A neurostimulant para-chloroamphetamine inhibits the arginylation branch of the N-end rule pathway

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Jiang, Yanxialei ^a   Choi, Won Hoon ^a   Lee, Jung Hoon ^a   Han, Dong Hoon ^a   Kim, Ji Hyeon ^a   Chung, Young Shin ^b   Kim, Se Hyun ^c   Lee, Min Jae ^a  

^a Kyung Hee University   (South Korea)

^b Hoseo University   (South Korea)

^c Dongguk University Ilsan Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CHLORAMPHETAMINE; GUANINE NUCLEOTIDE BINDING PROTEIN; RGS PROTEIN; RGS4 PROTEIN;

ANIMAL; C57BL MOUSE; DRUG EFFECTS; FRONTAL LOBE; HELA CELL LINE; HIPPOCAMPUS; HUMAN; MALE; METABOLISM; MOUSE; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; ARGININE; CELL LINE, TUMOR; FRONTAL LOBE; GTP-BINDING PROTEINS; HELA CELLS; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, INBRED C57BL; P-CHLOROAMPHETAMINE; PROTEOLYSIS; RGS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84923287406     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06344     Document Type: Article

References (54)

1. 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 12, 735-747 (2011).
2. Varshavsky, A. The N-end rule pathway and regulation by proteolysis. Protein Sci (2011).
3. Bachmair, A., Finley, D. & Varshavsky, A. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186 (1986).
4. Cerda-Maira, F. A. et al. Molecular analysis of the prokaryotic ubiquitin-like protein (Pup) conjugation pathway in Mycobacterium tuberculosis. Mol Microbiol 77, 1123-1135 (2010).
5. Humbard, M. A. et al. Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463, 54-60 (2010).
6. Varshavsky, A. The ubiquitin system, an immense realm. Annu Rev Biochem 81, 167-176 (2012).
7. Hwang, C. S., Shemorry, A. & Varshavsky, A. N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327, 973-977 (2010).
8. 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 50, 540-551 (2013).
9. Lee, M. J. et al. Characterization of arginylation branch of N-end rule pathway in G-protein-mediated proliferation and signaling of cardiomyocytes. J Biol Chem 287, 24043-24052 (2012).
10. An, J. Y. et al. UBR2 mediates transcriptional silencing during spermatogenesis via histone ubiquitination. Proc Natl Acad Sci U S A 107, 1912-1917 (2010).
11. An, J. Y. et al. UBR2 of the N-end rule pathway is required for chromosome stability via histone ubiquitylation in spermatocytes and somatic cells. PLoS One 7, e37414 (2012).
12. Lee, M. J. et al. RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc Natl Acad Sci U S A 102, 15030-15035 (2005).
13. 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 105, 76-81 (2008).
14. Ditzel, M. et al. Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat Cell Biol 5, 467-473 (2003).
15. Brower, C. S., Piatkov, K. I. & Varshavsky, A. Neurodegeneration-associated protein fragments as short-lived substrates of the N-end rule pathway. Mol Cell 50, 161-171 (2013).
16. Kim, H. K. et al. The N-terminal methionine of cellular proteins as a degradation signal. Cell 156, 158-169 (2014).
17. Tasaki, T. & Kwon, Y. T. The mammalian N-end rule pathway: new insights into its components and physiological roles. Trends Biochem Sci 32, 520-528 (2007).
18. Choi, W. S. et al. Structural basis for the recognition of N-end rule substrates by the UBR box of ubiquitin ligases. Nat Struct Mol Biol 17, 1175-1181 (2010).
19. Matta-Camacho, E., Kozlov, G., Li, F. F. & Gehring, K. Structural basis of substrate recognition and specificity in the N-end rule pathway. Nat Struct Mol Biol 17, 1182-1187 (2010).
20. Erbse, A. et al. ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439, 753-756 (2006).
21. Roman-Hernandez, G., Grant, R. A., Sauer, R. T. & Baker, T. A. Molecular basis of substrate selection by the N-end rule adaptor protein ClpS. Proc Natl Acad Sci U S A 106, 8888-8893 (2009).
22. Varshavsky, A. The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci U S A 93, 12142-12149 (1996).
23. Lee, M. J. et al. Synthetic heterovalent inhibitors targeting recognition E3 components of the N-end rule pathway. Proc Natl Acad Sci U S A 105, 100-105 (2008).
24. Sriram, S. et al. Development and characterization of monomeric N-end rule inhibitors through in vitro model substrates. J Med Chem 56, 2540-2546 (2013).
