Intracellular peptides: From discovery to function

EuPA Open Proteomics

Volumn 3, Issue , 2014, Pages 143-151

  Ferro, Emer S ^a   Rioli, Vanessa ^b   Castro, Leandro M ^a,c   Fricker, Lloyd D ^d  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cell signaling; Mass spectrometry; Peptides; Peptidomics; Protein protein interaction; Receptors

Indexed keywords

CELL PROTEIN; MICRORNA;

ARTICLE; BINDING SITE; CELL COMMUNICATION; CELL FUNCTION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; PROTEIN TARGETING; RNA STABILITY; SIGNAL TRANSDUCTION;

EID: 84901713520     PISSN: None     EISSN: 22129685     Source Type: Journal    
DOI: 10.1016/j.euprot.2014.02.009     Document Type: Article

References (82)

1. Kisselev A.F., Akopian T.N., Woo K.M., Goldberg A.L. The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J Biol Chem 1999, 274:3363-3371.
2. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426:895-899.
3. Reits E., Griekspoor A., Neijssen J., Groothuis T., Jalink K., van Veelen P., et al. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 2003, 18:97-108.
4. Huyer G., Kistler A., Nouvet F.J., George C.M., Boyle M.L., Michaelis S. Saccharomyces cerevisiae a-factor mutants reveal residues critical for processing, activity, and export. Eukaryot Cell 2006, 5:1560-1570.
5. Knudsen J., Mandrup S., Rasmussen J.T., Andreasen P.H., Poulsen F., Kristiansen K. The function of acyl-CoA-binding protein (ACBP)/diazepam binding inhibitor (DBI). Mol Cell Biochem 1993, 123:129-138.
6. Alho H., Costa E., Ferrero P., Fujimoto M., Cosenza-Murphy D., Guidotti A. Diazepam-binding inhibitor: a neuropeptide located in selected neuronal populations of rat brain. Science 1985, 229:179-182.
7. Ojika K., Mitake S., Tohdoh N., Appel S.H., Otsuka Y., Katada E., et al. Hippocampal cholinergic neurostimulating peptides (HCNP). Prog Neurobiol 2000, 60:37-83.
8. Hayashi M.A., Gomes M.D., Reboucas N.A., Fernandes B.L., Ferro E.S., de Camargo A.C. Species specificity of thimet oligopeptidase (EC 3.4.24.15). Biol Chem Hoppe Seyler 1996, 377:283-291.
9. Cleverly K., Wu T.J. Is the metalloendopeptidase EC 3.4.24.15 (EP24.15), the enzyme that cleaves luteinizing hormone-releasing hormone (LHRH), an activating enzyme?. Reproduction 2010, 139:319-330.
10. Oliveira V., Campos M., Melo R.L., Ferro E.S., Camargo A.C., Juliano M.A., et al. Substrate specificity characterization of recombinant metallo oligo-peptidases thimet oligopeptidase and neurolysin. Biochemistry 2001, 40:4417-4425.
11. Oliveira V., Campos M., Hemerly J.P., Ferro E.S., Camargo A.C., Juliano M.A., et al. Selective neurotensin-derived internally quenched fluorogenic substrates for neurolysin (EC 3.4.24.16): comparison with thimet oligopeptidase (EC 3.4.24.15) and neprilysin (EC 3.4.24.11). Anal Biochem 2001, 292:257-265.
12. Ferro E.S., Carreno F.R., Goni C., Garrido P.A., Guimaraes A.O., Castro L.M., et al. The intracellular distribution and secretion of endopeptidases 24.15 (EC 3.4.24.15) and 24.16 (EC 3.4.24.16). Protein Pept Lett 2004, 11:415-421.
13. Silva C.L., Portaro F.C., Bonato V.L., de Camargo A.C., Ferro E.S. Thimet oligopeptidase (EC 3.4.24.15), a novel protein on the route of MHC class I antigen presentation. Biochem Biophys Res Commun 1999, 255:591-595.
14. Portaro F.C., Gomes M.D., Cabrera A., Fernandes B.L., Silva C.L., Ferro E.S., et al. Thimet oligopeptidase and the stability of MHC class I epitopes in macrophage cytosol. Biochem Biophys Res Commun 1999, 255:596-601.
15. Ferro E.S., Hyslop S., Camargo A.C. Intracellullar peptides as putative natural regulators of protein interactions. J Neurochem 2004, 91:769-777.
16. Mochlyrosen D. Localization of protein-kinases by anchoring proteins - a theme in signal-transduction. Science 1995, 268:247-251.
17. Qvit N., Mochly-Rosen D. Highly specific modulators of protein kinase C localization: applications to heart failure. Drug Discov Today Dis Mech 2010, 7:e87-e93.
