaert K (2012) N-terminal acetylation and other functions of Nalpha-acetyltransferases. Biol Chem 393:291-298
12. Silva RD, Martinho RG (2015) Developmental roles of protein N-terminal acetylation. Proteomics 15:2402-2409
13. Tooley JG, Schaner Tooley CE (2014) New roles for old modifications: emerging roles of N-terminal post-translational modifications in development and disease. Protein Sci 23:1641-1649
14. Ree R, Myklebust LM, Thiel P, Foyn H, Fladmark KE, Arnesen T (2015) The N-terminal acetyltransferase Naa10 is essential for zebrafish development. Biosci Rep 35:e00249. doi: 10.1042/BSR20150168
15. Polevoda B, Brown S, Cardillo TS, Rigby S, Sherman F (2008) Yeast N(alpha)-terminal acetyltransferases are associated with ribosomes. J Cell Biochem 103:492-508
16. Polevoda B, Arnesen T, Sherman F (2009) A synopsis of eukaryotic Nalpha-terminal acetyltransferases: nomenclature, subunits and substrates. BMC Proc 3(Suppl 6):S2
17. Aksnes H, Van Damme P, Goris M, Starheim KK, Marie M, Stove SI et al (2015) An organellar nalpha-acetyltransferase, naa60, acetylates cytosolic N termini of transmembrane proteins and maintains Golgi integrity. Cell Rep 10:1362-1374
18. Kalvik TV, Arnesen T (2013) Protein N-terminal acetyltransferases in cancer. Oncogene 32:269-276
19. Aksnes H, Hole K, Arnesen T (2015) Molecular, cellular, and physiological significance of N-terminal acetylation. Int Rev Cell Mol Biol 316:267-305
20. Yu M, Ma M, Huang C, Yang H, Lai J, Yan S et al (2009) Correlation of expression of human arrest-defective-1 (hARD1) protein with breast cancer. Cancer Invest 27:978-983
21. Lee CF, Ou DSC, Lee SB, Chang LH, Lin RK, Li YS et al (2010) hNaa10p contributes to tumorigenesis by facilitating DNMT1-mediated tumor suppressor gene silencing. J Clin Invest 120:2920-2930
22. Ren T, Jiang B, Jin G, Li J, Dong B, Zhang J et al (2008) Generation of novel monoclonal antibodies and their application for detecting ARD1 expression in colorectal cancer. Cancer Lett 264:83-92
23. Hua KT, Tan CT, Johansson G, Lee JM, Yang PW, Lu HY et al (2011) N-Alpha-acetyltransferase 10 protein suppresses cancer cell metastasis by binding PIX proteins and inhibiting Cdc42/Rac1 activity. Cancer Cell 19:218-231
24. Ametzazurra A, Larrea E, Civeira MP, Prieto J, Aldabe R (2008) Implication of human N-alpha-acetyltransferase 5 in cellular proliferation and carcinogenesis. Oncogene 27:7296-7306
25. Starheim KK, Arnesen T, Gromyko D, Ryningen A, Varhaug JE, Lillehaug JR (2008) Identification of the human N(alpha)-acetyltransferase complex B (hNatB): a complex important for cell-cycle progression. Biochem J 415:325-331
26. Starheim KK, Gromyko D, Evjenth R, Ryningen A, Varhaug JE, Lillehaug JR et al (2009) Knockdown of human N alpha-terminal acetyltransferase complex C leads to p53-dependent apoptosis and aberrant human Arl8b localization. Mol Cell Biol 29:3569-3581
27. Starheim KK, Gevaert K, Arnesen T (2012) Protein N-terminal acetyltransferases: when the start matters. Trends Biochem Sci 37:152-161
28. Song OK, Wang X, Waterborg JH, Sternglanz R (2003) An Nalpha-acetyltransferase responsible for acetylation of the N-terminal residues of histones H4 and H2A. J Biol Chem 278:38109-38112
29. Polevoda B, Hoskins J, Sherman F (2009) Properties of Nat4, an N(alpha)-acetyltransferase of Saccharomyces cerevisiae that modifies N termini of histones H2A and H4. Mol Cell Biol 29:2913-2924
30. Magin RS, Liszczak GP, Marmorstein R (2015) The molecular basis for histone H4- and H2A-specific amino-terminal acetylation by NatD. Structure 23:332-341
31. Van Damme P, Stove SI, Glomnes N, Gevaert K, Arnesen T (2014) A Saccharomyces cerevisiae model reveals in vivo functional impairment of the Ogden syndrome N-terminal acetyltransferase NAA10 Ser37Pro mutant. Mol Cell Proteomics 13:2031-2041
32. Hole K, Van Damme P, Dalva M, Aksnes H, Glomnes N, Varhaug JE et al (2011) The human N-alpha-acetyltransferase 40 (hNaa40p/hNatD) is conserved from yeast and N-terminally acetylates histones H2A and H4. PLoS ONE 6:e24713
33. Schiza V, Molina-Serrano D, Kyriakou D, Hadjiantoniou A, Kirmizis A (2013) N-alpha-terminal acetylation of histone H4 regulates arginine methylation and ribosomal DNA silencing. PLoS Genet 9:e1003805
34. Riesen M, Morgan A (2009) Calorie restriction reduces rDNA recombination independently of rDNA silencing. Aging Cell 8:624-632
35. Smith DL Jr, Li C, Matecic M, Maqani N, Bryk M, Smith JS (2009) Calorie restriction effects on silencing and recombination at the yeast rDNA. Aging Cell 8:633-642
36. Liu Y, Zhou D, Zhang F, Tu Y, Xia Y, Wang H et al (2012) Liver Patt1 deficiency protects male mice from age-associated but not high-fat diet-induced hepatic steatosis. J Lipid Res 53:358-367
