Alteration of prolyl oligopeptidase and activated α-2-macroglobulin in multiple sclerosis subtypes and in the clinically isolated syndrome

Biochemical Pharmacology

Volumn 85, Issue 12, 2013, Pages 1783-1794

  Tenorio Laranga, Jofre ^a,f   Peltonen, Iida ^a   Keskitalo, Salla ^b   Duran Torres, Gilberto ^a   Natarajan, Renuka ^c   Männistö, Pekka T ^a   Nurmi, Antti ^d   Vartiainen, Nina ^d   Airas, Laura ^e   Elovaara, Irina ^c   García Horsman, J Arturo ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d Charles River Discovery Research Services   (Finland)

^e TURKU UNIVERSITY HOSPITAL   (Finland)

^f INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

2 Macroglobulin; Biomarkers; Cell signaling; Inflammation; Multiple sclerosis; Prolyl oligopeptidase

Indexed keywords

ALPHA 2 MACROGLOBULIN; COLLAGEN; FIBRINOGEN; PROLYL ENDOPEPTIDASE; THYMOSIN BETA4;

ADOLESCENT; ADULT; ARTICLE; BLOOD ANALYSIS; CELL STIMULATION; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; ENZYME ANALYSIS; FEMALE; HUMAN; IMMUNOCOMPETENT CELL; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADULT; AGED; ALPHA-MACROGLOBULINS; ANIMALS; BIOLOGICAL MARKERS; CELL LINE, TUMOR; DEMYELINATING DISEASES; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MULTIPLE SCLEROSIS; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; SERINE ENDOPEPTIDASES; YOUNG ADULT;

EID: 84878872409     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.04.018     Document Type: Article

References (54)

