Small-intestinal dysfunction accompanies the complex endocrinopathy of human proprotein convertase 1 deficiency

Journal of Clinical Investigation

Volumn 112, Issue 10, 2003, Pages 1550-1560

  Jackson, Robert S ^a   Creemers, John W M ^b   Farooqi, I Sadaf ^c   Raffin Sanson, Marie Laure ^d   Varro, Andrea ^e   Dockray, Graham J ^e   Holst, Jens J ^f   Brubaker, Patricia L ^g   Corvol, Pierre ^h   Polonsky, Kenneth S ⁱ   Ostrega, Diane ^j   Becker, Kenneth L ^k   Bertagna, Xavier ^d   Hutton, John C ^l   White, Anne ^m   Dattani, Mehul T ⁿ   Hussain, Khalid ⁿ   Middleton, Stephen J ^o   Nicole, Thomasina M ^p   Milla, Peter J ⁿ   Lindley, Keith J ⁿ   O'Rahilly, Stephen ^c,o   more..

^a EAST SURREY HOSPITAL   (United Kingdom)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d CNRS   (France)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g UNIVERSITY OF TORONTO   (Canada)

^h PSL Research University   (France)

ⁱ WASHINGTON UNIVERSITY   (United States)

^j UNIVERSITY OF CHICAGO   (United States)

^k GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^l UNIVERSITY OF COLORADO DENVER   (United States)

^m UNIVERSITY OF MANCHESTER   (United Kingdom)

ⁿ UNIVERSITY COLLEGE LONDON   (United Kingdom)

^o ADDENBROOKE S HOSPITAL   (United Kingdom)

^p YEOVIL DISTRICT HOSPITAL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN; GLUCAGON; HORMONE PRECURSOR; PROPROTEIN CONVERTASE 1; UNCLASSIFIED DRUG;

ADRENAL DISEASE; ADULT; ALLELISM; ARTICLE; CASE REPORT; CATALYSIS; CLINICAL FEATURE; DIARRHEA; DISEASE ASSOCIATION; DISEASE SEVERITY; ENDOCRINE DISEASE; ENZYME DEFICIENCY; HETEROZYGOSITY; HUMAN; HUMAN CELL; HYPOADRENALISM; HYPOGLYCEMIA; HYPOGONADISM; MALABSORPTION; MISSENSE MUTATION; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROPROTEIN CONVERTASE 1 DEFICIENCY; SMALL INTESTINE DISEASE;

EID: 0346096721     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200318784     Document Type: Article

References (58)

