Posttranslational arginylation as a global biological regulator

Developmental Biology

Volumn 358, Issue 1, 2011, Pages 1-8

  Saha, Sougata ^a   Kashina, Anna ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Angiogenesis; Arginyl tRNA protein transferase; Arginylation; Arginyltransferase; Posttranslational modifications; Proteasome; Regulation of development; Ubiquitin

Indexed keywords

ARGININE; ARGINYLTRANSFERASE; TRANSFER RNA;

ANGIOGENESIS; EMBRYO DEVELOPMENT; HEART DEVELOPMENT; HUMAN; MORPHOGENESIS; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ARGINYLATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW;

MAMMALIA;

EID: 81155162510     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.06.043     Document Type: Review

References (99)

1. Bachmair A., Finley D., Varshavsky A. In vivo half-life of a protein is a function of its amino-terminal residue. Science 1986, 234:179-186.
2. Balzi E., Choder M., Chen W.N., Varshavsky A., Goffeau A. Cloning and functional analysis of the arginyl-tRNA-protein transferase gene ATE1 of Saccharomyces cerevisiae. J. Biol. Chem. 1990, 265:7464-7471.
3. Berleth E.S., Li J., Braunscheidel J.A., Pickart C.M. A reactive nucleophile proximal to vicinal thiols is an evolutionarily conserved feature in the mechanism of Arg aminoacyl-tRNA protein transferase. Arch. Biochem. Biophys. 1992, 298:498-504.
4. Bohley P., Kopitz J., Adam G. Arginylation, surface hydrophobicity and degradation of cytosol proteins from rat hepatocytes. Adv. Exp. Med. Biol. 1988, 240:159-169.
5. Bohley P., Kopitz J., Adam G. Surface hydrophobicity, arginylation and degradation of cytosol proteins from rat hepatocytes. Biol. Chem. Hoppe. Seyler. 1988, 369:307-310. Suppl.
6. Bohley P., Kopitz J., Adam G., Rist B., von Appen F., Urban S. Post-translational arginylation and intracellular proteolysis. Biomed. Biochim. Acta. 1991, 50:343-346.
7. Bongiovanni G., Fidelio G.D., Barra H.S., Hallak M.E. The post-translational incorporation of arginine into a beta-amyloid peptide increases the probability of alpha-helix formation. Neuroreport 1995, 7:326-328.
8. Bongiovanni G., Fissolo S., Barra H.S., Hallak M.E. Posttranslational arginylation of soluble rat brain proteins after whole body hyperthermia. J. Neurosci. Res. 1999, 56:85-92.
9. Brower C.S., Varshavsky A. Ablation of arginylation in the mouse N-end rule pathway: loss of fat, higher metabolic rate, damaged spermatogenesis, and neurological perturbations. PLoS One 2009, 4:e7757.
10. Bulinski J.C. Tubulin posttranslational modifications: a Pushmi-Pullyu at work?. Dev. Cell 2009, 16:773-774.
11. Carpio M.A., Lopez Sambrooks C., Durand E.S., Hallak M.E. The arginylation-dependent association of calreticulin with stress granules is regulated by calcium. Biochem. J. 2010, 429:63-72.
12. Cestaro B. Effects of arginine, S-adenosylmethionine and polyamines on nerve regeneration. Acta Neurol. Scand. Suppl. 1994, 154:32-41.
13. Chakraborty G., Ingoglia N.A. N-terminal arginylation and ubiquitin-mediated proteolysis in nerve regeneration. Brain Res. Bull. 1993, 30:439-445.
14. Ciechanover A., Ferber S., Ganoth D., Elias S., Hershko A., Arfin S. Purification and characterization of arginyl-tRNA-protein transferase from rabbit reticulocytes. Its involvement in post-translational modification and degradation of acidic NH2 termini substrates of the ubiquitin pathway. J. Biol. Chem. 1988, 263:11155-11167.
15. Davydov I.V., Varshavsky A. RGS4 is arginylated and degraded by the N-end rule pathway in vitro. J. Biol. Chem. 2000, 275:22931-22941.
