N-terminal acetylome analysis reveals the specificity of Naa50 (Nat5) and suggests a kinetic competition between N-terminal acetyltransferases and methionine aminopeptidases

Proteomics

Volumn 15, Issue 14, 2015, Pages 2436-2446

  Van Damme, Petra ^a,b   Hole, Kristine ^c   Gevaert, Kris ^a,b   Arnesen, Thomas ^c,d  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF BERGEN   (Norway)

^d HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

Acetylation; Methionine aminopeptidase; N terminal acetyltransferase; N terminomics; Naa50; NAT; Nt acetylome

Indexed keywords

ALANINE; LEUCINE; LYSINE; METHIONINE; METHIONYL AMINOPEPTIDASE; METHIONYL AMINOPEPTIDASE 2; NAA50 PROTEIN; PEPTIDE ALPHA N ACETYLTRANSFERASE; PHENYLALANINE; PROTEOME; SERINE; THREONINE; THYRONINE; UNCLASSIFIED DRUG; VALINE;

ACETYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME KINETICS; ENZYME SPECIFICITY; FUNGAL STRAIN; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; WILD TYPE; YEAST CELL;

EID: 84930532645     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400575     Document Type: Article

References (51)

1. Pestana, A., Pitot, H. C., N-terminal acetylation of histone-like nascent peptides on rat-liver polyribosomes in vitro. Nature 1974, 247, 200–202.
2. Pestana, A., Pitot, H. C., Acetylation of nascent polypeptide-chains on rat-liver polyribosomes in vivo and in vitro. Biochemistry 1975, 14, 1404–1412.
3. Strous, G. J., Berns, A. J., Bloemendal, H., N-terminal acetylation of the nascent chains of alpha-crystallin. Biochem. Biophys. Res. Commun. 1974, 58, 876–884.
4. Strous, G. J., van Westreenen, H., Bloemendal, H., Synthesis of lens protein in vitro. N-terminal acetylation of alpha-crystallin. Eur. J. Biochem. 1973, 38, 79–85.
5. Arnesen, T., Van Damme, P., Polevoda, B., Helsens, K. et al., Proteomics analyses reveal the evolutionary conservation and divergence of N-terminal acetyltransferases from yeast and humans. Proc. Natl. Acad. Sci. USA 2009, 106, 8157–8162.
6. Brown, J. L., Roberts, W. K., Evidence that approximately eighty per cent of the soluble proteins from Ehrlich ascites cells are Nalpha-acetylated. J. Biol. Chem. 1976, 251, 1009–1014.
7. Van Damme, P., Hole, K., Pimenta-Marques, A., Helsens, K. 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.
8. Polevoda, B., Sherman, F., N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J. Mol. Biol. 2003, 325, 595–622.
9. Van Damme, P., Lasa, M., Polevoda, B., Gazquez, C. et al., N-terminal acetylome analyses and functional insights of the N-terminal acetyltransferase NatB. Proc. Nat. Acad. Sci. USA 2012, 109, 12449–12454.
10. Xiao, Q., Zhang, F., Nacev, B. A., Liu, J. O., Pei, D., Protein N-terminal processing: substrate specificity of Escherichia coli and human methionine aminopeptidases. Biochemistry 2010, 49, 5588–5599.
11. Arfin, S. M., Bradshaw, R. A., Cotranslational processing and protein turnover in eukaryotic cells. Biochemistry 1988, 27, 7979–7984.
12. Moerschell, R. P., Hosokawa, Y., Tsunasawa, S., Sherman, F., The specificities of yeast methionine aminopeptidase and acetylation of amino-terminal methionine in vivo. Processing of altered iso-1-cytochromes c created by oligonucleotide transformation. J. Biol. Chem. 1990, 265, 19638–19643.
13. Tsunasawa, S., Stewart, J. W., Sherman, F., Amino-terminal processing of mutant forms of yeast iso-1-cytochrome c. The specificities of methionine aminopeptidase and acetyltransferase. J. Biol. Chem. 1985, 260, 5382–5391.
