Propeptides are sufficient to regulate organelle-specific pH-dependent activation of furin and proprotein convertase 1/3

Journal of Molecular Biology

Volumn 423, Issue 1, 2012, Pages 47-62

  Dillon, Stephanie L ^a   Williamson, Danielle M ^a   Elferich, Johannes ^a   Radler, David ^a   Joshi, Rajendra ^b   Thomas, Gary ^a   Shinde, Ujwal ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b CENTRE FOR DEVELOPMENT OF ADVANCED COMPUTING   (India)

Author keywords

folding; molecular dynamics; pH sensor; protease activation; subtilisin

Indexed keywords

CYSTEINE; FURIN; HISTIDINE; LYSOZYME; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 3; SERINE PROTEINASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CELL ORGANELLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME INHIBITION; EUKARYOTE; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR DYNAMICS; PH; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTEIN UNFOLDING; PROTON TRANSPORT; SPECTROSCOPY;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 84866331827     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.06.023     Document Type: Article

References (70)

1. N.G. Seidah The proprotein convertases, 20 years later Methods Mol. Biol. 768 2011 23 57
2. N.G. Seidah What lies ahead for the proprotein convertases? Ann. N.Y. Acad. Sci. 1220 2011 149 161
3. G. Thomas Furin at the cutting edge: from protein traffic to embryogenesis and disease Nat. Rev. Mol. Cell Biol. 3 2002 753 766
4. 2 +-dependent serine protease Proc. Natl Acad. Sci. USA 86 1989 1434 1438 (Pubitemid 19078923)
5. R.S. Fuller, A.J. Brake, and J. Thorner Intracellular targeting and structural conservation of a prohormone-processing endoprotease Science 246 1989 482 486 (Pubitemid 19273935)
6. R.S. Fuller, R.E. Sterne, and J. Thorner Enzymes required for yeast prohormone processing Annu. Rev. Physiol. 50 1988 345 362 (Pubitemid 18088109)
7. G. Thomas, B.A. Thorne, L. Thomas, R.G. Allen, D.E. Hruby, R. Fuller, and J. Thorner Yeast KEX2 endopeptidase correctly cleaves a neuroendocrine prohormone in mammalian cells Science 241 1988 226 230
8. N.G. Seidah, S.J. Mowla, J. Hamelin, A.M. Mamarbachi, S. Benjannet, and B.B. Toure 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 1999 1321 1326 (Pubitemid 29098449)
9. B.B. Toure, J.S. Munzer, A. Basak, S. Benjannet, J. Rochemont, and C. Lazure Biosynthesis and enzymatic characterization of human SKI-1/S1P and the processing of its inhibitory prosegment J. Biol. Chem. 275 2000 2349 2358 (Pubitemid 30081992)
10. N.G. Seidah, S. Benjannet, L. Wickham, J. Marcinkiewicz, S.B. Jasmin, and S. Stifani The secretory proprotein convertase neural apoptosis-regulated convertase 1 (NARC-1): liver regeneration and neuronal differentiation Proc. Natl Acad. Sci. USA 100 2003 928 933 (Pubitemid 36183932)
11. N.G. Seidah, G. Mayer, A. Zaid, E. Rousselet, N. Nassoury, and S. Poirier The activation and physiological functions of the proprotein convertases Int. J. Biochem. Cell Biol. 40 2008 1111 1125
12. S. Henrich, A. Cameron, G.P. Bourenkov, R. Kiefersauer, R. Huber, and I. Lindberg The crystal structure of the proprotein processing proteinase furin explains its stringent specificity Nat. Struct. Biol. 10 2003 520 526 (Pubitemid 36792902)