1. S.L. Hauser, and J.R. Oksenberg The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration Neuron 52 2006 61 76 (Pubitemid 44466355)
2. W.I. McDonald, A. Compston, G. Edan, D. Goodkin, H.P. Hartung, and F.D. Lublin Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis Ann Neurol 50 2001 121 127
3. J.J. Graber, C.A. McGraw, D. Kimbrough, and S. Dhib-Jalbut Overlapping and distinct mechanisms of action of multiple sclerosis therapies Clin Neurol Neurosurg 112 2010 583 591
4. J.J. Graber, and S. Dhib-Jalbut Biomarkers of disease activity in multiple sclerosis J Neurol Sci 305 2011 1 10
5. U. Ziemann, M. Wahl, E. Hattingen, and H. Tumani Development of biomarkers for multiple sclerosis as a neurodegenerative disorder Prog Neurobiol 95 2011 670 685
6. J.A. García-Horsman, P.T. Männistö, and J.I. Venäläinen On the role of prolyl oligopeptidase in health and disease Neuropeptides 41 2007 1 24 (Pubitemid 46091700)
7. T.T. Myöhänen, J.A. García-Horsman, J. Tenorio-Laranga, and P.T. Männistö Issues about the physiological functions of prolyl oligopeptidase based on its discordant spatial association with substrates and inconsistencies among mRNA, protein levels, and enzymatic activity J Histochem Cytochem 57 2009 831 848
8. P.T. Männistö, J. Venäläinen, A. Jalkanen, and J.A. García-Horsman Prolyl oligopeptidase: a potential target for the treatment of cognitive disorders Drug News Perspect 20 2007 293 305 (Pubitemid 47345221)
9. I. Peltonen, A.J. Jalkanen, V. Sinervä, K.A. Puttonen, and P.T. Männistö Different effects of scopolamine and inhibition of prolyl oligopeptidase on mnemonic and motility functions of young and 8- to 9-month-old rats in the radial-arm maze Basic Clin Pharmacol Toxicol. 106 2010 280 287
10. A.J. Jalkanen, K.A. Puttonen, J.I. Venäläinen, V. Sinervä, A. Mannila, and S. Ruotsalainen Beneficial effect of prolyl oligopeptidase inhibition on spatial memory in young but not in old scopolamine-treated rats Basic Clin Pharmacol Toxicol 100 2007 132 138 (Pubitemid 46146718)
11. A. Penttinen, J. Tenorio-Laranga, A. Siikanen, M. Morawski, S. Rossner, and J.A. García-Horsman Prolyl oligopeptidase: a rising star on the stage of neuroinflammation research CNS Neurol Disord Drug Targets 10 2011 340 348
12. A.M. Lambeir Translational research on prolyl oligopeptidase inhibitors: the long road ahead Expert Opin Ther Patents 21 2011 977 981
13. M.J. Moreno-Baylach, K.A. Puttonen, J. Tenorio-Laranga, J.I. Venäläinen, M. Storvik, and M.M. Forsberg Prolyl endopeptidase is involved in cellular signalling in human neuroblastoma SH-SY5Y cells Neurosignals 19 2011 97 109
14. A. Klegeris, J. Li, T.K. Bammler, J. Jin, D. Zhu, and D.T. Kashima Prolyl endopeptidase is revealed following SILAC analysis to be a novel mediator of human microglial and THP-1 cell neurotoxicity Glia 56 6 2008 675 685
15. T.T. Myöhänen, M.J. Hannula, R. Van Elzen, M. Gerard, P. Van Der Veken, and J.A. García-Horsman A prolyl oligopeptidase inhibitor, KYP-2047, reduces α-synuclein protein levels and aggregates in cellular and animal models of Parkinson's disease Br J Pharmacol 166 3 2012 1097 1113
16. G. Breen, A.J. Harwood, K. Gregory, M. Sinclair, D. Collier, and D. St Clair Two peptidase activities decrease in treated bipolar disorder not schizophrenic patients Bipolar Disord 6 2004 156 161 (Pubitemid 38443570)
17. A. Gaggar, P.L. Jackson, B.D. Noerager, P.J. O'Reilly, D.B. McQuaid, and S.M. Rowe A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation J Immunol 180 2008 5662 5669
18. N.M. Weathington, A.H. van Houwelingen, B.D. Noerager, P.L. Jackson, A.D. Kraneveld, and F.S. Galin A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation Nat Med 12 2006 317 323 (Pubitemid 43355080)
19. J. Tenorio-Laranga, F. Coret-Ferrer, B. Casanova-Estruch, M. Burgal, and J.A. García-Horsman Prolyl oligopeptidase is inhibited in relapsing-remitting multiple sclerosis J Neuroinflammation 7 2010 23
20. C.H. Polman, S.C. Reingold, G. Edan, M. Filippi, H.P. Hartung, and L. Kappos Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria" Ann Neurol 58 2005 840 846 (Pubitemid 41746873)
21. J.F. Kurtzke Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS) Neurology 33 1983 1444 1452 (Pubitemid 14237132)
22. E. Agustí-Cobos, and J. Tenorio-Laranga Enhancement of fibrinolysis by inhibiting enzymatic cleavage of precursor alpha2-antiplasmin: a rebuttal J Thrombs Haemost: JTH 9 2011 1266 1267 Author reply 8-9
23. V.A. Schevchenko, E.A. Akayeva, I.M. Yeliseyeva, T.V. Yelisova, E.L. Yofa, and I.N. Nilova Human cytogenetic consequences of the Chernobyl accident Mutat Res 361 1996 29 34 (Pubitemid 26290702)
24. J.I. Venäläinen, R.O. Juvonen, M.M. Forsberg, A. García-Horsman, A. Poso, and E.A. Wallén Substrate-dependent, non-hyperbolic kinetics of pig brain prolyl oligopeptidase and its tight binding inhibition by JTP-4819 Biochem Pharmacol 64 2002 463 471 (Pubitemid 34874849)
25. M. Krieger, and J. Herz Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP) Annu Rev Biochem 63 1994 601 637
26. F. Van Leuven, P. Marynen, J.J. Cassiman, and H. Van den Berghe Proteolysis of human alpha 2-macroglobulin without hydrolysis of the internal thiolesters or expression of the receptor recognition site J Biol Chem 263 1988 468 471 (Pubitemid 18041099)
27. S.L. Gonias, A.E. Balber, W.J. Hubbard, and S.V. Pizzo Ligand binding, conformational change and plasma elimination of human, mouse and rat alpha-macroglobulin proteinase inhibitors Biochem J 209 1983 99 105 (Pubitemid 13153641)