14. Bonissone, S., Gupta, N., Romine, M., Bradshaw, R. A., Pevzner, P. A., N-terminal protein processing: a comparative proteogenomic analysis. Mol. Cell Proteomics 2013, 12, 14–28.
15. Kramer, G., Boehringer, D., Ban, N., Bukau, B., The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 2009, 16, 589–597.
16. Giglione, C., Boularot, A., Meinnel, T., Protein N-terminal methionine excision. Cell. Mol. Life Sci. 2004, 61, 1455–1474.
17. Arnesen, T., Anderson, D., Baldersheim, C., Lanotte, M. et al., Identification and characterization of the human ARD1-NATH protein acetyltransferase complex. Biochem. J. 2005, 386, 433–443.
18. Hole, K., Van Damme, P., Dalva, M., Aksnes, H. 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.
19. Starheim, K. K., Arnesen, T., Gromyko, D., Ryningen, A. 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.
20. Starheim, K. K., Gromyko, D., Evjenth, R., Ryningen, A. 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.
21. Bienvenut, W. V., Sumpton, D., Martinez, A., Lilla, S. et al., Comparative large scale characterization of plant versus mammal proteins reveals similar and idiosyncratic N-alpha-acetylation features. Mol. Cell Proteomics 2012, 11, M111 015131.
22. Aksnes, H., Van Damme, P., Goris, M., Starheim, Kristian K. et al., An organellar Nα-acetyltransferase, Naa60, acetylates cytosolic N termini of transmembrane proteins and maintains golgi integrity. Cell reports 2015, 10, 1362–1374.
23. Gautschi, M., Just, S., Mun, A., Ross, S. 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.
24. Mullen, J. R., Kayne, P. S., Moerschell, R. P., Tsunasawa, S. et al., Identification and characterization of genes and mutants for an N-terminal acetyltransferase from yeast. EMBO J. 1989, 8, 2067–2075.
25. Park, E. C., Szostak, J. W., ARD1 and NAT1 proteins form a complex that has N-terminal acetyltransferase activity. EMBO J. 1992, 11, 2087–2093.
26. Polevoda, B., Norbeck, J., Takakura, H., Blomberg, A., Sherman, F., Identification and specificities of N-terminal acetyltransferases from Saccharomyces cerevisiae. EMBO J. 1999, 18, 6155–6168.
27. Arnesen, T., Anderson, D., Torsvik, J., Halseth, H. B. 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.
28. Williams, B. C., Garrett-Engele, C. M., Li, Z., Williams, E. V. et al., Two putative acetyltransferases, san and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr. Biol. 2003, 13, 2025–2036.
29. Hou, F., Chu, C. W., Kong, X., Yokomori, K., Zou, H., The acetyltransferase activity of San stabilizes the mitotic cohesin at the centromeres in a shugoshin-independent manner. J. Cell Biol. 2007, 177, 587–597.
30. Pimenta-Marques, A., Tostoes, R., Marty, T., Barbosa, V. et al., Differential requirements of a mitotic acetyltransferase in somatic and germ line cells. Dev. Biol. 2008, 323, 197–206.
31. Evjenth, R., Hole, K., Karlsen, O. A., Ziegler, M. et al., Human Naa50p (Nat5/San) displays both protein N alpha- and N epsilon-acetyltransferase activity. J. Biol. Chem. 2009, 284, 31122–31129.
32. Van Damme, P., Evjenth, R., Foyn, H., Demeyer, K. et al., Proteome-derived peptide libraries allow detailed analysis of the substrate specificities of N(alpha)-acetyltransferases and point to hNaa10p as the post-translational actin N(alpha)-acetyltransferase. Mol. Cell. Proteomics 2011, 10, M110 004580.
33. Solbiati, J., Chapman-Smith, A., Miller, J. L., Miller, C. G., Cronan, J. E., Jr., Processing of the N termini of nascent polypeptide chains requires deformylation prior to methionine removal. J. Mol. Biol. 1999, 290, 607–614.