13. T. Holyoak, M.A. Wilson, T.D. Fenn, C.A. Kettner, G.A. Petsko, R.S. Fuller, and D. Ringe 2.4 Å resolution crystal structure of the prototypical hormone-processing protease Kex2 in complex with an Ala-Lys-Arg boronic acid inhibitor Biochemistry 42 2003 6709 6718 (Pubitemid 36666111)
14. S. Henrich, I. Lindberg, W. Bode, and M.E. Than Proprotein convertase models based on the crystal structures of furin and kexin: explanation of their specificity J. Mol. Biol. 345 2005 211 227 (Pubitemid 39574845)
15. T. Holyoak, C.A. Kettner, G.A. Petsko, R.S. Fuller, and D. Ringe Structural basis for differences in substrate selectivity in Kex2 and furin protein convertases Biochemistry 43 2004 2412 2421 (Pubitemid 38327836)
16. F. Bard, and V. Malhotra The formation of TGN-to-plasma-membrane transport carriers Annu. Rev. Cell Dev. Biol. 22 2006 439 455
17. U. Shinde, and G. Thomas Insights from bacterial subtilases into the mechanisms of intramolecular chaperone-mediated activation of furin Methods Mol. Biol. 768 2011 59 106
18. D.E. Bassi, H. Mahloogi, R. Lopez De Cicco, and A. Klein-Szanto Increased furin activity enhances the malignant phenotype of human head and neck cancer cells Am. J. Pathol. 162 2003 439 447 (Pubitemid 36267851)
19. D.E. Bassi, H. Mahloogi, and A.J. Klein-Szanto The proprotein convertases furin and PACE4 play a significant role in tumor progression Mol. Carcinog. 28 2000 63 69 (Pubitemid 30432473)
20. H. Choquet, P. Stijnen, and J.W. Creemers Genetic and functional characterization of PCSK1 Methods Mol. Biol. 768 2011 247 253
21. M. Benzinou, J.W. Creemers, H. Choquet, S. Lobbens, C. Dina, and E. Durand Common nonsynonymous variants in PCSK1 confer risk of obesity Nat. Genet. 40 2008 943 945
22. D.F. Steiner, Y. Rouille, Q. Gong, S. Martin, R. Carroll, and S.J. Chan The role of prohormone convertases in insulin biosynthesis: evidence for inherited defects in their action in man and experimental animals Diabetes Metab. 22 1996 94 104
23. G.B. Ehret, P.B. Munroe, K.M. Rice, M. Bochud, A.D. Johnson, and D.I. Chasman Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk Nature 478 2011 103 109
24. D.E. Bassi, R. Lopez De Cicco, H. Mahloogi, S. Zucker, G. Thomas, and A.J. Klein-Szanto Furin inhibition results in absent or decreased invasiveness and tumorigenicity of human cancer cells Proc. Natl Acad. Sci. USA 98 2001 10326 10331 (Pubitemid 32803019)
25. E.D. Anderson, J.K. VanSlyke, C.D. Thulin, F. Jean, and G. Thomas Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage EMBO J. 16 1997 1508 1518 (Pubitemid 27151946)
26. M. Inouye Intramolecular chaperone: the role of the pro-peptide in protein folding Enzyme 45 1991 314 321
27. S.S. Jaswal, J.L. Sohl, J.H. Davis, and D.A. Agard Energetic landscape of alpha-lytic protease optimizes longevity through kinetic stability Nature 415 2002 343 346 (Pubitemid 34087558)
28. E.D. Anderson, S.S. Molloy, F. Jean, H. Fei, S. Shimamura, and G. Thomas The ordered and compartment-specfific autoproteolytic removal of the furin intramolecular chaperone is required for enzyme activation J. Biol. Chem. 277 2002 12879 12890 (Pubitemid 34952654)
29. S.F. Feliciangeli, L. Thomas, G.K. Scott, E. Subbian, C.H. Hung, and S.S. Molloy Identification of a pH sensor in the furin propeptide that regulates enzyme activation J. Biol. Chem. 281 2006 16108 16116 (Pubitemid 43848506)
30. U. Shinde, and M. Inouye Intramolecular chaperones: polypeptide extensions that modulate protein folding Semin. Cell Dev. Biol. 11 2000 35 44 (Pubitemid 32096092)
