Developmental roles of protein N-terminal acetylation

Proteomics

Volumn 15, Issue 14, 2015, Pages 2402-2409

  Silva, Rui D ^a   Martinho, Rui G ^a,b  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Cell biology; Development; Drosophila; N terminal acetylation; Naa10 Ard1; Naa50 San

Indexed keywords

PEPTIDE ALPHA N ACETYLTRANSFERASE;

AMINO TERMINAL SEQUENCE; DEVELOPMENT; ENZYME MECHANISM; HYPOTHESIS; METABOLIC REGULATION; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN MODIFICATION; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION REGULATION;

EID: 85006355201     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400631     Document Type: Review

References (76)

1. Brown, J. L., Roberts, W. K., Evidence that approximately eighty per evidence that approximately eighty per cent of the soluble proteins from ehrlich ascites cells are nalpha-acetylated. J. Biol. Chem. 1976, 251, 1009–1976.
2. 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. U S A 2009, 106, 8157–8162.
3. 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-α-acetylation features. Mol. Cell. Proteomics 2012, 11, M111.015131.
4. Goetze, S., Qeli, E., Mosimann, C., Staes, a. et al., Identification and functional characterization of N-terminally acetylated proteins in Drosophila melanogaster. PLoS Biol 2009, 7, e1000236.
5. 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.
6. Gautschi, M., Mun, A., Ross, S., Ru, P. 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.
7. Polevoda, B., Brown, S., Cardillo, T. S., Rigby, S., Sherman, F., Yeast N(alpha)-terminal acetyltransferases are associated with ribosomes. J. Cell. Biochem. 2008, 103, 492–508.
8. Polevoda, B., Arnesen, T., Sherman, F., A synopsis of eukaryotic Nalpha-terminal acetyltransferases: nomenclature, subunits and substrates. BMC Proc. 2009, 3, S2.
9. Starheim, K. K., Gevaert, K., Arnesen, T., Protein N-terminal acetyltransferases: when the start matters. Trends Biochem. Sci. 2012, 37, 152–161.
10. Ametzazurra, a, Larrea, E., Civeira, M. P., Prieto, J., Aldabe, R., Implication of human N-alpha-acetyltransferase 5 in cellular proliferation and carcinogenesis. Oncogene 2008, 27, 7296–7306.
11. 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.
12. Mullen, J. R., Kaynel, 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.
13. 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.
14. Polevoda, B., Sherman, F., NatC Nalpha-terminal acetyltransferase of yeast contains three subunits, Mak3p, Mak10p, and Mak31p. J. Biol. Chem. 2001, 276, 20154–20159.
15. Song, O., Wang, X., Waterborg, J. H., Sternglanz, R., An Nalpha-acetyltransferase responsible for acetylation of the N-terminal residues of histones H4 and H2A. J. Biol. Chem. 2003, 278, 38109–38112.
16. 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.
17. 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. Natl. Acad. Sci. U S A 2012, 109, 12449–12454.
18. Ben-bassat, A., Bauer, K., Chang, S.-Y., Myambo, K. et al., Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure. J. Bacteriol. 1987, 169, 751–757.
19. Moerschells, R. P., Hosokawa, Y., Tsunasawa, S., The specificities of yeast methionine aminopeptidase and acetylation of processing of altered iso-1-cytochromes c created by oligonucleotide transformation. J. Biol. Chem. 1990, 265, 19638–19643.
20. 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.
21. 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.
22. Helbig, A. O., Gauci, S., Raijmakers, R., vanBreukelen, B. 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.
23. Arnesen, T., Towards a functional understanding of protein N-terminal acetylation. PLoS Biol. 2011, 9, e1001074.
24. Hershko, A., Heller, H., Eytan, E., Kaklut, G., Roset, I. A., Role of the alpha-amino group of protein in ubiquitin-mediated protein breakdown. Proc. Natl. Acad. Sci. U S A 1984, 81, 7021–7025.
25. Hoshiyasu, S., Kohzuma, K., Yoshida, K., Fujiwara, M. et al., Potential involvement of N-terminal acetylation in the quantitative regulation of the ε subunit of chloroplast ATP synthase under drought stress. Biosci. Biotechnol. Biochem. 2013, 77, 998–1007.
