Protein N-terminal acetyltransferases: When the start matters

Trends in Biochemical Sciences

Volumn 37, Issue 4, 2012, Pages 152-161

  Starheim, Kristian K ^a   Gevaert, Kris ^b,c   Arnesen, Thomas ^a,d  

^a UNIVERSITY OF BERGEN   (Norway)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

Acetyl coenzyme A; Endoplasmic reticulum translocation; N terminal acetylation; NAA; Nt proteomics; Ogden syndrome; Protein degradation; Protein N terminal acetyltransferase

Indexed keywords

ACETYL COENZYME A; ACYLTRANSFERASE; AMINO TERMINAL ACETYLTRANSFERASE; DNA METHYLTRANSFERASE 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; TUBERIN; UNCLASSIFIED DRUG;

ACETYLATION; BIOCHEMISTRY; BREAST CANCER; CARCINOGENESIS; CELL DEATH; CELL METABOLISM; CHILD DEATH; COLORECTAL CANCER; COMPLEX FORMATION; DEVELOPMENTAL DISORDER; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME REGULATION; ENZYME STRUCTURE; GENE MUTATION; GENETIC DISORDER; HUMAN; LUNG CANCER; LYMPH NODE METASTASIS; NONHUMAN; OGDEN SYNDROME; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION;

ACETYLATION; ACETYLTRANSFERASES; ANIMALS; HUMANS; MODELS, BIOLOGICAL; PROTEINS;

EUKARYOTA;

EID: 84859490749     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2012.02.003     Document Type: Review

References (68)