16. Decca M.B., Carpio M.A., Bosc C., Galiano M.R., Job D., Andrieux A., Hallak M.E. Post-translational arginylation of calreticulin: a new isospecies of calreticulin component of stress granules. J. Biol. Chem. 2007, 282:8237-8245.
17. Deutch C.E., Scarpulla R.C., Sonnenblick E.B., Soffer R.L. Pleiotropic phenotype of an Escherichia coli mutant lacking leucyl-, phenylalanyl-transfer ribonucleic acid-protein transferase. J. Bacteriol. 1977, 129:544-546.
18. Dougan D.A., Truscott K.N., Zeth K. The bacterial N-end rule pathway: expect the unexpected. Mol. Microbiol. 2010, 76:545-558.
19. Elias S., Ciechanover A. Post-translational addition of an arginine moiety to acidic NH2 termini of proteins is required for their recognition by ubiquitin-protein ligase. J. Biol. Chem. 1990, 265:15511-15517.
20. Eriste E., Norberg A., Nepomuceno D., Kuei C., Kamme F., Tran D.T., Strupat K., Jornvall H., Liu C., Lovenberg T.W., Sillard R. A novel form of neurotensin post-translationally modified by arginylation. J. Biol. Chem. 2005, 280:35089-35097.
21. Fissolo S., Bongiovanni G., Decca M.B., Hallak M.E. Post-translational arginylation of proteins in cultured cells. Neurochem. Res. 2000, 25:71-76.
22. Gonda D.K., Bachmair A., Wunning I., Tobias J.W., Lane W.S., Varshavsky A. Universality and structure of the N-end rule. J. Biol. Chem. 1989, 264:16700-16712.
23. Goz B., Voytek P. Arginyl transfer ribonucleic acid protein transferase and endogenous acceptor proteins in cultured mammalian cells. J. Biol. Chem. 1972, 247:5892-5897.
24. Graciet E., Walter F., Maoileidigh D.O., Pollmann S., Meyerowitz E.M., Varshavsky A., Wellmer F. The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13618-13623.
25. Hallak M.E., Barra H.S., Caputto R. Posttranslational incorporation of [14C]arginine into rat brain proteins. Acceptor changes during development. J. Neurochem. 1985, 44:665-669.
26. Hallak M.E., Bongiovanni G., Barra H.S. The posttranslational arginylation of proteins in different regions of the rat brain. J. Neurochem. 1991, 57:1735-1739.
27. Hammond J.W., Cai D., Verhey K.J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 2008, 20:71-76.
28. Hershko A., Ciechanover A., Varshavsky A. Basic medical research award. The ubiquitin system. Nat. Med. 2000, 6:1073-1081.
29. Holman T.J., Jones P.D., Russell L., Medhurst A., Ubeda Tomas S., Talloji P., Marquez J., Schmuths H., Tung S.A., Taylor I., Footitt S., Bachmair A., Theodoulou F.L., Holdsworth M.J. The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4549-4554.
30. Horinishi H., Kato M., Takahashi T. A sensitive and reproducible procedure for the assay of arginyl-tRNA:protein arginyl transferase. Anal. Biochem. 1976, 75:22-29.
31. Hu R.G., Sheng J., Qi X., Xu Z., Takahashi T.T., Varshavsky A. The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature 2005, 437:981-986.
32. Hu R.G., Brower C.S., Wang H., Davydov I.V., Sheng J., Zhou J., Kwon Y.T., Varshavsky A. Arginyltransferase, its specificity, putative substrates, bidirectional promoter, and splicing-derived isoforms. J. Biol. Chem. 2006, 281:32559-32573.
33. Hu R.G., Wang H., Xia Z., Varshavsky A. The N-end rule pathway is a sensor of heme. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:76-81.
34. Jack D.L., Chakraborty G., Ingoglia N.A. Ubiquitin is associated with aggregates of arginine modified proteins in injured nerves. Neuroreport 1992, 3:47-50.
35. Kaji H. Further studies on the soluble amino acid incorporating system from rat liver. Biochemistry 1968, 7:3844-3850.
36. Kaji H. Amino-terminal arginylation of chromosomal proteins by arginyl-tRNA. Biochemistry 1976, 15:5121-5125.