26. Zattas, D., Adle, D. J., Rubenstein, E. M., Hochstrasser, M., N-terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Mol. Biol. Cell 2013, 24, 890–900.
27. Hwang, C.-S., Shemorry, A., Varshavsky, A., N-terminal acetylation of cellular proteins creates specific degradation signals. Science 2010, 327, 973–977.
28. Shemorry, A., Hwang, C., Varshavsky, A., Control of Protein Quality and Stoichiometries by N-Terminal Acetylation and the N-End Rule Pathway. Mol. Cell 2013, 50, 540–551.
29. Forte, G. M. a, Pool, M. R., Stirling, C. J., N-terminal acetylation inhibits protein targeting to the endoplasmic reticulum. PLoS Biol. 2011, 9, e1001073.
30. Coulton, A. T., East, D. A., Galinska-Rakoczy, A., Lehman, W., Mulvihill, D. P., The recruitment of acetylated and unacetylated tropomyosin to distinct actin polymers permits the discrete regulation of specific myosins in fission yeast. J. Cell Sci. 2010, 123, 3235–3243.
31. Polevoda, B., Cardillo, T. S., Doyle, T. C., Bedi, G. S., Sherman, F., Nat3p and Mdm20p are required for function of yeast NatB Nalpha-terminal acetyltransferase and of actin and tropomyosin. J. Biol. Chem. 2003, 278, 30686–30697.
32. Singer, J. M., Shaw, J. M., Mdm20 protein functions with Nat3 protein to acetylate Tpm1 protein and regulate tropomyosin-actin interactions in budding yeast. Proc. Natl. Acad. Sci. U S A 2003, 100, 7644–7649.
33. Arnaudo, N., Fernández, I. S., McLaughlin, S. H., Peak-Chew, S. Y. et al., The N-terminal acetylation of Sir3 stabilizes its binding to the nucleosome core particle. Nat. Struct. Mol. Biol. 2013, 20, 1119–1121.
34. Van Welsem, T., Frederiks, F., Verzijlbergen, K. F., Faber, A. W. et al., Synthetic lethal screens identify gene silencing processes in yeast and implicate the acetylated amino terminus of Sir3 in recognition of the nucleosome core. Mol. Cell. Biol. 2008, 28, 3861–3872.
35. Scott, D. C., Monda, J. K., Bennett, E. J., Harper, J. W., Schulman, B. a., N-terminal acetylation acts as an avidity enhancer within an interconnected multiprotein complex. Science 2011, 334, 674–678.
36. Behnia, R., Barr, F. a, Flanagan, J. J., Barlowe, C., Munro, S., 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.
37. Behnia, R., Panic, B., Whyte, J. R. C., Munro, S., 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.
38. Dikiy, I., Eliezer, D., N-terminal acetylation stabilizes N-terminal helicity in lipid- and micelle-bound α-synuclein and increases its affinity for physiological membranes. J. Biol. Chem. 2014, 289, 3652–3665.
39. 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.
40. 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.
41. Setty, S. R. G., Strochlic, T. I., Tong, A. H. Y., Boone, C., Burd, C. G., Golgi targeting of ARF-like GTPase Arl3p requires its Nalpha-acetylation and the integral membrane protein Sys1p. Nat. Cell Biol. 2004, 6, 414–419.
42. 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, e24713.
43. 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.
44. 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.
45. 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.
46. Chu, C.-W., Hou, F., Zhang, J., Phu, L. 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.
47. 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.
48. Aksnes, H., Osberg, C., Arnesen, T., N-terminal acetylation by NatC is not a general determinant for substrate subcellular localization in Saccharomyces cerevisiae. PLoS One 2013, 8, e61012.
49. Aksnes, H., Van Damme, P., Goris, M., Starheim, K. K. et al., An organellar Nα-acetyltransferase, Naa60, acetylates cytosolic n termini of transmembrane proteins and maintains Golgi integrity. Cell Rep. 2015, 10, 1362–1374.
50. Rope, A. F., Wang, K., Evjenth, R., Xing, J. 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.
51. Esmailpour, T., Riazifar, H., Liu, L., Donkervoort, S. et al., A splice donor mutation in NAA10 results in the dysregulation of the retinoic acid signalling pathway and causes Lenz microphthalmia syndrome. J. Med. Genet. 2014, 51, 185–196.