28. M.J. Imber, and S.V. Pizzo Clearance and binding of two electrophoretic "fast" forms of human alpha 2-macroglobulin J Biol Chem 256 1981 8134 8139 (Pubitemid 12229851)
29. S.K. Moestrup The alpha 2-macroglobulin receptor and epithelial glycoprotein-330: two giant receptors mediating endocytosis of multiple ligands Biochim Biophys Acta 1197 1994 197 213
30. N.L. Banik Pathogenesis of myelin breakdown in demyelinating diseases: role of proteolytic enzymes Crit Rev Neurobiol 6 1992 257 271
31. M.L. Cuzner, A.N. Davison, and P. Rudge Proteolytic enzyme activity of blood leukocytes and cerebrospinal fluid in multiple sclerosis Ann Neurol 4 1978 337 344 (Pubitemid 9009862)
32. M. Gunnarsson, T. Stigbrand, and P.E. Jensen Decreased stability of alpha2-macroglobulin purified from patients with multiple sclerosis Acta Neurol Scand 101 2000 270 272 (Pubitemid 30155156)
33. M. Gunnarsson, P. Sundstrom, T. Stigbrand, and Jensen P.E. Native transformed alpha2-macroglobulin in plasma from patients with multiple sclerosis Acta Neurol Scand 108 2003 16 21 (Pubitemid 36791987)
34. P.E. Jensen, S. HumLe Jorgensen, P. Datta, and P.S. Sorensen Significantly increased fractions of transformed to total alpha2-macroglobulin concentrations in plasma from patients with multiple sclerosis Biochim Biophys Acta 1690 2004 203 207 (Pubitemid 39423615)
35. M.H. Han, S.I. Hwang, D.B. Roy, D.H. Lundgren, J.V. Price, and S.S. Ousman Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets Nature 451 2008 1076 1081 (Pubitemid 351317445)
36. P. Lambin, F. Pochon, and M. Steinbuch Heparin and plasma proteinase inhibitors: influence of heparin on the inhibition of thrombin by alpha 2 macroglobulin Adv Exp Med Biol 167 1984 263 272
37. E. Mantuano, G. Mukandala, X. Li, W.M. Campana, and S.L. Gonias Molecular dissection of the human alpha2-macroglobulin subunit reveals domains with antagonistic activities in cell signaling J Biol Chem 283 2008 19904 19911
38. S. Kamath, and G.Y. Lip Fibrinogen: biochemistry, epidemiology and determinants QJM: Monthly J Assoc Phys 96 2003 711 729 (Pubitemid 37259361)
39. L. Claudio, C.S. Raine, and C.F. Brosnan Evidence of persistent blood-brain barrier abnormalities in chronic-progressive multiple sclerosis Acta Neuropathol (Berl) 90 1995 228 238
40. P.Y. Paterson Experimental allergic encephalomyelitis: role of fibrin deposition in immunopathogenesis of inflammation in rats Fed Proc 35 1976 2428 2434
41. R.A. Adams, C. Schachtrup, D. Davalos, I. Tsigelny, and K. Akassoglou Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis Curr Med Chem 14 2007 2925 2936 (Pubitemid 350201659)
42. J. Tenorio-Laranga, P.T. Männistö, M. Storvik, P. Van der Veken, and J.A. García-Horsman Four day inhibition of prolyl oligopeptidase causes significant changes in the peptidome of rat brain, liver and kidney Biochimie 94 2012 1849 1859
43. T. Myöhänen, J. Tenorio-Laranga, B. Jokinen, R. Vazquez-Sanchez, M. Moreno-Baylach, and J. García-Horsman Prolyl oligopeptidase induces angiogenesis both in vitro and in vivo in a novel regulatory manner Br J Pharmacol 163 2011 1666 1678
44. S.J. Karlik, W.A. Roscoe, C. Patinote, and C. Contino-Pepin Targeting vascular changes in lesions in multiple sclerosis and experimental autoimmune encephalomyelitis Cent Nerv Syst Agents Med Chem 12 2012 7 14
45. N. Smart, C.A. Risebro, A.A. Melville, K. Moses, R.J. Schwartz, and K.R. Chien Thymosin beta-4 is essential for coronary vessel development and promotes neovascularization via adult epicardium Ann NY Acad Sci 1112 2007 171 188 (Pubitemid 47598641)
46. N. Smart, A. Rossdeutsch, and P.R. Riley Thymosin beta4 and angiogenesis: modes of action and therapeutic potential Angiogenesis 10 2007 229 241 (Pubitemid 350045880)
47. J. Zhang, Z.G. Zhang, D. Morris, Y. Li, C. Roberts, and S.B. Elias Neurological functional recovery after thymosin beta4 treatment in mice with experimental auto encephalomyelitis Neuroscience 164 2009 1887 1893
48. J. Tenorio-Laranga, P.T. Männistö, and J.A. García-Horsman Hunting for peptide substrates of prolyl oligopeptidase: classical versus non-classical bioactive peptides CNS Neurol Disord Drug Targets 10 2011 319 326
49. A.J. Jalkanen, J.J. Hakkarainen, M. Lehtonen, T. Venäläinen, T.M. Kääriäinen, and E. Jarho Brain pharmacokinetics of two prolyl oligopeptidase inhibitors, JTP-4819 and KYP-2047, in the rat Basic Clin Pharmacol Toxicol 109 6 2011 443 451
50. A.J. Jalkanen, T.P. Piepponen, J.J. Hakkarainen, I. De Meester, A.M. Lambeir, and M.M. Forsberg The effect of prolyl oligopeptidase inhibition on extracellular acetylcholine and dopamine levels in the rat striatum Neurochem Int 60 3 2012 301 309
51. J.I. Venäläinen, J.A. Garcia-Horsman, M.M. Forsberg, A. Jalkanen, E.A. Wallén, and E.M. Jarho Binding kinetics and duration of in vivo action of novel prolyl oligopeptidase inhibitors Biochem Pharmacol 71 5 2006 683 692 (Pubitemid 43122001)
52. S. Hagman, M. Raunio, M. Rossi, P. Dastidar, and I. Elovaara Disease-associated inflammatory biomarker profiles in blood in different subtypes of multiple sclerosis: prospective clinical and MRI follow-up study J Neuroimmunol 234 2011 141 147
53. P.J. Koelink, S.A. Overbeek, S. Braber, M.E. Morgan, P.A. Henricks, and M.A. Roda Collagen degradation and neutrophilic infiltration: a vicious circle in inflammatory bowel disease Gut 2013 1 10 10.1136/gutjnl-2012-303252
54. X. Chu, X. Ci, J. He, L. Jiang, M. Wei, and Q. Cao Effects of a natural prolyl oligopeptidase inhibitor, rosmarinic acid, on lipopolysaccharide-induced acute lung injury in mice Molecules 17 3 2012 3586 3598