37. Kaji H., Kaji A. Protein modification by arginylation. Chem. Biol. 2011, 18:6-7.
38. Kaji H., Rao P. Membrane modification by arginyl tRNA. FEBS Lett. 1976, 66:194-197.
39. Kaji A., Kaji H., Novelli G.D. A soluble amino acid incorporating system. Biochem. Biophys. Res. Commun. 1963, 10:406-409.
40. Kaji H., Novelli G.D., Kaji A. A soluble amino acid-incorporating system from rat liver. Biochim. Biophys. Acta 1963, 76:474-477.
41. Kaji A., Kaji H., Novelli G.D. Soluble amino acid-incorporating system. I. Preparation of the system and nature of the reaction. J. Biol. Chem. 1965, 240:1185-1191.
42. Kaji A., Kaji H., Novelli G.D. Soluble amino acid-incorporating system. Ii. Soluble nature of the system and the characterization of the radioactive product. J. Biol. Chem. 1965, 240:1192-1197.
43. Kaji H., Hara H., Lamon K.D. Fixation of cellular aging processes by SV40 virus transformation. Mech. Ageing Dev. 1980, 12:197-209.
44. Karakozova M., Kozak M., Wong C.C., Bailey A.O., Yates J.R., Mogilner A., Zebroski H., Kashina A. Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science 2006, 313:192-196.
45. Kato M. Heparin as an inhibitor of L-arginyl-tRNA: protein arginyltransferase. J. Biochem. 1983, 94:2015-2022.
46. Kato M., Nozawa Y. Complete purification of arginyl-tRNA:protein arginyltransferase from hog kidney and production of its antibody. Anal. Biochem. 1984, 143:361-367.
47. Kemper B., Habener J.F. Non-rebosomal incorporation of arginine into a specific protein by a cell-free extract of parathyroid tissue. Biochim. Biophys. Acta 1974, 349:235-239.
48. Klemperer N.S., Pickart C.M. Arsenite inhibits two steps in the ubiquitin-dependent proteolytic pathway. J. Biol. Chem. 1989, 264:19245-19252.
49. Kopitz J., Rist B., Bohley P. Post-translational arginylation of ornithine decarboxylase from rat hepatocytes. Biochem. J. 1990, 267:343-348.
50. Kurosaka S., Leu N.A., Zhang F., Bunte R., Saha S., Wang J., Guo C., He W., Kashina A. Arginylation-dependent neural crest cell migration is essential for mouse development. PLoS Genet. 2010, 6:e1000878.
51. Kwon Y.T., Kashina A.S., Varshavsky A. Alternative splicing results in differential expression, activity, and localization of the two forms of arginyl-tRNA-protein transferase, a component of the N-end rule pathway. Mol. Cell. Biol. 1999, 19:182-193.
52. Kwon Y.T., Kashina A.S., Davydov I.V., Hu R.G., An J.Y., Seo J.W., Du F., Varshavsky A. An essential role of N-terminal arginylation in cardiovascular development. Science 2002, 297:96-99.
53. Lamon K.D., Kaji H. Arginyl-tRNA transferase activity as a marker of cellular aging in peripheral rat tissues. Exp. Gerontol. 1980, 15:53-64.
54. Lamon K.D., Vogel W.H., Kaji H. Stress-induced increases in rat brain arginyl-tRNA transferase activity. Brain Res. 1980, 190:285-287.
55. Lamon K.D., Chiger J.L., Kaji H. Effects of hydrocortisone and aspirin on protein synthesis and post-translational protein modification in cultured cells. Biochem. Pharmacol. 1982, 31:2047-2052.
56. Lee M.J., Tasaki T., Moroi K., An J.Y., Kimura S., Davydov I.V., Kwon Y.T. RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15030-15035.
57. Leibowitz M.J., Soffer R.L. A soluble enzyme from Escherichia coli which catalyzes the transfer of leucine and phenylalanine from tRNA to acceptor proteins. Biochem. Biophys. Res. Commun. 1969, 36:47-53.
58. Leibowitz M.J., Soffer R.L. Enzymatic modification of proteins. 3. Purification and properties of a leucyl, phenylalanyl transfer ribonucleic acid protein transferase from Escherichia coli. J. Biol. Chem. 1970, 245:2066-2073.
