Mechanism of the facilitation of PC2 maturation by 7B2: Involvement in ProPC2 transport and activation but not folding

Journal of Cell Biology

Volumn 139, Issue 3, 1997, Pages 625-638

  Muller, Laurent ^a   Zhu, Xiaorong ^a   Lindberg, Iris ^a  

^a LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE PRECURSOR;

ACETYLATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL MATURATION; COMPLEX FORMATION; ENZYME ACTIVATION; FACILITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CELL LINE; CHO CELLS; CRICETINAE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HYDROGEN-ION CONCENTRATION; NERVE TISSUE PROTEINS; NEUROENDOCRINE SECRETORY PROTEIN 7B2; NEUROSECRETORY SYSTEMS; PITUITARY HORMONES; PROPROTEIN CONVERTASE 2; PROTEIN BINDING; PROTEIN FOLDING; SUBCELLULAR FRACTIONS; SUBTILISINS;

EID: 0030716779     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.3.625     Document Type: Article

References (72)

1. Ayoubi, T.A.Y., H.L.P. van Duijnhoven, W.J.M. van de Ven, B.G. Jenks, E.W. Roubos, and G.J.M. Martens. 1990. The neuroendocrine polypeptide 7B2 is a precursor protein. J. Biol. Chem. 265:15644-15647.
2. Baeuerle, P.A., and W.B. Huttner. 1987. Tyrosine sulfation is a trans-Golgi-specific protein modification. J. Cell Biol. 105:2655-2664.
3. Benjannet, S., N. Rondeau., L. Paquet, A. Boudreault, C. Lazure, M. Chretien, and N.G. Siedah. 1993. Comparative biosynthesis, glycosylation, and efficiency of prosegment cleavage of the prohormone convertases PC1 and PC2. Biochem. J. 294:735-743.
4. Benjannet, S., D. Savaria, M. Chretien, and N.G. Seidah. 1995. 7B2 is a specific intracellular binding protein of the prohormone convertase PC2. J. Neuroehem. 64:2303-2311.
5. Bennett, D.L., E.M. Bailyes, E. Nielsen, P.C. Guest, N.G. Rutherford, S.D. Arden, and J.C. Hutton. 1992. Identification of the type 2 proinsulin processing endopeptidase as PC2, a member of the eukaryotic subtilisin family. J. Biol. Chem. 267:15229-15236.
6. Bowman, E.J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA. 85:7972-7976.
7. Braakman, I., J. Helenius, and A. Helenius. 1992. Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO (Eur. Mol. Biol. Organ.) J. 11:1717-1722.
8. Braks, J.A.M., and G.J.M. Martens. 1994. 7B2 is a neuroendocrine chaperone that transiently interacts with prohormone convertase PC2 in the secretory pathway. Cell. 78:263-273.
9. Braks, J.A.M., and G.J.M. Martens. 1995. The neuroendocrine chaperone 7B2 can enhance in vitro POMC cleavage by prohormone convertase PC2. FEBS (Fed. Eur. Biochem. Soc.) Lett. 371:154-158.
10. Braks, J.A.M., A.M. Van Horssen, and G.J.M. Martens. 1996. Dissociation of the complex between the neuroendocrine chaperone 7B2 and prohormone convertase PC2 is not associated with proPC2 maturation. Eur. J. Biochem. 238:505-510.
11. Bresnahan, P.A., R. Leduc, L. Thomas, J. Thorner, H.L. Gibson, A.J. Brake, P.J. Barr. and G. Thomas. 1990. Human fur gene encodes a yeast KEX2-like endoprotease that cleaves pro-beta-NGF in vivo. J. Cell Biol. 111:2851-2859.
12. Bu, G., and S. Rennke. 1996. Receptor-associated protein is a folding chaperone for low density lipoprolein receptor-related protein. J. Biol. Chem. 271: 22218-22224.
13. Chaney, W., S. Sundaram, N. Friedman, and P. Stanely. 1989. The Lec4A CHO glvcosylation mutant arises from miscompartmentalization of a Golgi glycosyitransferase. J. Cell Biol. 109:2089-2096.
14. Creemcrs, J.W., E.F. Usac, N.A. Bright, J.W. Van de Loo, E. Jansen, W.J.M. Van de Ven, and J.C. Hutton. 1996. Identification of a transferable sorting domain for the regulated pathway in the prohormone convertase PC2. J. Biol. Chem. 271:25284-25291.
15. De Bie, I., M. Marcinkiewicz, D. Malide, C. Lazure, K. Nakayama, M. Bendayan, and N.G. Seidah. 1996. The isoforms of proprotein convertase PC5 are sorted to different subcellular compartments. J. Cell Biol. 135:1261-1275.
