The proprotein convertases and their implication in sterol and/or lipid metabolism

Biological Chemistry

Volumn 387, Issue 7, 2006, Pages 871-877

  Seidah, Nabil G ^a   Khatib, Abdel Majid ^a,b   Prat, Annik ^a  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b INSERM   (France)

Author keywords

Cancer metastasis; Cellular trafficking; Cholesterol and lipid metabolism; Proprotein convertase

Indexed keywords

AMINO ACID; FURIN; HIGH DENSITY LIPOPROTEIN; LIPID; LIPOPROTEIN; SERINE; SERINE PROTEINASE; STEROL; TRANSCRIPTION FACTOR;

ANIMAL CELL; CONFERENCE PAPER; ENDOTHELIUM; HUMAN; LIPID METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; HUMANS; HYDROLYSIS; LIPASE; LIPID METABOLISM; MICE; MOLECULAR SEQUENCE DATA; PROPROTEIN CONVERTASES; RECEPTORS, LDL; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; STEROLS;

EID: 33746216577     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2006.110     Document Type: Conference Paper

References (60)

1. Abifadel, M., Varret, M., Rabes, J.P., Allard, D., Ouguerram, K., Devillers, M., Cruaud, C., Benjannet, S., Wickham, L., Erlich, D., et al. (2003). Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat. Genet. 34, 154-156.
2. Attie, A.D. and Seidah, N.G. (2005). Dual regulation of the LDL receptor - some clarity and new questions. Cell Metab. 1, 290-292.
3. Basak, A., Chretien, M., and Seidah, N.G. (2002). A rapid fluorometric assay for the proteolytic activity of SKI-1/S1P based on the surface glycoprotein of the hemorrhagic fever Lassa virus. FEBS Lett. 514, 333-339.
4. Benjannet, S., Rhainds, D., Essalmani, R., Mayne, J., Wickham, L., Jin, W., Asselin, M.C., Hamelin, J., Varret, M., Allard, D., et al. (2004). NARC-1/PCSK9 and its natural mutants: zymogen cleavage and effects on the low density lipoprotein (LDL) receptor and LDL cholesterol. J. Biol. Chem. 279, 48865-48875.
5. Bergeron, E., Vincent, M.J., Wickham, L., Hamelin, J., Basak, A., Nichol, S.T., Chretien, M., and Seidah, N.G. (2005). Implication of proprotein convertases in the processing and spread of severe acute respiratory syndrome coronavirus. Biochem. Biophys. Res. Commun. 326, 554-563.
6. Brown, M.S. and Goldstein, J.L. (1999). A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. USA 96, 11041-11048.
7. Cohen, J., Pertsemlidis, A., Kotowski, I.K., Graham, R., Garcia, C.K., and Hobbs, H.H. (2005). Low LDL cholesterol in individuals of African descent resulting from frequent nonsense mutations in PCSK9. Nat. Genet. 37, 161-165.
8. Constam, D.B. and Robertson, E.J. (2000). SPC4/PACE4 regulates a TGFβ signaling network during axis formation. Genes Dev. 14, 1146-1155.
9. De Bie, I., Marcinkiewicz, M., Malide, D., Lazure, C., Nakayama, K., Bendayan, M., and Seidah, N.G. (1996). The isoforms of proprotein convertase PC5 are sorted to different subcellular compartments. J. Cell Biol. 135, 1261-1275.
10. De Cat, B., Muyldermans, S.Y., Coomans, C., Degeest, G., Vanderschueren, B., Creemers, J., Biemar, F., Peers, B., and David, G. (2003). Processing by proprotein convertases is required for glypican-3 modulation of cell survival, Wnt signaling, and gastrulation movements. J. Cell Biol. 163, 625-635.
11. Dubuc, G., Chamberland, A., Wassef, H., Davignon, J., Seidah, N.G., Bernier, L., and Prat, A. (2004). Statins upregulate PCSK9, the gene encoding the proprotein convertase neural apoptosis-regulated convertase-1 implicated in familial hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 24, 1454-1459.