1. Wilson, H.E., and White, A. 1998. Prohormones: their clinical relevance. Trends Endocrinol. Metab. 9:396-402.
2. Steiner, D. 1998. The proprotein convertases. Curr. Opin. Chem. Biol. 2:31-39.
3. Rouille, Y., et al. 1995. Proteolytic processing mechanisms in the biosynthesis of neuroendocrine peptides: the subtilisin-like proprotein convertases. Front. Neuroendocrinol. 16:322-361.
4. Bertagna, X. 1994. Proopiomelanocortin-derived peptides. Endocrinol. Metab. Clin. North Am. 23:467-485.
5. Dhanvantari, S., Seidah, N.G., and Brubaker, P.L. 1996. Role of prohormone convertases in the tissue-specific processing of proglucagon. Mol. Endocrinol. 10:342-355.
6. Rouille, Y., Kantengwa, S., Irminger, J.C., and Halban, P.A. 1997. Role of the prohormone convertase PC3 in the processing of proglucagon to glucagon-like peptide 1. J. Biol. Chem. 272:32810-32816.
7. Furuta, M., et al. 1997. Defective prohormone processing and altered pancreatic islet morphology in mice lacking active PC2. Proc. Natl. Acad. Sci. U. S. A. 94:6646-6651.
8. Zhu, X., et al. 2002. Disruption of PC1/3 expression in mice causes dwarfism and multiple neuroendocrine peptide processing defects. Proc. Natl. Acad. Sci. U. S. A. 99:10293-10298.
9. O'Rahilly, S., et al. 1995. Impaired processing of prohormones associated with abnormalities of glucose homeostasis and adrenal function. N. Engl. J. Med. 23:1386-1390.
10. Jackson, R.S., et al. 1997. Obesity and impaired prohormone processing associated with mutations in the human prohormone convertase 1 gene. Nat. Genet. 16:303-306.
11. Creemers, J.W., van de Loo, J.W., Plets, E., Hendershot, L.M., and Van De Ven, W.J. 2000. Binding of BiP to the processing enzyme lymphoma proprotein convertase prevents aggregation, but slows down maturation. J. Biol. Chem 275:38842-38847.
12. Creemers, J.W.M., Bailyes, E.M., Lindberg, I., and Hutton, J.C. 1999. Proteolytic processing. In Post-translational processing: a practical approach. B.D. Hames and S.J. Higgins, editors. Oxford University Press. Oxford, United Kingdom. 205-223
13. Damholt, A.B., Buchan, A.M., Holst, J.J., and Kofod, H. 1999. Proglucagon processing profile in canine L cells expressing endogenous prohormone convertase 1/3 and prohormone convertase 2. Endocrinology. 140:4800-4808.
14. Holst, J.J., et al. 1994. Proglucagon processing in porcine and human pancreas. J. Biol. Chem. 269:18827-18833.
15. Varro, A., et al. 1997. Gastrin biosynthesis in the antrum of patients with pernicious anaemia. Gastroenterology. 112:733-741.
16. Dockray, G.J., and Taylor, I.L. 1976. Heptadecapeptide gastrin: measurement in blood by specific radioimmunoassay. Gastroenterology. 71:971-977.
17. Dockray, G.J., and Walsh, J.H. 1975. Amino terminal gastrin fragment in serum of Zollinger-Ellison syndrome patients. Gastroenterology. 68:222-230
18. Laudat, M.H., et al. 1987. The hormonal state of pregnancy: modification of cortisol and testosterone. Ann. Endocrinol. (Paris) 48:334-338.
19. Raffin-Sanson, M.L., et al. 1996. High plasma proopiomelanocortin in aggressive adrenocorticotropin-secreting tumors. J. Clin. Endocrinol. Metab. 81:4272-4277.
20. Massias, J.F., Hardouin, S., Vieau, D., Lenne, F., and Bertagna, X. 1994. Phosphorylated forms of adrenocorticotropin and corticotropin-like intermediary lobe peptide in human tumors. Eur. J. Endocrinol. 131:341-346.
21. Crosby, S.R., Stewart, M.F., Ratcliffe, J.G., and White, A. 1988. Direct measurement of the precursors of adrenocorticotropin in human plasma by two-site immunoradiometric assay. J. Clin. Endocrinol. 67:1272-1277.
22. Whang, K.T., et al. 1998. Serum calcitonin precursors in sepsis and systemic inflammation. J. Clin. Endocrinol. Metab. 83:3296-3301.
23. Snider, R.H., Nylen, E.S., and Becker, K.L. 1997. Procalcitonin and its component peptides in systemic inflammation: immunochemical characterization. J. Investig. Med. 45:552-560.
24. Simon, D., et al. 1987. Measurement of active renin by the 4G1 antihuman renin monoclonal antibody. Clin. Exp. Hypertens. A. 9:1333-1340.
25. Sealey, J.E., Atlas, S.A., Laragh, J.H., Oza, N.B., and Ryan, J.W. 1979. Activation of a prorenin-like substance in human plasma by trypsin and by urinary kallikrein. Hypertension. 1:179-189.
26. Hutton, J.C. 1994. Insulin secretory granule biogenesis and the proinsulin-processing endopeptidases. Diabetologia. 37(Suppl. 2):S48-S56.
27. Nemeth, J., Varro, A., Bridson, J., Walker, R., and Dockray, G.J. 1992. Increased tissue concentrations of the gastrin precursor in patients treated with omeprazole. Eur. J. Clin. Invest. 22:638-644.
28. Zhou, Y., and Lindberg, I. 1994. Enzymatic properties of carboxyl-terminally truncated prohormone convertase 1 (PC1/SPC3) and evidence for autocatalytic conversion. J. Biol. Chem. 269:18408-18413.
29. Zhou, Y., and Lindberg, I. 1993. Purification and characterization of the prohormone convertase PC1(PC3) J. Biol. Chem. 268:5615-5623
30. Anderson, E.D., VanSlyke, J.K. Thulin, C.D., Jean, F., and Thomas, G. 1997. Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage. EMBO J. 16:1508-1518.
