Home LiteratureArticle Details
PMID: 3318807 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Proteolytic conversion of proinsulin into insulin. Identification of a Ca2+-dependent acidic endopeptidase in isolated insulin-secretory granules.

The Biochemical journal ·Vol. 246 ·No. 2 ·1987-09-01 ·Pages 279-86

Davidson HW, Peshavaria M, Hutton JC

Abstract

The nature of the endoproteolytic activity involved in the post-translational processing of proinsulin has been investigated in rat insulinoma tissue. 125I-proinsulin was converted by lysed insulin-secretory granules into insulin via an intermediate form identified as des-dibasic-proinsulin. This activity co-localized with immunoreactive (endogenous) insulin and carboxypeptidase H upon subcellular fractionation of the tissue, indicating a secretory-granular location. Under optimized conditions, conversion was quantitative. Inhibitor studies demonstrated that processing occurred by a reaction sequence involving cleavage on the C-terminal side of the pairs of basic amino acids, with subsequent removal of the newly exposed basic residues by carboxypeptidase H. Endoproteolytic activity was abolished by EDTA and CDTA (1,2-cyclohexanediaminetetra-acetic acid), but not by 1,10-phenanthroline or by group-specific inhibitors of serine, thiol or acidic proteinases. Inhibition by EDTA and CDTA could be reversed by both Ca2+ and Zn2+, although the former appeared to be the ion of physiological importance. Addition of Ca2+ in the absence of chelators stimulated endoproteinase activity, with a maximal effect at 5 mM, a concentration consistent with the intragranular environment. Similarly the pH optimum of 5.5 coincides with the prevailing intragranular pH. Together these properties suggest that the Ca2+-dependent endopeptidase described here is involved in vivo in the proteolytic processing of proinsulin.