12. Elagoz, A., Benjannet, S., Mammarbassi, A., Wickham, L., and Seidah, N.G. (2002). Biosynthesis and cellular trafficking of the convertase SKI-1/S1P: ectodomain shedding requires SKI-1 activity. J. Biol. Chem. 277, 11265-11275.
13. Espenshade, P.J., Cheng, D., Goldstein, J.L., and Brown, M.S. (1999). Autocatalytic processing of site-1 protease removes propeptide and permits cleavage of sterol regulatory element-binding proteins. J. Biol. Chem. 274, 22795-22804.
14. Essalmani, R., Hamelin, J., Marcinkiewicz, J., Chamberland, A., Mbikay, M., Chretien, M., Seidah, N.G., and Prat, A. (2006). Deletion of the gene encoding proprotein convertase 5/6 causes early embryonic lethality in the mouse. Mol. Cell. Biol. 26, 354-361.
15. Fujinaga, M., Cherney, M.M., Oyama, H., Oda, K., and James, M.N. (2004). The molecular structure and catalytic mechanism of a novel carboxyl peptidase from Scytalidium lignicolum. Proc. Natl. Acad. Sci. USA 101, 3364-3369.
16. Fuki, I.V., Blanchard, N., Jin, W., Marchadier, D.H., Millar, J.S., Glick, J.M., and Rader, D.J. (2003). Endogenously produced endothelial lipase enhances binding and cellular processing of plasma lipoproteins via heparan sulfate proteoglycan-mediated pathway. J. Biol. Chem. 278, 34331-34338.
17. Gauster, M., Hrzenjak, A., Schick, K., and Frank, S. (2005). Endothelial lipase is inactivated upon cleavage by the members of the proprotein convertase family. J. Lipid Res. 46, 977-987.
18. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and Mori, K. (1999). Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10, 3787-3799.
19. Jaye, M., Lynch, K.J., Krawiec, J., Marchadier, D., Maugeais, C., Doan, K., South, V., Amin, D., Perrone, M., and Rader, D.J. (1999). A novel endothelial-derived lipase that modulates HDL metabolism. Nat. Genet. 21, 424-428.
20. Jin, W., Fuki, I.V., Seidah, N.G., Benjannet, S., Glick, J.M., and Rader, D.J. (2005). Proprotein convertases are responsible for proteolysis and inactivation of endothelial lipase. J. Biol. Chem. 280, 36551-36559.
21. Khatib, A.M., Siegfried, G., Prat, A., Luis, J., Chretien, M., Metrakos, P., and Seidah, N.G. (2001). Inhibition of proprotein convertases is associated with loss of growth and tumorigenicity of HT-29 human colon carcinoma cells: importance of insulin-like growth factor-1 (IGF-1) receptor processing in IGF-1-mediated functions. J. Biol. Chem. 276, 30686-30693.
22. Khatib, A.M., Siegfried, G., Chretien, M., Metrakos, P., and Seidah, N.G. (2002). Proprotein convertases in tumor progression and malignancy: novel targets in cancer therapy. Am. J. Pathol. 160, 1921-1935.
23. Lenz, O., ter Meulen, J., Klenk, H.D., Seidah, N.G., and Garten, W. (2001). The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc. Natl. Acad. Sci. USA 98, 12701-12705.
24. Maxwell, K.N. and Breslow, J.L. (2004). Adenoviral-mediated expression of Pcsk9 in mice results in a low-density lipoprotein receptor knockout phenotype. Proc. Natl. Acad. Sci. USA 101, 7100-7105.
25. Mouchantaf, R., Watt, H.L., Sulea, T., Seidah, N.G., Alturaihi, H., Patel, Y.C., and Kumar, U. (2004). Prosomatostatin is proteolytically processed at the amino terminal segment by subtilase SKI-1. Regul. Pept. 120, 133-140.
26. no, M., Raab, G., Lau, K., Abraham, J.A., and Klagsbrun, M. (1994). Purification and characterization of transmembrane forms of heparin-binding EGF-like growth factor. J. Biol. Chem. 269, 31315-31321.