25. Jiang, Y. X. L. et al. Characterization of mammalian N-degrons and development of heterovalent inhibitors of the N-end rule pathway. Chem Sci 4, 3339-3346 (2013).
26. Lassen, J. B. The effect of p-chloroamphetamine on motility in rats after inhibition of monoamine synthesis, storage, uptake and receptor interaction. Psychopharmacologia 34, 243-254 (1974).
27. Harvey, J. A., McMaster, S. E. & Yunger, L. M. P-Chloramphetamine: Selective neurotoxic action in brain. Science 187, 841-843 (1975).
28. Zhang, Y. J. et al. Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc Natl Acad Sci U S A 106, 7607-7612 (2009).
29. Igaz, L. M. et al. Expression of TDP-43 C-terminal Fragments in Vitro Recapitulates Pathological Features of TDP-43 Proteinopathies. J Biol Chem 284, 8516-8524 (2009).
30. Gonda, D. K. et al. Universality and structure of the N-end rule. J Biol Chem 264, 16700-16712 (1989).
31. Tasaki, T. et al. A family of mammalian E3 ubiquitin ligases that contain the UBR box motif and recognize N-degrons. Mol Cell Biol 25, 7120-7136 (2005).
32. Hu, R. G. et al. The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature 437, 981-986 (2005).
33. Lipinski, C. A., Lombardo, F., Dominy, B. W. & Feeney, P. J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 46, 3-26 (2001).
34. Kwon, Y. T. et al. An essential role of N-terminal arginylation in cardiovascular development. Science 297, 96-99 (2002).
35. An, J. Y. et al. Impaired neurogenesis and cardiovascular development in mice lacking the E3 ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Proc Natl Acad Sci U S A 103, 6212-6217 (2006).
36. Hollinger, S. & Hepler, J. R. Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54, 527-559 (2002).
37. Ross, E. M. & Wilkie, T. M. GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 69, 795-827 (2000).
38. 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 4, e7757 (2009).
39. Dougan, D. A., Micevski, D. & Truscott, K. N. The N-end rule pathway: from recognition by N-recognins, todestructionby AAA 1proteases. Biochim Biophys Acta 1823, 83-91 (2012).
40. Erdely, H. A. et al. Regional expression of RGS4 mRNA in human brain. Eur J Neurosci 19, 3125-3128 (2004).
41. Krueger, C. E. et al. Conflict monitoring in early frontotemporal dementia. Neurology 73, 349-355 (2009).
42. Evdokimidis, I. et al. Frontal lobe dysfunction in amyotrophic lateral sclerosis. J Neurol Sci 195, 25-33 (2002).
43. Sriram, S. et al. Development and Characterization of Monomeric N-End Rule Inhibitors throughIn Vitro Model Substrates. J Med Chem 56, 2540-2546 (2013).
44. Wang, K. H., Roman-Hernandez, G., Grant, R. A., Sauer, R. T. & Baker, T. A. The molecular basis of N-end rule recognition. Mol Cell 32, 406-414 (2008).
45. Kisselev, A. F., Callard, A. & Goldberg, A. L. Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J Biol Chem 281, 8582-8590 (2006).
46. Besche, H. C., Haas, W., Gygi, S. P. & Goldberg, A. L. Isolation of mammalian 26S proteasomes and p97/VCP complexes using the ubiquitin-like domain from HHR23B reveals novel proteasome-associated proteins. Biochemistry 48, 2538-2549 (2009).
47. Rogers, J. H. et al. RGS4 causes increased mortality and reduced cardiac hypertrophy in response to pressure overload. J Clin Invest 104, 567-576 (1999).
48. Bodenstein, J., Sunahara, R. K. & Neubig, R. R. N-terminal residues control proteasomal degradation of RGS2, RGS4, and RGS5 in human embryonic kidney 293 cells. Mol Pharmacol 71, 1040-1050 (2007).
49. Stewart, J. J. Optimization of parameters for semiempirical methods V: modification of NDDO approximations and application to 70 elements. J Mol Model 13, 1173-1213 (2007).
50. Sanner, M. F. A component-based software environment for visualizing large macromolecular assemblies. Structure 13, 447-462 (2005).
51. Morris, G. M. et al. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 30, 2785-2791 (2009).
52. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98, 10037-10041 (2001).
53. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65, 55-63 (1983).
54. Dantuma, N. P., Lindsten, K., Glas, R., Jellne, M. & Masucci, M. G. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat Biotechnol 18, 538-543 (2000).