Interaction of prolyl oligopeptidase with α-synuclein

CNS and Neurological Disorders - Drug Targets

Volumn 10, Issue 3, 2011, Pages 349-354

  Lambeir, Anne Marie ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Amyloid; Neurodegeneration; Neurotransmission; Parkinson's disease; Peptidase; Prolyl oligopeptidase; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; COLLAGEN FIBRIL; DIMETHYL SULFOXIDE; INOSITOL PHOSPHATE; LITHIUM; NEUROMODULIN; PROLYL ENDOPEPTIDASE; PROLYL ENDOPEPTIDASE INHIBITOR; TUBULIN; UMAC 21; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; GROWTH CONE; HUMAN; IN VITRO STUDY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

EID: 79951694335     PISSN: 18715273     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152711794653878     Document Type: Article

References (63)

1. Surguchov, A. Molecular and cellular biology of synucleins. Int. Rev. Cell Mol. Biol., 2008, 270, 225-317.
2. Uversky, V.N.; Eliezer, D. Biophysics of Parkinson's disease: structure and aggregation of alpha-synuclein. Curr. Protein Pept. Sci., 2009, 10(5), 483-499.
3. Bisaglia, M.; Mammi, S.; Bubacco, L. Structural insights on physiological functions and pathological effects of alpha-synuclein. FASEB J., 2009, 23(2), 329-340.
4. Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. Alpha-synuclein in Lewy bodies. Nature, 1997, 388(6645), 839-840.
5. Abeliovich, A.; Schmitz, Y.; Farinas, I.; Choi-Lundberg, D.; Ho, W.H.; Castillo, P.E.; Shinsky, N.; Verdugo, J.M.; Armanini, M.; Ryan, A.; Hynes, M.; Phillips, H.; Sulzer, D.; Rosenthal, A. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron, 2000, 25(1), 239-252.
6. Aravind, L.; Iyer, L.M.; Koonin, E.V. Comparative genomics and structural biology of the molecular innovations of eukaryotes. Curr. Opin. Struct. Biol., 2006, 16(3), 409-419.
7. Venäläinen, J.I.; Juvonen, R.O.; Männistö, P.T. Evolutionary relationships of the prolyl oligopeptidase family enzymes. Eur. J. Biochem., 2004, 271(13), 2705-2715.
8. Walter, R. Partial purification and characterization of post-proline cleaving enzyme: enzymatic inactivation of neurohypophyseal hormones by kidney preparations of various species. Biochim. Biophys. Acta, 1976, 422(1), 138-158.
9. Myöhänen, T.T.; Venäläinen, J.I.; Garcia-Horsman, J.A.; Männistö, P.T. Spatial association of prolyl oligopeptidase, inositol 1,4,5-triphosphate type 1 receptor, substance P and its neurokinin-1 receptor in the rat brain: an immunohistochemical colocalization study. Neuroscience, 2008, 153(4), 1177-1189.
10. Myöhänen, T.T.; Venäläinen, J.I.; Garcia-Horsman, J.A.; Piltonen, M.; Männistö, P.T. Distribution of prolyl oligopeptidase in the mouse whole-body sections and peripheral tissues. Histochem. Cell Biol., 2008, 130(5), 993-1003.
11. Myöhänen, T.T.; Venäläinen, J.I.; Garcia-Horsman, J.A.; Piltonen, M.; Männistö, P.T. Cellular and subcellular distribution of rat brain prolyl oligopeptidase and its association with specific neuronal neurotransmitters. J. Comp. Neurol., 2008, 507(5), 1694-1708.
12. Myöhänen, T.T.; Venäläinen, J.I.; Tupala, E.; Garcia-Horsman, J.A.; Miettinen, R.; Männistö, P.T. Distribution of immunoreactive prolyl oligopeptidase in human and rat brain. Neurochem. Res., 2007, 32(8), 1365-1374.
13. Brandt, I.; Scharpe, S.; Lambeir, A.M. Suggested functions for prolyl oligopeptidase: a puzzling paradox. Clin. Chim. Acta, 2007, 377(1-2), 50-61.