59. Leibowitz M.J., Soffer R.L. Enzymatic modification of proteins. VII. Substrate specificity of leucyl, phenylalanyl-transfer ribonucleic acid-protein transferase. J. Biol. Chem. 1971, 246:5207-5212.
60. Leu N.A., Kurosaka S., Kashina A. Conditional Tek promoter-driven deletion of arginyltransferase in the germ line causes defects in gametogenesis and early embryonic lethality in mice. PLoS One 2009, 4:e7734.
61. Li J., Pickart C.M. Binding of phenylarsenoxide to Arg-tRNA protein transferase is independent of vicinal thiols. Biochemistry 1995, 34:15829-15837.
62. Li J., Pickart C.M. Inactivation of arginyl-tRNA protein transferase by a bifunctional arsenoxide: identification of residues proximal to the arsenoxide site. Biochemistry 1995, 34:139-147.
63. Lim P.O., Kim H.J., Nam H.G. Leaf senescence. Ann. Rev. Plant Biol. 2007, 58:115-136.
64. Lock R.A., Harding H.W., Rogers G.E. Arginine transferase activity in homogenates from guinea-pig hair follicles. J. Invest. Dermatol. 1976, 67:582-586.
65. Manahan C.O., App A.A. An arginyl-transfer ribonucleic acid protein transferase from cereal embryos. Plant Physiol. 1973, 52:13-16.
66. Momose K., Kaji A. Soluble amino acid-incorporating system. 3. Further studies on the product and its relation to the ribosomal system for incorporation. J. Biol. Chem. 1966, 241:3294-3307.
67. Mutsuddi M., Marshall C.M., Benzow K.A., Koob M.D., Reba y I. The spinocerebellar ataxia 8 noncoding RNA causes neurodegeneration and associates with staufen in Drosophila. Curr. Biol. 2004, 14(4):302-308. (PubMed PMID: 14972680).
68. Rai R., Kashina A. Identification of mammalian arginyltransferases that modify a specific subset of protein substrates. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10123-10128.
69. Rai R., Wong C.C., Xu T., Leu N.A., Dong D.W., Guo C., McLaughlin K.J., Yates J.R., Kashina A. Arginyltransferase regulates alpha cardiac actin function, myofibril formation and contractility during heart development. Development 2008, 135:3881-3889.
70. Rao P., Kaji H. Comparative studies on isoaccepting arginyl tRNAs from transformed cells and their utilization in post-translational protein modification. Arch. Biochem. Biophys. 1977, 181:591-595.
71. Rao P., Kaji H. Effect of temperature on arginine incorporation by ribosomeless extracts of cells transformed by a temperature-sensitive mutant of Rous sarcoma virus. Biochim. Biophys. Acta 1977, 477:394-403.
72. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 2008, 9:679-690.
73. Saha S., Mundia M.M., Zhang F., Demers R.W., Korobova F., Svitkina T., Perieteanu A.A., Dawson J.F., Kashina A. Arginylation regulates intracellular actin polymer level by modulating actin properties and binding of capping and severing proteins. Mol. Biol. Cell 2010, 21:1350-1361.
74. Soffer R.L. The arginine transfer reaction. Biochim. Biophys. Acta 1968, 155:228-240.
75. Soffer R.L. Aminoacyl-tRNA-protein transferases: a novel class of enzymes catalyzing peptide bond formation. Trans. N. Y. Acad. Sci. 1970, 32:974-988.
76. Soffer R.L. Enzymatic modification of proteins. II. Purification and properties of the arginyl transfer ribonucleic acid-protein transferase from rabbit liver cytoplasm. J. Biol. Chem. 1970, 245:731-737.
77. Soffer R.L. Enzymatic modification of proteins. 4. Arginylation of bovine thyroglobulin. J. Biol. Chem. 1971, 246:1481-1484.
78. Soffer R.L. Enzymatic modification of proteins. V. Protein acceptor specificity in the arginine-transfer reaction. J. Biol. Chem. 1971, 246:1602-1606.