16. Feng, W., J.R. Huth, S.E. Norton, and R.W. Ruddon. 1995. Asparagine-linked oligosaccharides facilitate human chorionic gonadotropin β-subunit folding but not assembly of prefolded β with α. Endocrinology. 138:52-61.
17. Gething, M.J., and J. Sambrook. 1992. Protein folding in the cell. Nature (Lond.). 355:33-45.
18. Guest, P.C., S.D. Arden, D.L. Bennett, A. Clark, N.G. Rutherford, and J.C. Hutton. 1992. The post-translational processing and intracellular sorting of PC2 in the islets of Langerhans. J. Biol. Chem. 267:22401-22406.
19. Hamond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
20. Hartl, F.U. 1996. Molecular chaperones in cellular protein folding. Nature (Lond.). 381:571-580.
21. Hatsuzawa, K., M. Hosaka, T. Nakagawa, M. Nagase, A. Shoda, K. Murakami, and K. Nakayama. 1990. Structure and expression of mouse furin, a yeast Kex2 related protease. Lack of processing of coexpressed prorenin in GH4C1 cells. J. Biol. Chem. 265:22075-22078.
22. Hatsuzawa, K., M. Nagahama, K Takahashi, K. Takada. K. Murakami, and K. Nakayama. 1992. Purification and characterization of furin, a Kex2-like processing endoprotease, produced in Chinese hamster ovary cells. J. Biol. Chem. 1267:16094-16099.
23. Helenius, A. 1994. How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticlum. Mol. Biol. Cell. 5:253-265.
24. Hendrick, J.P., and F.U. Hartl. 1993. Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62:349-384.
25. Hsi, K.L., N.G. Seidah, G. De Serres, and M. Chretien. 1982. Isolation and NH2-terminal sequence of a novel porcine anterior pituitary polypeptide. Homology to proinsulin, secretin and Rous sarcoma virus transforming protein TVFV60. FEBS (Fed. Eur. Biochem. Soc.) Lett. 147:261-266.
26. Hurtley, S.M., and A. Helenius. 1989. Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:277-307.
27. Kelly, R.B. 1985. Pathways of protein secretion in eukaryotes. Science (Wash. DC). 230:25-32.
28. Kiefer, M.C., J.E. Tucker, R. Joh, K.E. Landsberg, D. Saltman, and P.J. Barr. 1991. Identification of a second human subtilisin-like protease gene in the fes/fps region of chromosome 15. DNA Cell Biol. 10:757-769.
29. Kim, P.S., O.Y. Kwon, and P. Arvan. 1996. An endoplasmic reticulum storage disease causing congenital goiter with hypothyroidism. J. Cell Biol. 133:517-527.
30. Klausner, R.D., J.G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
31. Lamango, N.S., X. Zhu, and I. Lindberg. 1996. Purification and enzymatic characterization of recombinant prohormone convertase 2: stabilization of activity by 21 kD 7B2. Arch. Biochem. Biophys. 330:238-250.
32. Lindberg, I. 1994. Evidence for the cleavage of the PC1/PC3 prosegment in the endoplasmic reticulum. Mol. Cell. Neurosci. 5:263-268.
33. Lindberg, I., W.H. Van den Hurk, C. Bui, and C.J. Batie. 1995. Enzymatic characterization of immunopurified prohormone convertase 2. Potent inhibition by a 7B2 peptide fragment. Biochemistry. 34:5486-5493.
34. Lodish, H.F. 1988. Transport of secretory and membrane glycoproteins from the rough endoplasmic reticulum to the Golgi. A rate-limiting step in protein maturation and secretion. J. Biol. Chem. 263:2107-2110.
35. Lodish, H.F., and N. Kong. 1993. The secretory pathway is normal in dithiothreitol-treated cells, but disulfide-bonded proteins are reduced and reversibly retained in the endoplasmic reliculum. J. Biol. Chem. 268:20598-20605.
36. Mains, R.E., S.L. Milgram, H.T. Keutman, and B.A. Eipper. 1995. The NH2-terminal proregion of peptidylglycine alpha-amidating monooxygenase facilitates the secretion of soluble proteins. Mol. Endocrinol. 9:3-13.