31. R.J. Siezen Subtilases: subtilisin-like serine proteases Adv. Exp. Med. Biol. 379 1996 75 93 (Pubitemid 126729191)
32. R.J. Siezen, J.W. Creemers, and W.J. Van de Ven Homology modelling of the catalytic domain of human furin. A model for the eukaryotic subtilisin-like proprotein convertases. Eur. J. Biochem. 222 1994 255 266 (Pubitemid 24204894)
33. R.J. Siezen, and J.A. Leunissen Subtilases: the superfamily of subtilisin-like serine proteases Protein Sci. 6 1997 501 523 (Pubitemid 27120048)
34. E. Subbian, Y. Yabuta, and U. Shinde Positive selection dictates the choice between kinetic and thermodynamic protein folding and stability in subtilases Biochemistry 43 2004 14348 14360 (Pubitemid 39491969)
35. E. Subbian, Y. Yabuta, and U.P. Shinde Folding pathway mediated by an intramolecular chaperone: intrinsically unstructured propeptide modulates stochastic activation of subtilisin J. Mol. Biol. 347 2005 367 383 (Pubitemid 40312465)
36. E.L. Cunningham, S.S. Jaswal, J.L. Sohl, and D.A. Agard Kinetic stability as a mechanism for protease longevity Proc. Natl Acad. Sci. USA 96 1999 11008 11014 (Pubitemid 29487319)
37. J.L. Sohl, S.S. Jaswal, and D.A. Agard Unfolded conformations of alpha-lytic protease are more stable than its native state Nature 395 1998 817 819 (Pubitemid 28485451)
38. S.M. Truhlar, E.L. Cunningham, and D.A. Agard The folding landscape of Streptomyces griseus protease B reveals the energetic costs and benefits associated with evolving kinetic stability Protein Sci. 13 2004 381 390 (Pubitemid 38124959)
39. K. Nakayama Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins Biochem. J. 327 1997 625 635 (Pubitemid 27487665)
40. J.R. Casey, S. Grinstein, and J. Orlowski Sensors and regulators of intracellular pH Nat. Rev. Mol. Cell Biol. 11 2010 50 61
41. T.M. Embley, and W. Martin Eukaryotic evolution, changes and challenges Nature 440 2006 623 630
42. M. Soskine, and D.S. Tawfik Mutational effects and the evolution of new protein functions Nat. Rev. Genet. 11 2010 572 582
43. C. Marie-Claire, Y. Yabuta, K. Suefuji, H. Matsuzawa, and U. Shinde Folding pathway mediated by an intramolecular chaperone: the structural and functional characterization of the aqualysin I propeptide J. Mol. Biol. 305 2001 151 165 (Pubitemid 32039752)
44. U. Shinde, and G. Thomas Insights from bacterial subtilases into the mechanisms of intramolecular chaperone mediated activation of furin Methods Mol. Biol. 768 2011 59 106
45. Y.J. Chen, and M. Inouye The intramolecular chaperone-mediated protein folding Curr. Opin. Struct. Biol. 18 2008 765 770
46. U. Shinde, and M. Inouye Intramolecular chaperones and protein folding Trends Biochem. Sci. 18 1993 442 446 (Pubitemid 23316630)
47. S.C. Jain, U. Shinde, Y. Li, M. Inouye, and H.M. Berman The crystal structure of an autoprocessed Ser221Cys-subtilisin E-propeptide complex at 2.0 Å resolution J. Mol. Biol. 284 1998 137 144 (Pubitemid 28524002)
48. U. Shinde, Y. Li, S. Chatterjee, and M. Inouye Folding pathway mediated by an intramolecular chaperone Proc. Natl Acad. Sci. USA 90 1993 6924 6928 (Pubitemid 23222360)
49. S. Bhattacharjya, P. Xu, H. Xiang, M. Chretien, N.G. Seidah, and F. Ni pH-induced conformational transitions of a molten-globule-like state of the inhibitory prodomain of furin: implications for zymogen activation Protein Sci. 10 2001 934 942 (Pubitemid 32367484)