37. The Human Atlas. http://www.proteinatlas.org/ENSG00000110583-NAA40/cancer. Accessed 5 Nov 2015
38. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646-674
39. Norbury CJ, Hickson ID (2001) Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 41:367-401
40. Parrish AB, Freel CD, Kornbluth S (2013) Cellular mechanisms controlling caspase activation and function. Cold Spring Harb Perspect Biol 5:a008672. doi: 10.1101/cshperspect.a008672
41. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281(5381):1305-1308
42. McIlwain DR, Berger T, Mak TW (2013) Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 5:a008656
43. Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619
44. Brentnall M, Rodriguez-Menocal L, De Guevara RL, Cepero E, Boise LH (2013) Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol 14:32
45. Lopez J, Tait SW (2015) Mitochondrial apoptosis: killing cancer using the enemy within. Br J Cancer 112:957-962
46. Koff JL, Ramachandiran S, Bernal-Mizrachi L (2015) A time to kill: targeting apoptosis in cancer. Int J Mol Sci 16:2942-2955
47. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP et al (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282:1497-1501
48. Harasawa R, Mizusawa H, Nozawa K, Nakagawa T, Asada K, Kato I (1993) Detection and tentative identification of dominant mycoplasma species in cell cultures by restriction analysis of the 16S-23S rRNA intergenic spacer regions. Res Microbiol 144:489-943
49. Liu Z, Liu Y, Wang H, Ge X, Jin Q, Ding G et al (2009) Patt1, a novel protein acetyltransferase that is highly expressed in liver and downregulated in hepatocellular carcinoma, enhances apoptosis of hepatoma cells. Int J Biochem Cell Biol 41:2528-2537
50. Wu D, Chen X, Guo D, Hong Q, Fu B, Ding R et al (2005) Knockdown of fibronectin induces mitochondria-dependent apoptosis in rat mesangial cells. J Am Soc Nephrol 16:646-657
51. Fornaro M, Plescia J, Chheang S, Tallini G, Zhu YM, King M et al (2003) Fibronectin protects prostate cancer cells from tumor necrosis factor-alpha-induced apoptosis via the AKT/survivin pathway. J Biol Chem 278:50402-50411
52. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495-516
53. Sabbagh L, Kaech SM, Bourbonniere M, Woo M, Cohen LY, Haddad EK et al (2004) The selective increase in caspase-3 expression in effector but not memory T cells allows susceptibility to apoptosis. J Immunol 173:5425-5433
54. Droin N, Dubrez L, Eymin B, Renvoize C, Breard J, Dimanche-Boitrel MT et al (1998) Upregulation of CASP genes in human tumor cells undergoing etoposide-induced apoptosis. Oncogene 16:2885-2894
55. Druškovič M, Šuput D, Milisav I (2006) Overexpression of caspase-9 triggers its activation and apoptosis in vitro. Croat Med J 47:832-840
56. Ethier C, Labelle Y, Poirier GG (2007) PARP-1-induced cell death through inhibition of the MEK/ERK pathway in MNNG-treated HeLa cells. Apoptosis 12:2037-2049
57. Sousa FG, Matuo R, Soares DG, Escargueil AE, Henriques JA, Larsen AK et al (2012) PARPs and the DNA damage response. Carcinogenesis 33:1433-1440
58. Liu Y, Bodmer WF (2006) Analysis of P53 mutations and their expression in 56 colorectal cancer cell lines. Proc Natl Acad Sci USA 103:976-981
59. He X, Liao J, Liu F, Yan J, Yan J, Shang H et al (2015) Functional repair of p53 mutation in colorectal cancer cells using trans-splicing. Oncotarget 6:2034-2045
60. Drygin D, Lin A, Bliesath J, Ho CB, O'Brien SE, Proffitt C et al (2011) Targeting RNA polymerase I with an oral small molecule CX-5461 inhibits ribosomal RNA synthesis and solid tumor growth. Cancer Res 71:1418-1430
61. Gromyko D, Arnesen T, Ryningen A, Varhaug JE, Lillehaug JR (2010) Depletion of the human Nalpha-terminal acetyltransferase A induces p53-dependent apoptosis and p53-independent growth inhibition. Int J Cancer 127:2777-2789
62. Arnesen T, Gromyko D, Pendino F, Ryningen A, Varhaug JE, Lillehaug JR (2006) Induction of apoptosis in human cells by RNAi-mediated knockdown of hARD1 and NATH, components of the protein N-alpha-acetyltransferase complex. Oncogene 25:4350-4360
63. Polevoda B, Norbeck J, Takakura H, Blomberg A, Sherman F (1999) Identification and specificities of N-terminal acetyltransferases from Saccharomyces cerevisiae. EMBO J 18:6155-6168
64. Tweedie-Cullen RY, Brunner AM, Grossmann J, Mohanna S, Sichau D, Nanni P et al (2012) Identification of combinatorial patterns of post-translational modifications on individual histones in the mouse brain. PLoS ONE 7:e36980
65. Foyn H, Jones JE, Lewallen D, Narawane R, Varhaug JE, Thompson PR et al (2013) Design, synthesis, and kinetic characterization of protein N-terminal acetyltransferase inhibitors. ACS Chem Biol 8:1121-1127
66. Sarosiek KA, Ni Chonghaile T, Letai A (2013) Mitochondria: gatekeepers of response to chemotherapy. Trends Cell Biol 23:612-619