27. Nour, N., Basak, A., Chretien, M., and Seidah, N.G. (2003). Structure-function analysis of the prosegment of the proprotein convertase PC5A. J. Biol. Chem. 278, 2886-2895.
28. 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.
29. Puente, X.S., Sanchez, L.M., Overall, C.M., and Lopez-Otin, C. (2003). Human and mouse proteases: a comparative genomic approach. Nat. Rev. Genet. 4, 544-558.
30. Pullikotil, P., Vincent, M., Nichol, S.T., and Seidah, N.G. (2004). Development of protein-based inhibitors of the proprotein of convertase SKI-1/S1P: processing of SREBP-2, ATF6, and a viral glycoprotein. J. Biol. Chem. 279, 17338-17347.
31. Raggo, C., Rapin, N., Stirling, J., Gobeil, P., Smith-Windsor, E., O'Hare, P., and Misra, V. (2002). Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol. Cell Biol. 22, 5639-5649.
32. Rashid, S., Curtis, D.E., Garuti, R., Anderson, N.N., Bashmakov, Y., Ho, Y.K., Hammer, R.E., Moon, Y.A., and Horton, J.D. (2005). Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. Proc. Natl. Acad. Sci. USA 102, 5374-5379.
33. Rawson, R.B. (2003). Control of lipid metabolism by regulated intramembrane proteolysis of sterol regulatory element binding proteins (SREBPs). Biochem. Soc. Symp. 221-231.
34. Rawson, R.B., Zelenski, N.G., Nijhawan, D., Ye, J., Sakai, J., Hasan, M.T., Chang, T.Y., Brown, M.S., and Goldstein, J.L. (1997). Complementation cloning of S2P, a gene encoding a putative metalloprotease required for intramembrane cleavage of SREBPs. Mol. Cell 1, 47-57.
35. Rhee, D.K., Marcelino, J., Al Mayouf, S., Schelling, D.K., Bartels, C.F., Cui, Y., Laxer, R., Goldbach-Mansky, R., and Warman, M.L. (2005). Consequences of disease-causing mutations on lubricin protein synthesis, secretion, and post-translational processing. J. Biol. Chem. 280, 31325-31332.
36. Richer, M.J., Keays, C.A., Waterhouse, J., Minhas, J., Hashimoto, C., and Jean, F. (2004). The Spn4 gene of Drosophila encodes a potent furin-directed secretory pathway serpin. Proc. Natl. Acad. Sci. USA 101, 10560-10565.
37. Sakai, J., Rawson, R.B., Espenshade, P.J., Cheng, D., Seegmiller, A.C., Goldstein, J.L., and Brown, M.S. (1998). Molecular identification of the sterol-regulated luminal protease that cleaves SREBPs and controls lipid composition of animal cells. Mol. Cell 2, 505-514.
38. Sanchez, A.J., Vincent, M.J., Erickson, B.R., and Nichol, S.T. (2006). Crimean-Congo hemorrhagic fever virus glycoprotein precursor is cleaved by furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J. Virol. 80, 514-525.
39. Schlombs, K., Wagner, T., and Scheel, J. (2003). Site-1 protease is required for cartilage development in zebrafish. Proc. Natl. Acad. Sci. USA 100, 14024-14029.
40. Seidah, N.G. (2006). Unexpected similarity between the cytosolic West Nile virus NS3 and the secretory furin-like serine proteinases. Biochem. J. 393, e1-e3.
41. Seidah, N.G. and Chretien, M. (1999). Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res. 848, 45-62.
42. Seidah, N.G. and Prat, A. (2002). Precursor convertases in the secretory pathway, cytosol and extracellular milieu. Essays Biochem. 38, 79-94.
43. Seidah, N.G., Mowla, S.J., Hamelin, J., Mamarbachi, A.M., Benjannet, S., Toure, B.B., Basak, A., Munzer, J.S., Marcinkiewicz, J., Zhong, M., et al. (1999a). Mammalian subtilisin/kexin isozyme SKI-1: a widely expressed proprotein convertase with a unique cleavage specificity and cellular localization. Proc. Natl. Acad. Sci. USA 96, 1321-1326.