50. A.L. Fink, L.J. Calciano, Y. Goto, T. Kurotsu, and D.R. Palleros Classification of acid denaturation of proteins: intermediates and unfolded states Biochemistry 33 1994 12504 12511 (Pubitemid 24340457)
51. Y. Goto, L.J. Calciano, and A.L. Fink Acid-induced folding of proteins Proc. Natl Acad. Sci. USA 87 1990 573 577
52. V.N. Uversky, and Y. Goto Acid denaturation and anion-induced folding of globular proteins: multitude of equilibium partially folded intermediates Curr. Protein Pept. Sci. 10 2009 447 455
53. P.E. Wright, and H.J. Dyson Linking folding and binding Curr. Opin. Struct. Biol. 19 2009 31 38
54. M.J. Gething, K. McCammon, and J. Sambrook Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport Cell 46 1986 939 950 (Pubitemid 16027942)
55. S.S. Molloy, L. Thomas, J.K. VanSlyke, P.E. Stenberg, and G. Thomas Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface EMBO J. 13 1994 18 33
56. S. Munro, and H.R. Pelham A C-terminal signal prevents secretion of luminal ER proteins Cell 48 1987 899 907
57. M. Karplus, and J. Kuriyan Molecular dynamics and protein function Proc. Natl Acad. Sci. USA 102 2005 6679 6685 (Pubitemid 40675376)
58. V. Daggett, and M. Levitt A model of the molten globule state from molecular dynamics simulations Proc. Natl Acad. Sci. USA 89 1992 5142 5146
59. V. Daggett, and M. Levitt Protein unfolding pathways explored through molecular dynamics simulations J. Mol. Biol. 232 1993 600 619 (Pubitemid 23251182)
60. C.L. Brooks III Characterization of native apomyoglobin by molecular dynamics simulation J. Mol. Biol. 227 1992 375 380
61. N.L. Salimi, B. Ho, and D.A. Agard Unfolding simulations reveal the mechanism of extreme unfolding cooperativity in the kinetically stable alpha-lytic protease PLoS Comput. Biol. 6 2010 e1000689
62. W. Huang, A.P. Eichenberger, and W.F. van Gunsteren Molecular dynamics simulation of thionated hen egg white lysozyme Protein Sci. 21 2012 1153 1161
63. I.S. Povolotskaya, and F.A. Kondrashov Sequence space and the ongoing expansion of the protein universe Nature 465 2010 922 926
64. X. Fu, M. Inouye, and U. Shinde Folding pathway mediated by an intramolecular chaperone. The inhibitory and chaperone functions of the subtilisin propeptide are not obligatorily linked J. Biol. Chem. 275 2000 16871 16878 (Pubitemid 30398923)
65. S. Benjannet, N. Rondeau, R. Day, M. Chretien, and N.G. Seidah PC1 and PC2 are proprotein convertases capable of cleaving proopiomelanocortin at distinct pairs of basic residues Proc. Natl Acad. Sci. USA 88 1991 3564 3568 (Pubitemid 21916663)
66. N.J. Greenfield Using circular dichroism spectra to estimate protein secondary structure Nat. Protoc. 1 2006 2876 2890
67. M.A. Tangrea, P.N. Bryan, N. Sari, and J. Orban Solution structure of the pro-hormone convertase 1 pro-domain from Mus musculus J. Mol. Biol. 320 2002 801 812 (Pubitemid 34729406)
68. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, and E. Villa Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
69. B.R. Brooks, C.L. Brooks III, A.D. Mackerell Jr, L. Nilsson, R.J. Petrella, and B. Roux CHARMM: the biomolecular simulation program J. Comput. Chem. 30 2009 1545 1614
70. B. Roux, B. Prod'hom, and M. Karplus Ion transport in the gramicidin channel: molecular dynamics study of single and double occupancy Biophys. J. 68 1995 876 892