14. Männistö, P.T.; Venäläinen, J.; Jalkanen, A.; Garcia-Horsman, J.A. Prolyl oligopeptidase: a potential target for the treatment of cognitive disorders. Drug News Perspect., 2007, 20(5), 293-305.
15. Garcia-Horsman, J.A.; Männistö, P.T.; Venäläinen, J.I. On the role of prolyl oligopeptidase in health and disease. Neuropeptides, 2007, 41(1), 1-24.
16. Morain, P.; Robin, J.L.; De Nanteuil, G.; Jochemsen, R.; Heidet, V.; Guez, D. Pharmacodynamic and pharmacokinetic profile of S 17092, a new orally active prolyl endopeptidase inhibitor, in elderly healthy volunteers.A phase I study. Br. J. Clin. Pharmacol., 2000, 50, 350-359.
17. Umemura, K.; Kondo, K.; Ikeda, Y.; Kobayashi, T.; Urata, Y.; Nakashima, M. Pharmacokinetics and safety of JTP-4819, a novel specific orally active prolyl endopeptidase inhibitor, in healthy male volunteers. Br. J. Clin. Pharmacol., 1997, 43,613-618.
18. Williams, R.S.; Eames, M.; Ryves, W.J.; Viggars, J.; Harwood, A.J. Loss of a prolyl oligopeptidase confers resistance to lithium by elevation of inositol (1,4,5) trisphosphate. EMBO J., 1999, 18(10), 2734-2745.
19. Williams, R.S.; Cheng, L.; Mudge, A.W.; Harwood, A.J. A common mechanism of action for three mood-stabilizing drugs. Nature, 2002, 417(6886), 292-295.
20. Haffner, C.D.; Diaz, C.J.; Miller, A.B.; Reid, R.A.; Madauss, K.P.; Hassell, A.; Hanlon, M.H.; Porter, D.J.; Becherer, J.D.; Carter, L.H. Pyrrolidinyl pyridone and pyrazinone analogues as potent inhibitors of prolyl oligopeptidase (POP). Bioorg. Med. Chem. Lett., 2008, 18(15), 4360-4363.
21. Jarho, E.M.; Venäläinen, J.I.; Huuskonen, J.; Christiaans, J.A.; Garcia-Horsman, J.A.; Forsberg, M.M.; Jarvinen, T.; Gynther, J.; Männistö, P.T.; Wallen, E.A. A cyclopent-2-enecarbonyl group mimics proline at the P2 position of prolyl oligopeptidase inhibitors. J. Med. Chem., 2004, 47(23), 5605-5607.
22. Jarho, E.M.; Wallen, E.A.; Christiaans, J.A.; Forsberg, M.M.; Venäläinen, J.I.; Männistö, P.T.; Gynther, J.; Poso, A. Dicarboxylic acid azacycle l-prolyl-pyrrolidine amides as prolyl oligopeptidase inhibitors and three-dimensional quantitative structure-activity relationship of the enzyme-inhibitor interactions. J. Med. Chem., 2005, 48(15), 4772-4782.
23. Kanai, K.; Aranyi, P.; Bocskei, Z.; Ferenczy, G.; Harmat, V.; Simon, K.; Batori, S.; Naray-Szabo, G.; Hermecz, I. Prolyl oligopeptidase inhibition by N-acyl-pro-pyrrolidine-type molecules. J. Med. Chem., 2008, 51(23), 7514-7522.
24. Tran, T.; Quan, C.; Edosada, C.Y.; Mayeda, M.; Wiesmann, C.; Sutherlin, D.; Wolf, B.B. Synthesis and structure-activity relationship of N-acyl-Gly-, N-acyl-Sar- and N-blocked-boroPro inhibitors of FAP, DPP4, and POP. Bioorg. Med. Chem. Lett., 2007, 17(5), 1438-1442.