18. Souroujon M.C., Mochly-Rosen D. Peptide modulators of protein-protein interactions in intracellular signaling. Nat Biotechnol 1998, 16:919-924.
19. Kaneto H., Nakatani Y., Kawamori D., Miyatsuka T., Matsuoka T.A. Involvement of oxidative stress and the JNK pathway in glucose toxicity. Rev Diabet Stud 2004, 1:165-174.
20. Rosenmund C., Carr D.W., Bergeson S.E., Nilaver G., Scott J.D., Westbrook G.L. Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 1994, 368:853-856.
21. Ishida A., Kameshita I., Okuno S., Kitani T., Fujisawa H. A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 1995, 212:806-812.
22. Soderling S.H., Beavo J.A. Regulation of cAMP and cGMP signaling: new phosphodiesterases and new functions. Curr Opin Cell Biol 2000, 12:174-179.
23. +/calmodulin-dependent protein kinase II. J Biol Chem 2001, 276:3719-3722.
24. Haynes C.M., Yang Y., Blais S.P., Neubert T.A., Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol Cell 2010, 37:529-540.
25. Orlowski M. The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry 1990, 29:10289-10297.
26. Hershko A., Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998, 67:425-479.
27. Hershko A. From rabbit reticulocytes to clam oocytes: in search of the system that targets mitotic cyclins for degradation. Mol Biol Cell 2010, 21:1645-1647.
28. Lecker S.H., Goldberg A.L. Slowing muscle atrophy: putting the brakes on protein breakdown. J Physiol 2002, 545:729.
29. Kessler B.M., Glas R., Ploegh H.L. MHC class I antigen processing regulated by cytosolic proteolysis-short cuts that alter peptide generation. Mol Immunol 2002, 39:171-179.
30. Niedermann G., Geier E., Lucchiari-Hartz M., Hitziger N., Ramsperger A., Eichmann K. The specificity of proteasomes: impact on MHC class I processing and presentation of antigens. Immunol Rev 1999, 172:29-48.
31. Pickart C.M. Back to the future with ubiquitin. Cell 2004, 116:181-190.
32. Yu Z., Wang F., Milacic V., Li X., Cui Q.C., Zhang B., et al. Evaluation of copper-dependent proteasome-inhibitory and apoptosis-inducing activities of novel pyrrolidine dithiocarbamate analogues. Int J Mol Med 2007, 20:919-925.
33. Fernandez-Gamba A., Leal M.C., Morelli L., Castano E.M. Insulin-degrading enzyme: structure-function relationship and its possible roles in health and disease. Curr Pharm Des 2009, 15:3644-3655.
34. Gass J., Khosla C. Prolyl endopeptidases. Cell Mol Life Sci 2007, 64:345-355.
35. York I.A., Bhutani N., Zendzian S., Goldberg A.L., Rock K.L. Tripeptidyl peptidase II is the major peptidase needed to trim long antigenic precursors, but is not required for most MHC class I antigen presentation. J Immunol 2006, 177:1434-1443.
36. Turner A.J., Nalivaeva N.N. New insights into the roles of metalloproteinases in neurodegeneration and neuroprotection. Int Rev Neurobiol 2007, 82:113-135.
37. Grasso G., Rizzarelli E., Spoto G. The proteolytic activity of insulin-degrading enzyme: a mass spectrometry study. J Mass Spectrom 2009, 44:735-741.
38. Berti D.A., Morano C., Russo L.C., Castro L.M., Cunha F.M., Zhang X., et al. Analysis of intracellular substrates and products of thimet oligopeptidase in human embryonic kidney 293 cells. J Biol Chem 2009, 284:14105-14116.
39. Reits E., Neijssen J., Herberts C., Benckhuijsen W., Janssen L., Drijfhout J.W., et al. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 2004, 20:495-506.
40. Marcilla M., Villasevil E.M., de Castro J.A. Tripeptidyl peptidase II is dispensable for the generation of both proteasome-dependent and proteasome-independent ligands of HLA-B27 and other class I molecules. Eur J Immunol 2008, 38:631-639.
41. Tenorio-Laranga J., Mannisto P.T., Storvik M., Van der Veken P., Garcia-Horsman J.A. Four day inhibition of prolyl oligopeptidase causes significant changes in the peptidome of rat brain, liver and kidney. Biochimie 2012, 94:1849-1859.