34. Miller, C. A., 3rd, Martinat, M. A., Hyman, L. E., Assessment of aryl hydrocarbon receptor complex interactions using pBEVY plasmids: expressionvectors with bi-directional promoters for use in Saccharomyces cerevisiae. Nucleic Acids Res. 1998, 26, 3577–3583.
35. Staes, A., Impens, F., Van Damme, P., Ruttens, B. et al., Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat. Protocols 2011, 6, 1130–1141.
36. Van Damme, P., Arnesen, T., Ruttens, B., Gevaert, K., In-gel N-acetylation for the quantification of the degree of protein in vivo N-terminal acetylation. Methods Mol. Biol. 2013, 981, 115–126.
37. Staes, A., Van Damme, P., Helsens, K., Demol, H. et al., Improved recovery of proteome-informative, protein N-terminal peptides by combined fractional diagonal chromatography (COFRADIC). Proteomics 2008, 8, 1362–1370.
38. Van Damme, P., Van Damme, J., Demol, H., Staes, A. et al., A review of COFRADIC techniques targeting protein N-terminal acetylation. BMC Proc. 2009, 3(Suppl 6), S6.
39. Koch, A., Gawron, D., Steyaert, S., Ndah, E. et al., A proteogenomics approach integrating proteomics and ribosome profiling increases the efficiency of protein identification and enables the discovery of alternative translation start sites. Proteomics 2014, 14, 2688–2698.
40. Martens, L., Vandekerckhove, J., Gevaert, K., DBToolkit: processing protein databases for peptide-centric proteomics. Bioinformatics 2005, 21, 3584–3585.
41. Helsens, K., Colaert, N., Barsnes, H., Muth, T. et al., ms_lims, a simple yet powerful open source laboratory information management system for MS-driven proteomics. Proteomics 2010, 10, 1261–1264.
42. Vizcaino, J. A., Deutsch, E. W., Wang, R., Csordas, A. et al., ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 2014, 32, 223–226.
43. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A. et al., The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2013, 41, D1063–D1069.
44. Evjenth, R., Hole, K., Ziegler, M., Lillehaug, J. R., Application of reverse-phase HPLC to quantify oligopeptide acetylation eliminates interference from unspecific acetyl CoA hydrolysis. BMC Proc. 2009, 3(Suppl 6), S5.
45. Van Damme, P., Stove, S. I., Glomnes, N., Gevaert, K., Arnesen, T., A Saccharomyces cerevisiae model reveals in vivo functional impairment of the Ogden syndrome N-terminal acetyltransferase Naa10S37P mutant. Mol. Cell Proteomics 2014, 13, 2031–2041.
46. Van Damme, P., Evjenth, R., Foyn, H., Demeyer, K. et al., Proteome-derived peptide libraries allow detailed analysis of the substrate specificities of N{alpha}-acetyltransferases and point to hNaa10p as the post-translational actin N{alpha}-acetyltransferase. Mol. Cell Proteomics 2011, 10, M110 004580.
47. Frottin, F., Martinez, A., Peynot, P., Mitra, S. et al., The proteomics of N-terminal methionine cleavage. Mol. Cell Proteomics 2006, 5, 2336–2349.
48. Raue, U., Oellerer, S., Rospert, S., Association of protein biogenesis factors at the yeast ribosomal tunnel exit is affected by the translational status and nascent polypeptide sequence. J. Biol. Chem. 2007, 282, 7809–7816.
49. Shemorry, A., Hwang, C. S., Varshavsky, A., Control of protein quality and stoichiometries by N-terminal acetylation and the N-end rule pathway. Mol. Cell 2013, 50, 540–551.
50. Hwang, C. S., Shemorry, A., Varshavsky, A., N-terminal acetylation of cellular proteins creates specific degradation signals. Science 2010, 327, 973–977.
51. Sriram, S. M., Kim, B. Y., Kwon, Y. T., The N-end rule pathway: emerging functions and molecular principles of substrate recognition. Nat. Rev. Mol. Cell Biol. 2011, 12, 735–747.