79. Soffer R.L. Peptide acceptors in the arginine transfer reaction. J. Biol. Chem. 1973, 248:2918-2921.
80. Soffer R.L. Peptide acceptors in the leucine, phenylalanine transfer reaction. J. Biol. Chem. 1973, 248:8424-8428.
81. Soffer R.L. Enzymatic arginylation of beta-melanocyte-stimulating hormone and of angiotensin II. J. Biol. Chem. 1975, 250:2626-2629.
82. Soffer R.L., Horinishi H. Enzymic modification of proteins. I. General characteristics of the arginine-transfer reaction in rabbit liver cytoplasm. J. Mol. Biol. 1969, 43:163-175.
83. Solomon V., Lecker S.H., Goldberg A.L. The N-end rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle. J. Biol. Chem. 1998, 273:25216-25222.
84. Spradling A.C., Stern D., Beaton A., Rhem E.J., Laverty T., Mozden N., Misra S., Rubin G.M. The berkeley drosophila genome project gene disruption project: single P-element insertions mutating 25% of vital drosophila genes. Genetics 1999, 153(1):135-177. PubMed Central PMCID: PMC1460730).
85. Takao K., Samejima K. Arginyl-tRNA-protein transferase activities in crude supernatants of rat tissues. Biol. Pharm. Bull. 1999, 22:1007-1009.
86. Tanaka Y., Kaji H. Incorporation of arginine by soluble extracts of ascites tumor cells and regenerating rat liver. Cancer Res. 1974, 34:2204-2208.
87. Varshavsky A. The early history of the ubiquitin field. Protein Sci. 2006, 15:647-654.
88. Wagner B.J., Margolis J.W. Post-translational arginylation in the bovine lens. Exp. Eye Res. 1991, 53:609-614.
89. Wang Y.M., Ingoglia N.A. N-terminal arginylation of sciatic nerve and brain proteins following injury. Neurochem. Res. 1997, 22:1453-1459.
90. Wang J., Han X., Saha S., Xu T., Rai R., Zhang F., Wolf Y.I., Wolfson A., Yates J.R., Kashina A. Arginyltransferase is an ATP-independent self-regulating enzyme that forms distinct functional complexes in vivo. Chem. Biol. 2011, 18:121-130.
91. Wong C.C.L., Xu T., Rai R., Bailey A.O., Yates J.R., Wolf Y.I., Zebroski H., Kashina A. Global analysis of posttranslational protein arginylation. PLoS Biol. 2007, 5:e258.
92. Xu N.S., Chakraborty G., Hassankhani A., Ingoglia N.A. N-terminal arginylation of proteins in explants of injured sciatic nerves and embryonic brains of rats. Neurochem. Res. 1993, 18:1117-1123.
93. Xu T., Wong C.C.L., Kashina A., Yates J.R. Identification of posstranslationally arginylated proteins and peptides by mass spectrometry. Nat. Protoc. 2009, 43:325-332.
94. Yoshida S., Ito M., Callis J., Nishida I., Watanabe A. A delayed leaf senescence mutant is defective in arginyl-tRNA:protein arginyltransferase, a component of the N-end rule pathway in Arabidopsis. Plant J. 2002, 32:129-137.
95. Yu M., Grabow M., Ingoglia N.A. Isolation of a peptide that inhibits the posttranslational arginylation of proteins in rat brain. J. Mol. Neurosci. 1993, 4:195-203.
96. Yu M., Chakraborty G., Grabow M., Ingoglia N.A. Serine protease inhibitors block N-terminal arginylation of proteins by inhibiting the arginylation of tRNA in rat brains. Neurochem. Res. 1994, 19:105-110.
97. Zanakis M.F., Chakraborty G., Sturman J.A., Ingoglia N.A. Posttranslational protein modification by amino acid addition in intact and regenerating axons of the rat sciatic nerve. J. Neurochem. 1984, 43:1286-1294.
98. Zhang N., Donnelly R., Ingoglia N.A. Evidence that oxidized proteins are substrates for N-terminal arginylation. Neurochem. Res. 1998, 23:1411-1420.
99. Zhang F., Saha S., Shabalina S.A., Kashina A. Differential arginylation of actin isoforms is regulated by coding sequence-dependent degradation. Science 2010, 329:1534-1537.