44. Seidah, N.G., Benjannet, S., Hamelin, J., Mamarbachi, A.M., Basak, A., Marcinkiewicz, J., Mbikay, M., Chretien, M., and Marcinkiewicz, M. (1999b). The subtilisin/kexin family of precursor convertases. Emphasis on PC1, PC2/7B2, POMC and the novel enzyme SKI-1. Ann. NY Acad. Sci. 885, 57-74.
45. Seidah, N.G., Benjannet, S., Wickham, L., Marcinkiewicz, J., Jasmin, S.B., Stifani, S., Basak, A., Prat, A., and Chretien, M. (2003). The secretory proprotein convertase neural apoptosis-regulated convertase 1 (NARC-1): liver regeneration and neuronal differentiation. Proc. Natl. Acad. Sci. USA 100, 928-933.
46. Shen, J., Chen, X., Hendershot, L., and Prywes, R. (2002). ER stress regulation of ATF6 localization by dissociation of BiP/ GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3, 99-111.
47. Siezen, R.J. and Leunissen, J.A. (1997). Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 6, 501-523.
48. Stieneke-Grober, A., Vey, M., Angliker, H., Shaw, E., Thomas, G., Roberts, C., Klenk, H.D., and Garten, W. (1992). Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11, 2407-2414.
49. Stirling, J. and O'Hare, P. (2006). CREB4, a transmembrane bZip transcription factor and potential new substrate for regulation and cleavage by S1P. Mol. Biol. Cell 17, 413-426.
50. Tang, M., Mikhailik, A., Pauli, I., Giudice, L.C., Fazelabas, A.T., Tulac, S., Carson, D.D., Kaufman, D.G., Barbier, C., Creemers, J.W., and Tabibzadeh, S. (2005). Decidual differentiation of stromal cells promotes proprotein convertase 5/6 expression and lefty processing. Endocrinology 146, 5313-5320.
51. 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.
52. Thomas, G. (2002). Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3, 753-766.
53. Tsuji, A., Sakurai, K., Kiyokage, E., Yamazaki, T., Koide, S., Toida, K., Ishimura, K., and Matsuda, Y. (2003). Secretory proprotein convertases PACE4 and PC6A are heparin-binding proteins which are localized in the extracellular matrix. Potential role of PACE4 in the activation of proproteins in the extracellular matrix. Biochim. Biophys. Acta 1645, 95-104.
54. Vey, M., Schafer, W., Berghofer, S., Klenk, H.D., and Garten, W. (1994). Maturation of the trans-Golgi network protease furin: compartmentalization of propeptide removal, substrate cleavage, and COOH-terminal truncation. J. Cell Biol. 127, 1829-1842.
55. Vincent, M.J., Sanchez, A.J., Erickson, B.R., Basak, A., Chretien, M., Seidah, N.G., and Nichol, S.T. (2003). Crimean-Congo hemorrhagic fever virus glycoprotein proteolytic processing by subtilase SKI-1. J. Virol. 77, 8640-8649.
56. Yang, T., Espenshade, P.J., Wright, M.E., Yabe, D., Gong, Y., Aebersold, R., Goldstein, J.L., and Brown, M.S. (2002). Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110, 489-500.
57. Ye, J., Rawson, R.B., Komuro, R., Chen, X., Dave, U.P., Prywes, R., Brown, M.S., and Goldstein, J.L. (2000). ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6, 1355-1364.
58. Zhang, K. and Kaufman, R.J. (2006). The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66, S102-S109.
59. Zheng, M., Seidah, N.G., and Pintar, J.E. (1997). The developmental expression in the rat CNS and peripheral tissues of proteases PC5 and PACE4 mRNAs: comparison with other proprotein processing enzymes. Dev. Biol. 181, 268-283.
60. Zhong, M., Munzer, J.S., Basak, A., Benjannet, S., Mowla, S.J., Decroly, E., Chretien, M., and Seidah, N.G. (1999). The prosegments of furin and PC7 as potent inhibitors of proprotein convertases. In vitro and ex vivo assessment of their efficacy and selectivity. J. Biol. Chem. 274, 33913-33920.