42. Brandt I., De Vriendt K., Devreese B., Van Beeumen J., Van Dongen W., Augustyns K., et al. Search for substrates for prolyl oligopeptidase in porcine brain. Peptides 2005, 26:2536-2546.
43. Matsui M., Fowler J.H., Walling L.L. Leucine aminopeptidases: diversity in structure and function. Biol Chem 2006, 387:1535-1544.
44. Hattori A., Tsujimoto M. Processing of antigenic peptides by aminopeptidases. Biol Pharm Bull 2004, 27:777-780.
45. Rioli V., Gozzo F.C., Heimann A.S., Linardi A., Krieger J.E., Shida C.S., et al. Novel natural peptide substrates for endopeptidase 24.15, neurolysin, and angiotensin-converting enzyme. J Biol Chem 2003, 278:8547-8555.
46. Svensson M., Skold K., Svenningsson P., Andren P.E. Peptidomics-based discovery of novel neuropeptides. J Proteome Res 2003, 2:213-219.
47. Che F.Y., Lim J., Biswas R., Pan H., Fricker L.D. Quantitative neuropeptidomics of microwave-irradiated mouse brain and pituitary. Mol Cell Proteomics 2005, 4:1391-1405.
48. Dowell J.A., Heyden W.V., Li L. Rat Neuropeptidomics by LC-MS/MS and MALDI-FTMS: Enhanced Dissection and Extraction Techniques Coupled with 2D RP-RP HPLC. J Proteome Res 2006, 5:3368-3375.
49. Van Dijck A., Hayakawa E., Landuyt B., Baggerman G., Van Dam D., Luyten W., et al. Comparison of extraction methods for peptidomics analysis of mouse brain tissue. J Neurosci Methods 2011, 197:231-237.
50. Che F.Y., Zhang X., Berezniuk I., Callaway M., Lim J., Fricker L.D. Optimization of neuropeptide extraction from the mouse hypothalamus. J Proteome Res 2007, 6:4667-4676.
51. Fricker L.D. Analysis of mouse brain peptides using mass spectrometry-based peptidomics: implications for novel functions ranging from non-classical neuropeptides to microproteins. Mol Biosyst 2010, 6:1355-1365.
52. Castro L.M., Berti D.A., Russo L.C., Coelho V., Gozzo F.C., Oliveira V., et al. Similar intracellular peptide profile of TAP1/beta2 microglobulin double-knockout mice and C57BL/6 wild-type mice as revealed by peptidomic analysis. AAPS J 2010, 12:608-616.
53. Gelman J.S., Sironi J., Castro L.M., Ferro E.S., Fricker L.D. Peptidomic analysis of human cell lines. J Proteome Res 2011, 10:1583-1592.
54. Gelman J.S., Sironi J., Berezniuk I., Dasgupta S., Castro L.M., Gozzo F.C., et al. Alterations of the intracellular peptidome in response to the proteasome inhibitor bortezomib. PLoS ONE 2013, 8:e53263.
55. Schirle M., Heurtier M.A., Kuster B. Profiling core proteomes of human cell lines by one-dimensional PAGE and liquid chromatography-tandem mass spectrometry. Mol Cell Proteomics 2003, 2:1297-1305.
56. Doherty M.K., Hammond D.E., Clague M.J., Gaskell S.J., Beynon R.J. Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J Proteome Res 2009, 8:104-112.
57. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 2011, 44:325-340.
58. Fricker L.D., Gelman J.S., Castro L.M., Gozzo F.C., Ferro E.S. Peptidomic analysis of HEK293T cells: effect of the proteasome inhibitor epoxomicin on intracellular peptides. J Proteome Res 2012, 11:1981-1990.
59. Ciechanover A., Gonen H., Bercovich B., Cohen S., Fajerman I., Israel A., et al. Mechanisms of ubiquitin-mediated, limited processing of the NF-kappaB1 precursor protein p105. Biochimie 2001, 83:341-349.
60. Gomes I., Grushko J.S., Golebiewska U., Hoogendoorn S., Gupta A., Heimann A.S., et al. Novel endogenous peptide agonists of cannabinoid receptors. FASEB J 2009, 23:3020-3029.
61. Bauer M., Chicca A., Tamborrini M., Eisen D., Lerner R., Lutz B., et al. Identification and quantification of a new family of peptide endocannabinoids (Pepcans) showing negative allosteric modulation at CB1 receptors. J Biol Chem 2012, 287:36944-36967.
62. Biagioli M., Pinto M., Cesselli D., Zaninello M., Lazarevic D., Roncaglia P., et al. Unexpected expression of alpha- and beta-globin in mesencephalic dopaminergic neurons and glial cells. Proc Natl Acad Sci U S A 2009, 106:15454-15459.