37. Martens, G.J., M.J. Bussemakers, and B.G. Jenks. 1989. The novel pituitary polypeptide 7B2 is a highly-conserved protein coexpressed with proopiomelanoconin. Eur. J. Biochem. 181:75-79.
38. Martens, G.J.M., J.A.M. Braks, D.W. Eib, Y. Zhou, and I. Lindberg. 1994. The neuroendocrine polypeptide 7B2 is an endogenous inhibitor of prohormone convertase PC2. Proc. Natl. Acad. Sci. USA. 91:5784-5787.
39. Matthews, G., K.I.J. Shennan, A.J. Seal. N.A. Taylor, A. Colman, and K. Dochcity. 1994. Autocatalytic maturation of the prohormone convertase PC2. J. Biol. Chem. 269:588-592.
40. Molloy, S.S., P.A. Bresnahan, S.H. Leppla, K.R. Klimpel, and G. Thomas. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267:16396-16402.
41. Molly, S.S., L. Thomas, J.K. Van Slyke, P.E. Stenberg, and G. Thomas. 1994. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO (Eur. Mol. Biol. Organ.) J. 13:18-33.
42. Muller, L., A. Barret, R. Picart, N.G. Seidah, and C. Tougard. 1997. Immunocytochemical localization of the prohormone convertases PC1 and PC2 in rat prolactin cells. J. Histochem. Cytochem. 45:1-8.
43. Nakayama, K., W.S. Kim, S. Torii, M. Hosaka, T. Nakagawa, J. Ikemizu, T. Baba, and K. Murakami. 1992. Identification of the fourth member of the mammalian endoprotease family homologous to the yeast Kex2 protease. J. Biol. Chem. 267:5897-5900.
44. Ou, W-J., P.H. Cameron, D.Y. Thomas, and J.J.M. Bergeron. 1993. Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature (Lond.). 364:771-776.
45. Paquet, L., N. Rondeau, N.G. Seidah, C. Lazure, M. Chretien, and M. Mbikay. 1991. Immunological identification and sequence characterization of a peptide derived from the processing of neuroendocrine protein 7B2. FEBS (Fed. Eur. Biochem. Soc.) Lett. 294:23-26.
46. Paquet, L., F. Bergeron, A. Boudreault, N.G. Seidah, M. Chretien, M. Mbikay, and C. Lazure. 1994. The neuroendocrine precursor 7B2 is a sulfated protein proteolytically processed by a ubiquitous furinlike convertase. J. Biol. Chem. 269:19279-19285.
47. Pelham, H.R. 1991. Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr. Opin. Cell Biol. 3:585-591.
48. Rothman, J.E. 1989. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell. 59:591-601.
49. Rouille, Y., S.J. Duguay, K. Lund. M. Furuta, Q. Gong, G. Lipkind, A.A. Oliva, Jr., S.J. Chan, and D.F. Steiner. 1995. Proteolytic processing mechanisms in the biosynthesis of neuroendocrine peptides: the subtilisin-like proprotein convertases. Front. Neuroendocrinol. 16:322-361.
50. Satoh, M., K. Hirayoshi, S. Yokota, N. Hosokawa, and K. Nagata. 1996. Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen. J. Cell Biol. 133:469-483.
51. Seidah, N.G., L. Gaspar, P. Mion, M. Marcinkiewicz, M. Mbikay, and M. Chretien. 1990. cDNA sequence of two distinct pituitary proteins homologous to Kex2 and furin gene products: tissue-specific mRNAs encoding candidates for pro-hormone processing proteinases. DNA Cell Biol. 9:415-424.
52. Seidah, N.G., M. Marcinkiewicz, S. Benjannet, L. Gaspar, G. Beaubien, M.G. Mattei, C. Lazure, M. Mbikay, and M. Chretien. 1991. Cloning and primary sequence of a mouse candidate prohormone convertase PC1 homologous to PC2, furin, and Kex2: distinct chromosomal localization and messenger RNA distribution in brain and pituitary compared to PC2. Mol. Endocrinol. 5:111-122.
53. Seidah, N.G., R. Day, J. Hamelin, A. Gaspar, M.W. Collard, and M. Chretien. 1992. Testicular expression of PC4 in the rat: molecular diversity of a novel germ cell-specific Kex2/subtilisin-like proprotein convertase. Mol. Endocrinol. 6:1559-1570.
54. Seidah, N.G., and M. Chretien. 1994. Pro-protein convertases of subtilisin/kexin family. Methods Enzymol. 244:171-188.
55. Shen, F.S., I. Lindberg, and N.G. Seidah. 1993. Biosynthesis of the prohormone convertase PC2 in Chinese hamster ovary cells and in rat insulinoma cells. J. Biol. Chem. 268:24910-24915.