1. Arnesen T., et al. Proteomics analyses reveal the evolutionary conservation and divergence of N-terminal acetyltransferases from yeast and humans. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8157-8162.
2. Goetze S., et al. Identification and functional characterization of N-terminally acetylated proteins in Drosophila melanogaster. PLoS Biol. 2009, 7:e1000236.
3. Liszczak G., et al. Structure of a ternary Naa50p (NAT5/SAN) N-terminal acetyltransferase complex reveals the molecular basis for substrate-specific acetylation. J. Biol. Chem. 2011, 286:37002-37010.
4. Hwang C.S., et al. N-terminal acetylation of cellular proteins creates specific degradation signals. Science 2010, 327:973-977.
5. Forte G.M., et al. N-terminal acetylation inhibits protein targeting to the endoplasmic reticulum. PLoS Biol. 2011, 9:e1001073.
6. Scott D.C., et al. N-terminal acetylation acts as an avidity enhancer within an interconnected multiprotein complex. Science 2011, 334:674-678.
7. Hofmann I., Munro S. An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility. J. Cell Sci. 2006, 119:1494-1503.
8. Cai L., et al. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 2011, 42:426-437.
9. Yi C.H., et al. Metabolic regulation of protein N-alpha-acetylation by Bcl-xL promotes cell survival. Cell 2011, 146:607-620.
10. Helbig A.O., et al. Profiling of N-acetylated protein termini provides in-depth insights into the N-terminal nature of the proteome. Mol. Cell. Proteomics 2010, 9:928-939.
11. Helsens K., et al. Bioinformatics analysis of a Saccharomyces cerevisiae N-terminal proteome provides evidence of alternative translation initiation and post-translational N-terminal acetylation. J. Proteome Res. 2011, 10:3578-3589.
12. Seo J.H., et al. Arrest defective 1 autoacetylation is a critical step in its ability to stimulate cancer cell proliferation. Cancer Res. 2010, 70:4422-4432.
13. Kuo H.-P., et al. ARD1 stabilization of TSC2 suppresses tumorigenesis through the mTOR signaling pathway. Sci. Signal. 2010, 3:ra9.
14. Hua K.-T., et al. N-α-acetyltransferase 10 protein suppresses cancer cell metastasis by binding PIX proteins and inhibiting Cdc42/Rac1 activity. Cancer Cell 2011, 19:218-231.
15. Lee C.-F., et al. hNaa10p contributes to tumorigenesis by facilitating DNMT1-mediated tumor suppressor gene silencing. J. Clin. Investig. 2010, 120:2920-2930.
16. Rope A.F., et al. Using VAAST to identify an X-linked disorder resulting in lethality in male infants due to N-terminal acetyltransferase deficiency. Am. J. Hum. Genet. 2011, 89:28-43.
17. Gordiyenko Y., et al. Acetylation of L12 increases interactions in the Escherichia coli ribosomal stalk complex. J. Mol. Biol. 2008, 380:404-414.
18. Charbaut E., et al. N-terminal acetylation of ectopic recombinant proteins in Escherichia coli. FEBS Lett. 2002, 529:341-345.
19. Vetting M.W., et al. A novel dimeric structure of the RimL Nalpha-acetyltransferase from Salmonella typhimurium. J. Biol. Chem. 2005, 280:22108-22114.
20. Polevoda B., Sherman F. N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J. Mol. Biol. 2003, 325:595-622.
21. Falb M., et al. Archaeal N-terminal protein maturation commonly involves N-terminal acetylation: a large-scale proteomics survey results. J. Mol. Biol. 2006, 362:915-924.
22. Mackay D.T., et al. An acetylase with relaxed specificity catalyses protein N-terminal acetylation in Sulfolobus solfataricus. Mol. Microbiol. 2007, 64:1540-1548.
23. Van Damme P., et al. NatF contributes to an evolutionary shift in protein N-terminal acetylation and is important for normal chromosome segregation. PLoS Genet. 2011, 7:e1002169.
24. Martinez A., et al. Extent of N-terminal modifications in cytosolic proteins from eukaryotes. Proteins 2008, 8:2809-2831.
25. Bienvenut W.V., et al. Comparative large-scale characterisation of plant vs. mammal proteins reveals similar and idiosyncratic N-alpha acetylation features. Mol. Cell. Proteomics 2012, 10.1074/mcp.M111.015131.
26. Starheim K.K., et al. Identification of the human N(alpha)-acetyltransferase complex B (hNatB): a complex important for cell-cycle progression. Biochem. J. 2008, 415:325-331.
27. Starheim K.K., et al. Knockdown of human N alpha-terminal acetyltransferase complex C leads to p53-dependent apoptosis and aberrant human Arl8b localization. Mol. Cell. Biol. 2009, 29:3569-3581.
28. Evjenth R., et al. Human Naa50p (Nat5/San) displays both protein N alpha- and N epsilon-acetyltransferase activity. J. Biol. Chem. 2009, 284:31122-31129.
29. Hole K., et al. The human N-alpha-acetyltransferase 40 (hNaa40p/hNatD) is conserved from yeast and N-terminally acetylates histones H2A and H4. PLoS ONE 2011, 6:e24713.
30. Mullen J.R., et al. Identification and characterization of genes and mutants for an N-terminal acetyltransferase from yeast. EMBO J. 1989, 8:2067-2075.
31. Polevoda B., et al. Identification and specificities of N-terminal acetyltransferases from Saccharomyces cerevisiae. EMBO J. 1999, 18:6155-6168.
32. Polevoda B., Sherman F. Composition and function of the eukaryotic N-terminal acetyltransferase subunits. Biochem. Biophy. Res. Commun. 2003, 308:1-11.
33. Gromyko D., et al. Depletion of the human Nα-terminal acetyltransferase A induces p53-dependent apoptosis and p53-independent growth inhibition. Int. J. Cancer 2010, 127:2777-2789.
34. Arnesen T., et al. Identification and characterization of the human ARD1-NATH protein acetyltransferase complex. Biochem. J. 2005, 386:433-443.
