Zymogen activation of neurotrypsin and neurotrypsin-dependent agrin cleavage on the cell surface are enhanced by glycosaminoglycans

Biochemical Journal

Volumn 453, Issue 1, 2013, Pages 83-100

  Gisler, Claudio ^a   Lüscher, Daniel ^a   Schätzle, Philipp ^a   Dürr, Stephanie ^a   Baici, Antonio ^a   Galliciotti, Giovanna ^a   Reif, Raymond ^a   Bolliger, Marc F ^a   Kunz, Beat ^a   Sonderegger, Peter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Agrin; Glycosaminoglycan (GAG); Neurotrypsin; Proprotein convertase; Proteolysis; Zymogen activation

Indexed keywords

AGRIN; ENZYME PRECURSOR; GLYCOSAMINOGLYCAN; N METHYL DEXTRO ASPARTIC ACID; NEUROTRYPSIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL SURFACE; EMBRYO; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; RAT; SYNAPSE; SYNAPTIC POTENTIAL;

AGRIN; ANIMALS; BINDING SITES; CERCOPITHECUS AETHIOPS; COS CELLS; ENZYME ACTIVATION; GLYCOSAMINOGLYCANS; HEK293 CELLS; HUMANS; PRESYNAPTIC TERMINALS; PROPROTEIN CONVERTASES; SERINE ENDOPEPTIDASES; SYNDECAN-2;

EID: 84879012724     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130166     Document Type: Article

References (47)