56. Shennan, K.I.J., N.A. Taylor, J.L. Jermany, G. Matthews, and K. Docherty. 1995. Difference in pH optima and calcium requirements for maturation of the prohormone convertases PC2 and PC3 indicates different intracellular locations for these events. J. Biol. Chem. 270:1402-1407.
57. Siezen, R.J., J.W.M. Creemers, and W.J.M. Van de Ven. 1994. Homology modeling of the catalytic domain of human furin: a model for the eukaryotic subtilisin-like proprotein convertases. Eur. J. Biochem. 222:255-266.
58. Siezen, R.J., J.A.M. Leunissen, and U. Shinde. 1995. Homology analysis of the propeptides of subtilisin-like serine proteases (subtilases). In Intramolecular Chaperones and Protein Folding. U. Shinde and N. Inouye, editors. R.G. Landes Company, Austin, TX. 233-256.
59. Simons, J.F., S. Ferro-Novick, M.D. Rose, and A. Helenius. 1995. BiP/Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast. J. Cell Biol. 130:41-49.
60. Smeekens, S.P., A.S. Avruch, J. LaMendola, S.J. Chan, and D.F. Steiner. 1991. Identification of a cDNA encoding a second putative prohormone convertase related to PC2 in At20 cells and islets of Langerhans. Proc. Natl. Acad. Sci. USA. 88:340-344.
61. Umata, T., Y. Moriyama, M. Futai, and E. Mekada. 1990. The cytotoxic action of diphtheria toxin and its degradation in intact Vero cells are inhibited by bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase. J. Biol. Chem. 265:21940-21945.
62. Van Duijnhoven, H.L., M.C. Verschusen, E.D. Timmer, P.M. Vissers, A. Groeneveld, T.A. Ayoubi, A.M. Van den Ouweland, and W. J. Van de Ven. 1991. Application of recombinant DNA technology in epitope mapping and targeting. Development and characterization of a panel of monoclonal antibodies against the 7B2 neuroendocrine protein. J. lmmunol. Methods. 142: 187-198.
63. Van Horssen, A.M., W.H. Van den Hurk, E.M. Bailyes, J.C. Hutton, G.J.M. Martens, and I. Lindberg. 1995. Identification of the region within the neuroendocrine polypeptide 7B2 responsible for the inhibition of prohormone convertase PC2.J. Biol. Chem. 270:14292-14296.
64. Vey, M., W. Schafer, S. Berghofer, H.D. Klenk, and W. Garten. 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.
65. Willnow, T.E., A. Rohlman, J. Horton, H. Otani, J.R. Braun, R.E. Hammer, and J. Herz. 1496. RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytotic receptors. EMBO (Eur. Mol. Biol. Organ.) J. 15:2632-2639.
66. Yoshimori, T., A. Yamamoto, Y. Moriyama, M. Futai, and Y. Tashiro. 1991. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase. inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 266:17707-17712.
67. Zhou, Y., and I. Lindberg. 1993. Purification and characterization of the prohormone convertase PC1(PC3).J. Biol. Chem. 268:5615-5623.
68. Zhou, A., and R.E. Mains. 1994. Endoproteolytic processing of POMC and prohormone convertases 1 and 2 in neuroendocrine cells overexpressing PC1 or PC2.J. Biol. Chem. 269:17440-17447.
69. Zhu, X., Y. Ohta, F. Jordan, and M. lnouye. 1989. Proscquence of subtilisin can guide the refolding of denatured subtilisin in an intermolecular process. Nature (Lond.). 339:483-484.
70. Zhu, X., and I. Lindherg, 1995. 7B2 facilitates the maturation of proPC2 in neuroendocrine cells and is required for the expression of enzymatic activity.J. Cell Biol. 129:1641-1650.
71. Zhu, X., Y. Rouille, N.S. Lamango, D.F. Steiner, and I. Lindberg. 1996a. Internal cleavage of the inhibitory 7B2 carboxyl-terminal peptide by PC2: a potential mechanism for its inactivation. Proc. Natl. Acad. Sci. USA. 93:4919-4924.
72. Zhu, X., N.S. Lamango, and I. Lindberg. 1996b. Involvement of a polyproline helix-like structure in the interaction of 7B2 with prohormone convertase 2. J. Biol. Chem. 271:23582-23587.