25. Venäläinen, J.I.; Wallen, E.A.; Poso, A.; Garcia-Horsman, J.A.; Männistö, P.T. Synthesis and characterization of the novel fluorescent prolyl oligopeptidase inhibitor 4-fluoresceinthiocarbamoyl-6-aminocaproyl-L-prolyl-2(S)-(hydroxyacetyl)pyrrolidine. J. Med. Chem., 2005, 48(23), 7093-7095.
26. Wallen, E.A.; Christiaans, J.A.; Forsberg, M.M.; Venäläinen, J.I.; Männistö, P.T.; Gynther, J. Dicarboxylic acid bis(L-prolylpyrrolidine) amides as prolyl oligopeptidase inhibitors. J. Med. Chem., 2002, 45(20), 4581-4584.
27. Wallen, E.A.; Christiaans, J.A.; Jarho, E.M.; Forsberg, M.M.; Venäläinen, J.I.; Männistö, P.T.; Gynther, J. New prolyl oligopeptidase inhibitors developed from dicarboxylic acid bis(lprolyl-pyrrolidine) amides. J. Med. Chem., 2003, 46(21), 4543-4551.
28. Schulz, I.; Gerhartz, B.; Neubauer, A.; Holloschi, A.; Heiser, U.; Hafner, M.; Demuth, H.U. Modulation of inositol 1,4,5-triphosphate concentration by prolyl endopeptidase inhibition. Eur. J. Biochem., 2002, 269(23), 5813-5820.
29. King, J.; Keim, M.; Teo, R.; Weening, K.E.; Kapur, M.; McQuillan, K.; Ryves, J.; Rogers, B.; Dalton, E.; Williams, R.S.; Harwood, A.J. Genetic control of lithium sensitivity and regulation of inositol biosynthetic genes. PLoS One, 2010, 5(6), e11151.
30. Di Daniel, E.; Glover, C.P.; Grot, E.; Chan, M.K.; Sanderson, T.H.; White, J.H.; Ellis, C.L.; Gallagher, K.T.; Uney, J.; Thomas, J.; Maycox, P.R.; Mudge, A.W. Prolyl oligopeptidase binds to GAP-43 and functions without its peptidase activity. Mol. Cell Neurosci., 2009, 41(3), 373-382.
31. Brandt, I.; De Vriendt, K.; Devreese, B.; Van Beeumen, J.; Van Dongen, W.; Augustyns, K.; De Meester, I.; Scharpe, S.; Lambeir, A.M. Search for substrates for prolyl oligopeptidase in porcine brain. Peptides, 2005, 26(12), 2536-2546.
32. Ueda, K.; Fukushima, H.; Masliah, E.; Xia, Y.; Iwai, A.; Yoshimoto, M.; Otero, D.A.; Kondo, J.; Ihara, Y.; Saitoh, T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. USA, 1993, 90(23), 11282-11286.
33. Liu, C.W.; Giasson, B.I.; Lewis, K.A.; Lee, V.M.; Demartino, G.N.; Thomas, P.J. A precipitating role for truncated alphasynuclein and the proteasome in alpha-synuclein aggregation: implications for pathogenesis of Parkinson disease. J. Biol. Chem., 2005, 280(24), 22670-22678.
34. Kim, H.J.; Lee, D.; Lee, C.H.; Chung, K.C.; Kim, J.; Paik, S.R. Calpain-resistant fragment(s) of alpha-synuclein regulates the synuclein-cleaving activity of 20S proteasome. Arch. Biochem. Biophys., 2006, 455(1), 40-47.
35. Levin, J.; Giese, A.; Boetzel, K.; Israel, L.; Hogen, T.; Nubling, G.; Kretzschmar, H.; Lorenzl, S. Increased alpha-synuclein aggregation following limited cleavage by certain matrix metalloproteinases. Exp. Neurol., 2009, 215(1), 201-208.
36. Bennett, M.C.; Bishop, J.F.; Leng, Y.; Chock, P.B.; Chase, T.N.; Mouradian, M.M. Degradation of alpha-synuclein by proteasome. J. Biol. Chem., 1999, 274(48), 33855-33858.