35. Gautschi M., et al. The yeast N(alpha)-acetyltransferase NatA is quantitatively anchored to the ribosome and interacts with nascent polypeptides. Mol. Cell. Biol. 2003, 23:7403-7414.
36. Van Damme P., et al. Proteome-derived peptide libraries allow detailed analysis of the substrate specificities of N{alpha}-acetyltransferases and point to hNaa10p as the posttranslational actin N{alpha}-acetyltransferase. Mol. Cell. Proteomics 2011, 10.1074/mcp.M110.004580.
37. Starheim K.K., et al. Composition and biological significance of the human Nalpha-terminal acetyltransferases. BMC Proc. 2009, 3(Suppl 6):S3.
38. Chun K.-H., et al. Differential regulation of splicing, localization and stability of mammalian ARD1235 and ARD1225 isoforms. Biochem. Biophys. Res. Commun. 2007, 353:18-25.
39. Arnesen T., et al. The chaperone-like protein HYPK acts together with NatA in cotranslational N-terminal acetylation and prevention of Huntingtin aggregation. Mol. Cell. Biol. 2010, 30:1898-1909.
40. Lim J.-h. Hypoxia-inducible factor-1A obstructs a Wnt signaling pathway by inhibiting the hARD1-mediated activation of B-catenin. Cancer Res. 2008, 13:5177-5184.
41. Ametzazurra A., et al. Implication of human N-alpha-acetyltransferase 5 in cellular proliferation and carcinogenesis. Oncogene 2008, 27:7296-7306.
42. Polevoda B., et al. Nat3p and Mdm20p are required for function of yeast NatB N-alpha-terminal acetyltransferase and of actin and tropomyosin. J. Biol. Chem. 2003, 278:30686-30697.
43. Polevoda B., Sherman F. NatC Nalpha-terminal acetyltransferase of yeast contains three subunits, Mak3p, Mak10p, and Mak31p. J. Biol. Chem. 2001, 276:20154-20159.
44. Tercero J.C., Wickner R.B. MAK3 encodes an N-acetyltransferase whose modification of the L-A gag NH2 terminus is necessary for virus particle assembly. J. Biol. Chem. 1992, 267:20277-20281.
45. Song O.-k, et al. An Nalpha-acetyltransferase responsible for acetylation of the N-terminal residues of histones H4 and H2A. J. Biol. Chem. 2003, 278:38109-38112.
46. Polevoda B., et al. Properties of Nat4, an N(alpha)-acetyltransferase of Saccharomyces cerevisiae that modifies N termini of histones H2A and H4. Mol. Cell. Biol. 2009, 29:2913-2924.
47. Arnesen T., et al. Cloning and characterization of hNAT5/hSAN: an evolutionarily conserved component of the NatA protein N-alpha-acetyltransferase complex. Gene 2006, 371:291-295.
48. Williams B.C., et al. Two putative acetyltransferases, san and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr. Biol. 2003, 13:2025-2036.
49. Hou F., et al. The acetyltransferase activity of San stabilizes the mitotic cohesin at the centromeres in a shugoshin-independent manner. J. Cell Biol. 2007, 177:587-597.
50. Pimenta-Marques A., et al. Differential requirements of a mitotic acetyltransferase in somatic and germ line cells. Dev. Biol. 2008, 323:197-206.
51. Chu C.-W., et al. A novel acetylation of β-tubulin by san modulates microtubule polymerization via down-regulating tubulin incorporation. Mol. Biol. Cell 2011, 22:448-456.
52. Narita K. Isolation of acetylpeptide from enzymic digests of TMV-protein. Biochim. Biophy. Acta 1958, 28:184-191.
53. Varshavsky A. The N-end rule pathway and regulation by proteolysis. Protein Sci. 2011, 20:1298-1345.
54. Jörnvall H. Acetylation of protein N-terminal amino groups structural observations on alpha-amino acetylated proteins. J. Theor. Biol. 1975, 55:1-12.
55. Ciechanover A., Ben-Saadon R. N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol. 2004, 14:103-106.
56. Helbig A.O., et al. Perturbation of the yeast N-acetyltransferase NatB induces elevation of protein phosphorylation levels perturbation of the yeast N-acetyltransferase NatB induces elevation of protein phosphorylation levels. BMC Genomics 2010, 11:685.
57. Behnia R., et al. Targeting of the Arf-like GTPase Arl3p to the Golgi requires N-terminal acetylation and the membrane protein Sys1p. Nat. Cell Biol. 2004, 6:405-413.
58. Behnia R., et al. The yeast orthologue of GRASP65 forms a complex with a coiled-coil protein that contributes to ER to Golgi traffic. J. Cell Biol. 2007, 176:255-261.
59. Murthi A., Hopper A.K. Genome-wide screen for inner nuclear membrane protein targeting in Saccharomyces cerevisiae: roles for N-acetylation and an integral membrane protein. Genetics 2005, 170:1553-1560.
60. Caesar R., Blomberg A. The stress-induced Tfs1p requires NatB-mediated acetylation to inhibit carboxypeptidase Y and to regulate the protein kinase A pathway. J. Biol. Chem. 2004, 279:38532-38543.
61. Lim J.-h, et al. Human arrest defective 1 acetylates and activates beta-catenin, promoting lung cancer cell proliferation. Cancer Res. 2006, 66:10677-10682.
62. Shin D.H., et al. Arrest defective-1 controls tumor cell behavior by acetylating myosin light chain kinase. PloS ONE 2009, 4:e7451.
63. Målen H., et al. The protein Nalpha-terminal acetyltransferase hNaa10p (hArd1) is phosphorylated in HEK293 cells. BMC research notes 2009, 2:32.
64. Pang A.L.Y., et al. Expression of human NAA11 (ARD1B) gene is tissue-specific and is regulated by DNA methylation. Epigenetics 2011, 10.4161/epi.6.11.18125.
65. Friis R.M.N., et al. A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Res. 2009, 37:3969-3980.
66. Wellen K., et al. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009, 324:1076-1080.
67. Ren T., et al. Generation of novel monoclonal antibodies and their application for detecting ARD1 expression in colorectal cancer. Cancer Lett. 2008, 264:83-92.
68. Yu M., et al. Immunohistochemical analysis of human arrest-defective-1 expressed in cancers in vivo. Oncol. Rep. 2009, 21:909-915.