31. Anderson, E.D., et al. 2002. The ordered and compartment-specific autoproteolytic removal of the furin intramolecular chaperone is required for enzyme activation. J. Biol. Chem. 277:12879-12890.
32. Boudreault, A., Gauthier, D., and Lazure, C. 1998. Proprotein convertase PC1/3-related peptides are potent slow tight-binding inhibitors of murine PC1/3 and H furin. J. Biol. Chem. 273:31574-31580.
33. Zhou, A., Bloomquist, B.T., and Mains, R.E. 1993. The prohormone convertases PC1 and PC2 mediate distinct endoproteolytic cleavages in a strict temporal order during proopiomelanocortin biosynthetic processing. J. Biol. Chem. 268:1763-1769.
34. Scopsi, L., Gullo, M., Rilke, F., Martin, S., and Steiner, D.F. 1995. Proprotein convertases (PC1/PC3 and PC2) in normal and neoplastic human tissues: their use as markers of neuroendocrine differentiation. J. Clin. Endocrinol. Metab. 80:294-301.
35. Drucker, D.J. 1998. Glucagon-like peptides. Diabetes. 47:159-169.
36. Lusson, J., et al. 1993. cDNA structure of the mouse and rat subtilisin/kexin-like PC5: a candidate proprotein convertase expressed in endocrine and non-endocrine cells. Proc. Natl. Acad Sci. U. S. A. 90:6691-6695.
37. Dong, W., et al. 1995. Distinct mRNA expression of the highly homologous convertases PC5 and PACE4 in the rat brain and pituitary. J. Neurosci. 15:1778-1796.
38. Seidah, N.G., Chretien, M., and Day, R., 1994. The family of subtilisin/kexin like pro-protein and pro-hormone convertases: divergent or shared functions. Biochimie 76:197-209.
39. Furuta, M., et al. 1997. Defective prohormone processing and altered pancreatic islet morphology in mice lacking active SPC2. Proc. Natl. Acad. Sci. U. S. A. 94:6646-6651.
40. Zhu, X, et al. 2002. Severe block in processing of proinsulin to insulin accompanied by elevation of des-64,65 proinsulin intermediates in islets of mice lacking prohormone convertase 1/3. Proc. Natl. Acad. Sci. U. S. A. 99:10299-10304.
41. Molloy, S.S., Thomas, L., Van Slyke, J.K., Sternberg, P.E., and Thomas, G. 1994. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J. 13:18-33.
42. Creemers, J.W., et al. 1995. Endoproteolytic cleavage of its propeptide is a prerequisite for efficient transport of furin out of the endoplasmic reticulum. J. Biol. Chem. 270:2695-2702.
43. van de Loo, J.W., et al. 1997. Biosynthesis, distinct post-translational modifications, and functional characterization of lymphoma proprotein convertase. J. Biol. Chem. 272:27116-27123.
44. Creemers, J.W., et al. 1993. Modulation of furin-mediated proprotein processing activity by site-directed mutagenesis. J. Biol. Chem. 268:21826-21834
45. Henrich, S., et al. 2003. The crystal structure of the proprotein processing proteinase furin explains its stringent specificity. Nat. Struct. Biol. 10:520-526.
46. Holyoak, T., et al. 2003. 2.4 A resolution crystal structure of the prototypical hormone-processing protease Kex2 in complex with an Ala-Lys-Arg boronic acid inhibitor. Biochemistry. 42:6709-6718.
47. Ueda, K., et al. 2003. Mutational analysis of predicted interactions between the catalytic and P domains of prohormone convertase 3 (PC3/PC1). Proc. Natl. Acad. Sci. U. S. A. 100:5622-5627.
48. Siezen, R.J., Creemers, J.W., and Van de Ven, W.J. 1994. Homology modelling of the catalytic domain of human furin A model for the eukaryotic subtilisin-like proprotein convertases. Eur. J. Biochem. 222:255-266.
49. Lipkind, G., Gong, Q., and Steiner, D.F. 1995. Molecular modeling of the substrate specificity of prohormone convertases SPC2 and SPC3. J. Biol. Chem. 270:13277-13284.
50. Fewell, S.W., Travers, K.J., Weissman, J.S., and Brodsky, J.L. 2001. The action of molecular chaperones in the early secretory pathway. Annu. Rev. Genet. 35:149-191.
51. Yaswen, L., Diehl, N., Brennan, M.B., and Hochgeschwender, U. 1999. Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin. Nat. Med. 5:984-985.
52. Loh, Y.P., Parrish, D.C., and Tuteja, R. 1985. Purification and characterization of a paired basic residue-specific pro-opiomelanocortin converting enzyme from bovine pituitary intermediate lobe secretory vesicles. J. Biol. Chem. 260:7194-7205.
53. Loh, Y.P., and Cawley, N.X. 1995. Processing enzymes of pepsin family: yeast aspartic protease 3 and pro-opiomelanocortin converting enzyme. Methods Enzymol. 248:136-146
54. Mains, R.E., et al. 1997. PACE4: a subtilisin-like endoprotease with unique properties. Biochem. J. 321:587-593.
55. Seidah, N.G., et al. 1999. The subtilisin/kexin family of precursor convertases. Emphasis on PC1, PC2/7B2, POMC and the novel enzyme SKI-1. Ann. N. Y. Acad. Sci. 885:57-74.
56. Jutras, I., Seidah, N.G., Reudelhuber, T.L., and Brechler, V. 1997. Two activation states of the prohormone convertase PC1 in the secretory pathway. J. Biol. Chem. 272:15184-15188.
57. Mercure, C., Jutras, I., Day, R., Seidah, N.G., and Reudelhuber, T.L. 1996. Prohormone convertase PC5 is a candidate processing enzyme for prorenin in the human adrenal cortex. Hypertension. 28:840-846.
58. Nakagawa, T., et al. 1993. Identification and functional expression of a new member of the mammalian kex-2 like processing endoprotease family: its striking structural similarity to PACE 4. J. Biochem. (Tokyo). 113:132-135.