37. Vanhoof, G.; Goossens, F.; De Meester, I.; Hendriks, D.; Scharpe, S. Proline motifs in peptides and their biological processing. FASEB J., 1995, 9(9), 736-744.
38. Brandt, I.; Gerard, M.; Sergeant, K.; Devreese, B.; Baekelandt, V.; Augustyns, K.; Scharpe, S.; Engelborghs, Y.; Lambeir, A.M. Prolyl oligopeptidase stimulates the aggregation of alpha-synuclein. Peptides, 2008, 29(9), 1472-1478.
39. Fink, A.L. The aggregation and fibrillation of alpha-synuclein. Acc. Chem. Res., 2006, 39(9), 628-634.
40. Frieden, C. Protein aggregation processes: In search of the mechanism. Protein Sci., 2007, 16(11), 2334-2344.
41. nd Meeting of the Belgian Society of Biochemistry and Molecular Biology: Proteases and Protease Inhibitors, Antwerp, 2010.
42. Tompa, P.; Fuxreiter, M.; Oldfield, C.J.; Simon, I.; Dunker, A.K.; Uversky, V.N. Close encounters of the third kind: disordered domains and the interactions of proteins. Bioessays, 2009, 31(3), 328-335.
43. Gerard, M.; Deleersnijder, A.; Daniels, V.; Schreurs, S.; Munck, S.; Reumers, V.; Pottel, H.; Engelborghs, Y.; Van den Haute, C.; Taymans, J.M.; Debyser, Z.; Baekelandt, V. Inhibition of FK506 binding proteins reduces alpha-synuclein aggregation and Parkinson's disease-like pathology. J. Neurosci., 2010, 30(7), 2454-2463.
44. Miura, H.; Hashida, K.; Sudo, H.; Awa, Y.; Takarada-Iemata, M.; Kokame, K.; Takahashi, T.; Matsumoto, M.; Kitao, Y.; Hori, O. Deletion of Herp facilitates degradation of cytosolic proteins. Genes Cells, 2010, 15(8), 843-853.
45. Schulz, I.; Zeitschel, U.; Rudolph, T.; Ruiz-Carrillo, D.; Rahfeld, J.U.; Gerhartz, B.; Bigl, V.; Demuth, H.U.; Rossner, S. Subcellular localization suggests novel functions for prolyl endopeptidase in protein secretion. J. Neurochem., 2005, 94(4), 970-979.
46. Lo Bianco, C.; Ridet, J.L.; Schneider, B.L.; Deglon, N.; Aebischer, P. Alpha -Synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10813-10818.
47. Olanow, C.W.; Perl, D.P.; DeMartino, G.N.; McNaught, K.S. Lewy-body formation is an aggresome-related process: a hypothesis. Lancet Neurol., 2004, 3(8), 496-503.
48. Myöhänen, T.T.; Gerard, M.; Van Der Veken, P.; Van Elzen, R.; Baekelandt, V.; Lambeir, A.M. The inhibition of prolyl oligopeptidase reduces α-synuclein in A30P mutated cells. In International Meeting on Proline Specific Cleavage and oxy-prolyl formation, Halle (Saale), Germany, 2010.
49. Jalkanen, A.J.; Puttonen, K.A.; Venäläinen, J.I.; Sinervä, V.; Mannila, A.; Ruotsalainen, S.; Jarho, E.M.; Wallén, E.A.; Männistö PT. Beneficial effect of prolyl oligopeptidase inhibition on spatial memory in young but not in old scopolamine-treated rats. Basic Clin. Pharmacol. Toxicol., 2007, 100(2),132-138.
50. Mattson, M.P. Calcium and neurodegeneration. Aging Cell, 2007, 6(3), 337-350.
51. Narayanan, V.; Guo, Y.; Scarlata, S. Fluorescence studies suggest a role for alpha-synuclein in the phosphatidylinositol lipid signaling pathway. Biochemistry, 2005, 44(2), 462-470.
52. Esteves, A.R.; Arduino, D.M.; Swerdlow, R.H.; Oliveira, C.R.; Cardoso, S.M. Microtubule depolymerization potentiates alphasynuclein oligomerization. Front. Aging Neurosci., 2010, 1, 5.