1. Molinari, F., Rio, M., Meskenaite, V., Encha-Razavi, F., Auge, J., Bacq, D., Briault, S., Vekemans, M., Munnich, A., Attie-Bitach, T. et al. (2002) Truncating neurotrypsin mutation in autosomal recessive nonsyndromic mental retardation. Science 298, 1779-1781 (Pubitemid 35404119)
2. Frischknecht, R., Fejtova, A., Viesti, M., Stephan, A. and Sonderegger, P. (2008) Activity-induced synaptic capture and exocytosis of the neuronal serine protease neurotrypsin. J. Nanoneurosci. 28, 1568-1579 (Pubitemid 351287029)
3. Matsumoto-Miyai, K., Sokolowska, E., Zurlinden, A., Gee, C. E., Luscher, D., Hettwer, S., Wolfel, J., Ladner, A. P., Ster, J., Gerber, U. et al. (2009) Coincident pre- and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage. Cell 136, 1161-1171
4. Reif, R., Sales, S., Hettwer, S., Dreier, B., Gisler, C., Wolfel, J., Luscher, D., Zurlinden, A., Stephan, A., Ahmed, S. et al. (2007) Specific cleavage of agrin by neurotrypsin, a synaptic protease linked to mental retardation. FASEB J. 21, 3468-3478 (Pubitemid 350075137)
5. Stephan, A., Mateos, J. M., Kozlov, S. V., Cinelli, P., Kistler, A. D., Hettwer, S., Rulicke, T., Streit, P., Kunz, B. and Sonderegger, P. (2008) Neurotrypsin cleaves agrin locally at the synapse. FASEB J. 22, 1861-1873 (Pubitemid 351811463)
6. Knott, G. and Holtmaat, A. (2008) Dendritic spine plasticity-current understanding from in vivo studies. Brain Res. Rev. 58, 282-289
7. Reif, R., Sales, S., Dreier, B., Luscher, D., Wolfel, J., Gisler, C., Baici, A., Kunz, B. and Sonderegger, P. (2008) Purification and enzymological characterization of murine neurotrypsin. Protein Expression Purif. 61, 13-21
8. Gesemann, M., Cavalli, V., Denzer, A. J., Brancaccio, A., Schumacher, B. and Ruegg, M. A. (1996) Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16, 755-767 (Pubitemid 26124053)
9. Campanelli, J. T., Gayer, G. G. and Scheller, R. H. (1996) Alternative RNA splicing that determines agrin activity regulates binding to heparin and α-;dystroglycan. Development 122, 1663-1672 (Pubitemid 26159652)
10. O'Toole, J. J., Deyst, K. A., Bowe, M. A., Nastuk, M. A., McKechnie, B. A. and Fallon, J. R. (1996) Alternative splicing of agrin regulates its binding to heparin α-dystroglycan, and the cell surface. Proc. Natl. Acad. Sci. U.S.A. 93, 7369-7374
11. Baldi, L., Muller, N., Picasso, S., Jacquet, R., Girard, P., Thanh, H. P., Derow, E. and Wurm, F. M. (2005) Transient gene expression in suspension HEK-293 cells: application to large-scale protein production. Biotechnol. Prog. 21, 148-153 (Pubitemid 40218483)
12. Bezakova, G. and Ruegg, M. A. (2003) New insights into the roles of agrin. Nat. Rev. Mol. Cell Biol. 4, 295-308 (Pubitemid 36383956)
13. Winzen, U., Cole, G. J. and Halfter, W. (2003) Agrin is a chimeric proteoglycan with the attachment sites for heparan sulfate/chondroitin sulfate located in two multiple serine-glycine clusters. J. Biol. Chem. 278, 30106-30114 (Pubitemid 36962403)
14. Fromm, J. R., Hileman, R. E., Caldwell, E. E., Weiler, J. M. and Linhardt, R. J. (1997) Pattern and spacing of basic amino acids in heparin binding sites. Arch. Biochem. Biophys. 343, 92-100 (Pubitemid 27274346)
15. Cardin, A. D. and Weintraub, H. J. (1989) Molecular modeling of proteinglycosaminoglycan interactions. Arteriosclerosis 9, 21-32
16. Gandhi, N. S. and Mancera, R. L. (2008) The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 72, 455-482
17. Torrent, M., Nogues, M. V., Andreu, D. and Boix, E. (2012) The 'CPC clip motif': a conserved structural signature for heparin-binding proteins. PLoS ONE 7, e42692
18. Lietha, D., Chirgadze, D. Y., Mulloy, B., Blundell, T. L. and Gherardi, E. (2001) Crystal structures of NK1-heparin complexes reveal the basis for NK1 activity and enable engineering of potent agonists of the MET receptor. EMBO J. 20, 5543-5555 (Pubitemid 33010032)
19. Stephens, R. W., Bokman, A. M., Myohanen, H. T., Reisberg, T., Tapiovaara, H., Pedersen, N., Grondahl-Hansen, J., Llinas, M. and Vaheri, A. (1992) Heparin binding to the urokinase kringle domain. Biochemistry 31, 7572-7579
20. Gray, E., Hogwood, J. and Mulloy, B. (2012) The anticoagulant and antithrombotic mechanisms of heparin. Handb. Exp. Pharmacol. 207, 43-61
21. Pierce, A., Lyon, M., Hampson, I. N., Cowling, G. J. and Gallagher, J. T. (1992) Molecular cloning of the major cell surface heparan sulfate proteoglycan from rat liver. J. Biol. Chem. 267, 3894-3900
22. Choi, S., Lee, E., Kwon, S., Park, H., Yi, J. Y., Kim, S., Han, I. O., Yun, Y. and Oh, E. S. (2005) Transmembrane domain-induced oligomerization is crucial for the functions of syndecan-2 and syndecan-4. J. Biol. Chem. 280, 42573-42579 (Pubitemid 43049215)
23. Dews, I. C. and Mackenzie, K. R. (2007) Transmembrane domains of the syndecan family of growth factor coreceptors display a hierarchy of homotypic and heterotypic interactions. Proc. Natl. Acad. Sci. U.S.A. 104, 20782-20787
24. Li, Q., Rajanahally, S., Edson, M. A. and Matzuk, M. M. (2009) Stable expression and characterization of N-terminal tagged recombinant human bone morphogenetic protein 15. Mol. Hum. Reprod. 15, 779-788