63. Richter F., Meurers B.H., Zhu C., Medvedeva V.P., Chesselet M.F. Neurons express hemoglobin alpha and beta chains in rat and human brains. J Comp Neurol 2009, 51:538-547.
64. Gelman J.S., Dasgupta S., Berezniuk I., Fricker L.D. Analysis of peptides secreted from cultured mouse brain tissue. Biochim Biophys Acta 2013, 1834:2408-2417.
65. Nickel W., Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009, 10:148-155.
66. Heimann A.S., Favarato M.H., Gozzo F.C., Rioli V., Carreno F.R., Eberlin M.N., et al. ACE gene titration in mice uncovers a new mechanism for ACE on the control of body weight. Physiol Genomics 2005, 20:173-182.
67. Machado M.F., Cunha F.M., Berti D.A., Heimann A.S., Klitzke C.F., Rioli V., et al. Substrate phosphorylation affects degradation and interaction to endopeptidase 24.15, neurolysin, and angiotensin-converting enzyme. Biochem Biophys Res Commun 2006, 339:520-525.
68. Cunha F.M., Berti D.A., Ferreira Z.S., Klitzke C.F., Markus R.P., Ferro E.S. Intracellular peptides as natural regulators of cell signaling. J Biol Chem 2008, 283:24448-24459.
69. Russo L.C., Castro L.M., Gozzo F.C., Ferro E.S. Inhibition of thimet oligopeptidase by siRNA alters specific intracellular peptides and potentiates isoproterenol signal transduction. FEBS Lett 2012, 586:3287-3292.
70. Berti D.A., Russo L.C., Castro L.M., Cruz L., Gozzo F.C., Heimann J.C., et al. Identification of intracellular peptides in rat adipose tissue: Insights into insulin resistance. Proteomics 2012, 12:2668-2681.
71. Brady A.E., Limbird L.E. G protein-coupled receptor interacting proteins: emerging roles in localization and signal transduction. Cell Signal 2002, 14:297-309.
72. Wolfe B.L., Trejo J. Clathrin-dependent mechanisms of G protein-coupled receptor endocytosis. Traffic 2007, 8:462-470.
73. Russo L.C., Asega A.F., Castro L.M., Negraes P.D., Cruz L., Gozzo F.C., et al. Natural intracellular peptides can modulate the interactions of mouse brain proteins and thimet oligopeptidase with 14-3-3epsilon and calmodulin. Proteomics 2012, 12:2641-2655.
74. Kondo T., Plaza S., Zanet J., Benrabah E., Valenti P., Hashimoto Y., et al. Small peptides switch the transcriptional activity of Shavenbaby during Drosophila embryogenesis. Science 2010, 329:336-339.
75. Slavoff S.A., Mitchell A.J., Schwaid A.G., Cabili M.N., Ma J., Levin J.Z., et al. Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat Chem Biol 2012, 9:59-64.
76. Dolan B.P., Bennink J.R., Yewdell J.W. Translating DRiPs: progress in understanding viral and cellular sources of MHC class I peptide ligands. Cell Mol Life Sci 2011, 68:1481-1489.
77. Braks J.A.M., Martens G.J.M. 7B2 is a neuroendocrine chaperone that transiently interacts with prohormone convertase PC2 in the secretory pathway. Cell 1994, 78:263-273.
78. Fricker L.D., McKinzie A.A., Sun J., Curran E., Qian Y., Yan L., et al. Identification and characterization of proSAAS, a granin-like neuroendocrine peptide precursor that inhibits prohormone processing. J Neurosci 2000, 20:639-648.
79. Wisner A., Dufour E., Messaoudi M., Nejdi A., Marcel A., Ungeheuer M.N., et al. Human opiorphin, a natural antinociceptive modulator of opioid-dependent pathways. Proc Natl Acad Sci U S A 2006, 103:17979-17984.
80. Albiston A.L., McDowall S.G., Matsacos D., Sim P., Clune E., Mustafa T., et al. Evidence that the angiotensin IV (AT(4)) receptor is the enzyme insulin-regulated aminopeptidase. J Biol Chem 2001, 276:48623-48626.
81. Arkin M.R., Whitty A. The road less traveled: modulating signal transduction enzymes by inhibiting their protein-protein interactions. Curr Opin Chem Biol 2009, 13:284-290.
82. Armon-Omer A., Levin A., Hayouka Z., Butz K., Hoppe-Seyler F., Loya S., et al. Correlation between shiftide activity and HIV-1 integrase inhibition by a peptide selected from a combinatorial library. J Mol Biol 2008, 376:971-982.