MeSH Terms
Calcium/pharmacology Cations, Divalent Cytoplasmic Granules/metabolism Endopeptidases/metabolism Hydrogen-Ion Concentration Insulin/metabolism Insulin Secretion Insulinoma/metabolism Proinsulin/metabolism Protease Inhibitors/pharmacology Subcellular Fractions/metabolism
Chemicals
Cations, Divalent Insulin Protease Inhibitors Proinsulin Endopeptidases proinsulin endopeptidase I Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Davidson H W
Department of Clinical Biochemistry, University of Cambridge, Addenbrooke's Hospital, U.K.
Peshavaria M
Hutton J C
References (45)
45 references, click to expand
  1. Biochemical and clinical implications of proinsulin conversion intermediates.
    J Clin Invest. 1985 Oct;76(4):1398-405 PMID: 3902891
  2. The insulin-secretory-granule carboxypeptidase H. Purification and demonstration of involvement in proinsulin processing.
    Biochem J. 1987 Jul 15;245(2):575-82 PMID: 2822027
  3. High resolution acrylamide gel electrophoresis of histones.
    Arch Biochem Biophys. 1969 Mar;130(1):337-46 PMID: 5778650
  4. Subcellular localization of proinsulin to insulin conversion in isolated rat islets.
    Endocrinology. 1970 Jan;86(1):88-96 PMID: 4901349
  5. Conversion of proinsulin to insulin in a subcellular fraction from rat islets.
    Biochem Biophys Res Commun. 1970 Dec 9;41(5):1223-30 PMID: 4921757
  6. An electrophoretic study of the low-molecular-weight components of myosin.
    Biochem J. 1970 Aug;119(1):31-8 PMID: 5485752
  7. The structure of bovine proinsulin.
    J Biol Chem. 1971 May 10;246(9):2780-95 PMID: 4928892
  8. A bovine pancreatic enzyme catalyzing the conversion of proinsulin to insulin.
    Proc Natl Acad Sci U S A. 1971 Jun;68(6):1312-5 PMID: 5288380
  9. Studies on the conversion of proinsulin to insulin. I. Conversion in vitro with trypsin and carboxypeptidase B.
    J Biol Chem. 1971 Nov 25;246(22):6786-91 PMID: 4942325
  10. Effect of pH on conversion of proinsulin to insulin by a subcellular fraction of rat islets.
    Proc Soc Exp Biol Med. 1972 Feb;139(2):652-5 PMID: 4550940
  11. On the biosynthesis of insulin in anglerfish islets.
    J Biol Chem. 1972 Jun 25;247(12):4080-8 PMID: 4555957
  12. Studies on the conversion of proinsulin to insulin. 3. Studies in vitro with a crude secretion granule fraction isolated from rat islets of Langerhans.
    J Biol Chem. 1973 Jul 10;248(13):4544-51 PMID: 4578085
  13. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  14. Concentration of MgATP2- and other ions in solution. Calculation of the true concentrations of species present in mixtures of associating ions.
    Biochem J. 1976 Oct 1;159(1):1-5 PMID: 11772
  15. A transplantable insulinoma in the rat.
    Proc Natl Acad Sci U S A. 1977 Feb;74(2):628-32 PMID: 191819
  16. Enzymic processing of proparathyroid hormone by cell-free extracts of parathyroid glands.
    Biochemistry. 1977 Aug 23;16(17):3910-7 PMID: 409427
  17. Conversion of proinsulin into insulin by cathepsins B and L from rat liver lysosomes.
    Acta Biol Med Ger. 1977;36(11-12):1723-7 PMID: 616718
  18. Sequential cleavage of proinsulin by human pancreatic kallikrein and a human pancreatic kininase.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3612-6 PMID: 386342
  19. Plasminogen activator of islets of Langerhans: modulation by glucose and correlation with insulin production.
    Proc Natl Acad Sci U S A. 1980 Feb;77(2):875-9 PMID: 6444726
  20. The purified plasma membrane ATPase of the yeast Schizosaccharomyces pombe forms a phosphorylated intermediate.
    J Biol Chem. 1980 Oct 10;255(19):9353-7 PMID: 6447701
  21. A human proinsulin variant at arginine 65.
    Nature. 1981 Jun 25;291(5817):679-81 PMID: 7242673
  22. Characterization of proinsulin- and proglucagon-converting activities in isolated islet secretory granules.
    J Cell Biol. 1981 Aug;90(2):312-22 PMID: 7026570
  23. Isolation and characterization of calmodulin from an insulin-secreting tumour.
    Biochem J. 1981 Mar 1;193(3):875-85 PMID: 6272721
  24. Post-translational proteolysis in polypeptide hormone biosynthesis.
    Annu Rev Physiol. 1982;44:625-38 PMID: 7041809
  25. Proton-translocating Mg2+-dependent ATPase activity in insulin-secretory granules.
    Biochem J. 1982 Apr 15;204(1):161-70 PMID: 6126182
  26. The internal pH and membrane potential of the insulin-secretory granule.
    Biochem J. 1982 Apr 15;204(1):171-8 PMID: 6126183
  27. Conversion of proinsulin to insulin: involvement of a 31,500 molecular weight thiol protease.
    Proc Natl Acad Sci U S A. 1982 Aug;79(15):4613-7 PMID: 6750605
  28. Amounts and distribution of intracellular magnesium and calcium in pancreatic beta-cells.
    Acta Physiol Scand. 1982 Feb;114(2):235-41 PMID: 6753491
  29. Isolation and characterisation of insulin secretory granules from a rat islet cell tumour.
    Diabetologia. 1982 Oct;23(4):365-73 PMID: 6292032
  30. Identification of a 31,500 molecular weight islet cell protease as cathepsin B.
    Proc Natl Acad Sci U S A. 1983 Jun;80(11):3245-9 PMID: 6344078
  31. Low-molecular-weight constituents of isolated insulin-secretory granules. Bivalent cations, adenine nucleotides and inorganic phosphate.
    Biochem J. 1983 Feb 15;210(2):297-305 PMID: 6344863
  32. Purification and characterization of enkephalin convertase, an enkephalin-synthesizing carboxypeptidase.
    J Biol Chem. 1983 Sep 25;258(18):10950-5 PMID: 6411723
  33. Carboxypeptidase activity in the insulin secretory granule.
    FEBS Lett. 1983 Oct 3;162(1):137-41 PMID: 6311629
  34. Proteolysis in neuropeptide processing and other neural functions.
    Annu Rev Neurosci. 1984;7:189-222 PMID: 6370079
  35. Contrasting patterns of insulin biosynthesis, compartmental storage, and secretion. Rat tumor versus islet cells.
    Diabetes. 1984 Jun;33(6):556-61 PMID: 6202578
  36. Cathepsin B-related proteases in the insulin secretory granule.
    J Biol Chem. 1984 May 25;259(10):6041-4 PMID: 6327660
  37. Isolation of the putative structural gene for the lysine-arginine-cleaving endopeptidase required for processing of yeast prepro-alpha-factor.
    Cell. 1984 Jul;37(3):1075-89 PMID: 6430565
  38. Selective localization of calpain I (the low-Ca2+-requiring form of Ca2+-dependent cysteine proteinase) in B-cells of human pancreatic islets.
    FEBS Lett. 1985 May 6;184(1):120-4 PMID: 2985441
  39. Purification and characterization of a paired basic residue-specific pro-opiomelanocortin converting enzyme from bovine pituitary intermediate lobe secretory vesicles.
    J Biol Chem. 1985 Jun 25;260(12):7194-205 PMID: 2987247
  40. Hormone processing and membrane-bound proteinases in yeast.
    EMBO J. 1985 Jan;4(1):173-7 PMID: 3894003
  41. Direct identification of prohormone conversion site in insulin-secreting cells.
    Cell. 1985 Sep;42(2):671-81 PMID: 3896518
  42. Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2273-81 PMID: 3536964
  43. Biosynthesis of betagranin in pancreatic beta-cells. Identification of a chromogranin A-like precursor and its parallel processing with proinsulin.
    Biochem J. 1987 Jun 1;244(2):449-56 PMID: 3311030
  44. Proteolytic processing of chromogranin A in purified insulin granules. Formation of a 20 kDa N-terminal fragment (betagranin) by the concerted action of a Ca2+-dependent endopeptidase and carboxypeptidase H (EC 3.4.17.10).
    Biochem J. 1987 Jun 1;244(2):457-64 PMID: 2822006
  45. Purification and characterization of a paired basic residue-specific prohormone-converting enzyme from bovine pituitary neural lobe secretory vesicles.
    J Biol Chem. 1986 Nov 5;261(31):14392-7 PMID: 3021739
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1987-09-01
Pages
279-86
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1148274
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com