25. Taylor, N. A., Van De Ven, W. J. and Creemers, J. W. (2003) Curbing activation: proprotein convertases in homeostasis and pathology. FASEB J. 17, 1215-1227 (Pubitemid 36775768)
26. Seidah, N. G., Mayer, G., Zaid, A., Rousselet, E., Nassoury, N., Poirier, S., Essalmani, R. and Prat, A. (2008) The activation and physiological functions of the proprotein convertases. Int. J. Biochem. Cell Biol. 40, 1111-1125
27. Bergeron, E., Basak, A., Decroly, E. and Seidah, N. G. (2003) Processing of α4 integrin by the proprotein convertases: histidine at position P6 regulates cleavage. Biochem. J. 373, 475-484 (Pubitemid 36897849)
28. Scamuffa, N., Basak, A., Lalou, C., Wargnier, A., Marcinkiewicz, J., Siegfried, G., Chretien, M., Calvo, F., Seidah, N. G. and Khatib, A. M. (2008) Regulation of prohepcidin processing and activity by the subtilisin-like proprotein convertases Furin, PC5, PACE4 and PC7. Gut 57, 1573-1582
29. Siegfried, G., Basak, A., Prichett-Pejic, W., Scamuffa, N., Ma, L., Benjannet, S., Veinot, J. P., Calvo, F., Seidah, N. and Khatib, A. M. (2005) Regulation of the stepwise proteolytic cleavage and secretion of PDGF-B by the proprotein convertases. Oncogene 24, 6925-6935 (Pubitemid 41509415)
30. Jin, W., Fuki, I. V., Seidah, N. G., Benjannet, S., Glick, J. M. and Rader, D. J. (2005) Proprotein convertases [corrected] are responsible for proteolysis and inactivation of endothelial lipase. J. Biol. Chem. 280, 36551-36559 (Pubitemid 41587730)
31. Siegfried, G., Basak, A., Cromlish, J. A., Benjannet, S., Marcinkiewicz, J., Chretien, M., Seidah, N. G. and Khatib, A. M. (2003) The secretory proprotein convertases furin, PC5, and PC7 activate VEGF-C to induce tumorigenesis. J. Clin. Invest. 111, 1723-1732 (Pubitemid 38057753)
32. Creemers, J. W. and Khatib, A. M. (2008) Knock-out mouse models of proprotein convertases: unique functions or redundancy? Front. Biosci. 13, 4960-4971 (Pubitemid 351599650)
33. Scamuffa, N., Calvo, F., Chretien, M., Seidah, N. G. and Khatib, A. M. (2006) Proprotein convertases: lessons from knockouts. FASEB J. 20, 1954-1963 (Pubitemid 44953895)
34. Nour, N., Mayer, G., Mort, J. S., Salvas, A., Mbikay, M., Morrison, C. J., Overall, C. M. and Seidah, N. G. (2005) The cysteine-rich domain of the secreted proprotein convertases PC5A and PACE4 functions as a cell surface anchor and interacts with tissue inhibitors of metalloproteinases. Mol. Biol. Cell 16, 5215-5226 (Pubitemid 41566833)
35. Mayer, G., Hamelin, J., Asselin, M. C., Pasquato, A., Marcinkiewicz, E., Tang, M., Tabibzadeh, S. and Seidah, N. G. (2008) The regulated cell surface zymogen activation of the proprotein convertase PC5A directs the processing of its secretory substrates. J. Biol. Chem. 283, 2373-2384
36. Huntington, J. A. (2003) Mechanisms of glycosaminoglycan activation of the serpins in hemostasis. J. Thromb. Haemostasis 1, 1535-1549
37. Li, W., Johnson, D. J., Esmon, C. T. and Huntington, J. A. (2004) Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat. Struct. Mol. Biol. 11, 857-862 (Pubitemid 39128802)
38. Dementiev, A., Petitou, M., Herbert, J. M. and Gettins, P. G. (2004) The ternary complex of antithrombin-anhydrothrombin-heparin reveals the basis of inhibitor specificity. Nat. Struct. Mol. Biol. 11, 863-867 (Pubitemid 39128803)
39. Gschwend, T. P., Krueger, S. R., Kozlov, S. V., Wolfer, D. P. and Sonderegger, P. (1997) Neurotrypsin, a novel multidomain serine protease expressed in the nervous system. Mol. Cell. Neurosci. 9, 207-219 (Pubitemid 27323433)
40. Proba, K., Gschwend, T. P. and Sonderegger, P. (1998) Cloning and sequencing of the cDNA encoding human neurotrypsin. Biochim. Biophys. Acta 1396, 143-147 (Pubitemid 28150174)
41. Knott, G. W., Holtmaat, A., Wilbrecht, L., Welker, E. and Svoboda, K. (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 9, 1117-1124 (Pubitemid 44306304)
42. Nagerl, U. V., Kostinger, G., Anderson, J. C., Martin, K. A. and Bonhoeffer, T. (2007) Protracted synaptogenesis after activity-dependent spinogenesis in hippocampal neurons. J. Nanoneurosci. 27, 8149-8156 (Pubitemid 47173311)
43. Fielding, R. A., Vellas, B., Evans, W. J., Bhasin, S., Morley, J. E., Newman, A. B., Abellan van Kan, G., Andrieu, S., Bauer, J., Breuille, D. et al. (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J. Am. Med. Dir. Assoc. 12, 249-256
44. Butikofer, L., Zurlinden, A., Bolliger, M. F., Kunz, B. and Sonderegger, P. (2011) Destabilization of the neuromuscular junction by proteolytic cleavage of agrin results in precocious sarcopenia. FASEB J. 25, 4378-4393
45. Bolliger, M. F., Zurlinden, A., Luscher, D., Butikofer, L., Shakhova, O., Francolini, M., Kozlov, S. V., Cinelli, P., Stephan, A., Kistler, A. D. et al. (2010) Specific proteolytic cleavage of agrin regulates maturation of the neuromuscular junction. J. Cell Sci. 123, 3944-3955
46. Bode, W. (2006) The structure of thrombin: a janus-headed proteinase. Semin. Thromb. Hemostasis 32, 16-31
47. Krishnaswamy, S. (2005) Exosite-driven substrate specificity and function in coagulation. J. Thromb. Haemostasis 3, 54-67