53. Zhou, R.M.; Huang, Y.X.; Li, X.L.; Chen, C.; Shi, Q.; Wang, G.R.; Tian, C.; Wang, Z.Y.; Jing, Y.Y.; Gao, C.; Dong, X.P. Molecular interaction of alpha-synuclein with tubulin influences on the polymerization of microtubule in vitro and structure of microtubule in cells. Mol. Biol. Rep., 2010, 37(7), 3183-3192.
54. Tenorio-Laranga, J.; Venäläinen, J.I.; Männistö, P.T.; Garcia-Horsman, J.A. Characterization of membrane-bound prolyl endopeptidase from brain. FEBS J., 2008, 275(17), 4415-4427.
55. Camargo, A.C.; Almeida, M.L.; Emson, P.C. Involvement of endooligopeptidases A and B in the degradation of neurotensin by rabbit brain. J. Neurochem., 1984, 42(6), 1758-1761.
56. O'Leary, R.M.; Gallagher, S.P.; O'Connor, B. Purification and characterization of a novel membrane-bound form of prolyl endopeptidase from bovine brain. Int. J. Biochem. Cell Biol., 1996, 28(4), 441-449.
57. O'Leary, R.M.; O'Connor, B. Identification and localisation of a synaptosomal membrane prolyl endopeptidase from bovine brain. Eur. J. Biochem., 1995, 227(1-2), 277-283.
58. Morawski, M.; Schulz, I.; Rahfeld, J.-U.; Boonen, K.; Creemers, J.; Demuth, H.-U.; Rossner, S. Subcellular localization of PREP and PREPL in neuronal cells suggests functions in intracellular transport and protein secretion. In International Meeting on prolinespecific cleavage and oxyprolyl formation, Halle (Saale), Germany, 2010.
59. Cooper, A.A.; Gitler, A.D.; Cashikar, A.; Haynes, C.M.; Hill, K.J.; Bhullar, B.; Liu, K.; Xu, K.; Strathearn, K.E.; Liu, F.; Cao, S.; Caldwell, K.A.; Caldwell, G.A.; Marsischky, G.; Kolodner, R.D.; Labaer, J.; Rochet, J.C.; Bonini, N.M.; Lindquist, S. Alphasynuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science, 2006, 313(5785), 324-328.
60. Yu, S.; Li, X.; Liu, G.; Han, J.; Zhang, C.; Li, Y.; Xu, S.; Liu, C.; Gao, Y.; Yang, H.; Ueda, K.; Chan, P. Extensive nuclear localization of alpha-synuclein in normal rat brain neurons revealed by a novel monoclonal antibody. Neuroscience, 2007, 145(2), 539-555.
61. Hong, Z.; Shi, M.; Chung, K.A.; Quinn, J.F.; Peskind, E.R.; Galasko, D.; Jankovic, J.; Zabetian, C.P.; Leverenz, J.B.; Baird, G.; Montine, T.J.; Hancock, A.M.; Hwang, H.; Pan, C.; Bradner, J.; Kang, U.J.; Jensen, P.H.; Zhang, J. DJ-1 and alpha-synuclein in human cerebrospinal fluid as biomarkers of Parkinson's disease. Brain, 2010, 133(Pt 3), 713-726.
62. Van Gool, A.R.; Verkerk, R.; Fekkes, D.; Sleijfer, S.; Bannink, M.; Kruit, W.H.; van der Holt, B.; Scharpé, S.; Eggermont, A.M.; Stoter, G.; Hengeveld, M.W. Plasma activity of prolyl endopeptidase in relation to psychopathology during immunotherapy with IFN-alpha in patients with renal cell carcinoma. J. Interferon Cytokine Res., 2008, 28(5), 283-286.
63. Collins, P.J.; McMahon, G.; O'Brien, P.; O'Connor, B. Purification, identification and characterisation of seprase from bovine serum. Int. J. Biochem. Cell Biol., 2004, 36(11), 2320-2333.