52. Myklebust, L. M., Van Damme, P., Støve, S. I., Dörfel, M. J. et al., Biochemical and cellular analysis of Ogden syndrome reveals downstream Nt-acetylation defects. Hum. Mol. Genet. 2014, 24, 1956–1976.
53. Popp, B., Støve, S. I., Endele, S., Myklebust, L. M. et al., De novo missense mutations in the NAA10 gene cause severe non-syndromic developmental delay in males and females. Eur. J. Hum. Genet. 2014, 23, 602–619.
54. Wang, Y., Mijares, M., Gall, M. D., Turan, T. et al., Drosophila variable nurse cells encodes arrest defective 1 (ARD1), the catalytic subunit of the major N-terminal acetyltransferase complex. Dev. Dyn. 2010, 239, 2813–2827.
55. Hua, K.-T., Tan, C.-T., Johansson, G., Lee, J.-M. 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.
56. Shin, D. H., Chun, Y.-S., Lee, K.-H., Shin, H.-W., Park, J.-W., Arrest defective-1 controls tumor cell behavior by acetylating myosin light chain kinase. PLoS One 2009, 4, e7451.
57. Wang, Z., Wang, Z., Guo, J., Li, Y. et al., Inactivation of androgen-induced regulator ARD1 inhibits androgen receptor acetylation and prostate tumorigenesis. Proc. Natl. Acad. Sci. U S A 2012, 109, 3053–3058.
58. Xu, H., Jiang, B., Meng, L., Ren, T. et al., N-α-acetyltransferase 10 protein inhibits apoptosis through RelA/p65-regulated MCL1 expression. Carcinogenesis 2012, 33, 1193–1202.
59. Kalvik, T. V, Arnesen, T., Protein N-terminal acetyltransferases in cancer. Oncogene 2012, 32, 269–276.
60. Seo, J. H., Cha, J.-H., Park, J.-H., Jeong, C.-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.
61. Graveley, B. R., Brooks, A. N., Carlson, J. W., Duff, M. O. et al., The developmental transcriptome of Drosophila melanogaster. Nature 2011, 471, 473–479.
62. Warnhoff, K., Murphy, J. T., Kumar, S., Schneider, D. L. et al., The DAF-16 FOXO transcription factor regulates natc-1 to modulate stress resistance in Caenorhabditis elegans, linking insulin/IGF-1 signaling to protein N-terminal acetylation. PLoS Genet. 2014, 10, e1004703.
63. Stephan, D., Sánchez-Soriano, N., Loschek, L. F., Gerhards, R. et al., Drosophila Psidin regulates olfactory neuron number and axon targeting through two distinct molecular mechanisms. J. Neurosci. 2012, 32, 16080–16094.
64. Kuo, H. P., Lee, D. F., Xia, W., Lai, C. C. et al., Phosphorylation of ARD1 by IKKβ contributes to its destabilization and degradation. Biochem. Biophys. Res. Commun. 2009, 389, 156–161.
65. Yoon, H., Kim, H.-L., Chun, Y.-S., Shin, D. H. et al., NAA10 controls osteoblast differentiation and bone formation as a feedback regulator of Runx2. Nat. Commun. 2014, 5, 5176.
66. Kaelin, W. G., McKnight, S. L., Influence of metabolism on epigenetics and disease. Cell 2013, 153, 56–69.
67. Yi, C. H., Pan, H., Seebacher, J., Jang, I.-H. et al., Metabolic regulation of protein N-alpha-acetylation by Bcl-xL promotes cell survival. Cell 2011, 146, 607–620.
68. Barbehenn, E. K., Wales, R. G., Lowry, O. H., Measurement of metabolites in single preimplantation embryos; a new means to study metabolic control in early embryos. J. Embryol. Exp. Morphol. 1978, 43, 29–46.
69. Zhang, J., Khvorostov, I., Hong, J. S., Oktay, Y. et al., UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J. 2011, 30, 4860–4873.
70. Shyh-Chang, N., Daley, G. Q., Cantley, L. C., Stem cell metabolism in tissue development and aging. Development 2013, 140, 2535–2547.
71. Fantin, V. R., St-Pierre, J., Leder, P., Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006, 9, 425–434.
72. Warburg, O., On origin of cancer cells. Science (80-.). 1956, 123, 309–314.
73. Warburg, O., On respiratory impairment in cancer cells. Science 1956, 124, 269–270.
74. Heiden, M. Vander, Cantley, L., Thompson, C., Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324, 1029–1033.
75. Comerford, S. A., Huang, Z., Du, X., Wang, Y. et al., Acetate dependence of tumors. Cell 2014, 159, 1591–1602.
76. Mashimo, T., Pichumani, K., Vemireddy, V., Hatanpaa, K. J. et al., Acetate is a bioenergetic substrate for human glioblastoma and brain metastases. Cell 2014, 159, 1603–1614.