Adventures with insulin in the islets of langerhans

Journal of Biological Chemistry

Volumn 286, Issue 20, 2011, Pages 17399-17421

  Steiner, Donald F ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; CHAINS; ENZYMES; INSULIN; PEPTIDES;

ACTIVE PRECURSORS; BIOCHEMICAL RESEARCH; DIABETES MELLITUS; ISLETS OF LANGERHANS; NEUROENDOCRINE PEPTIDES; PROTEIN PRECURSORS; SECRETORY PATHWAYS; VIRAL ENVELOPE PROTEINS;

PROTEINS;

C PEPTIDE; FURIN; HORMONE PRECURSOR; INSULIN; PROINSULIN;

AMINO ACID SEQUENCE; ARTICLE; DIABETES MELLITUS; ENZYME ACTIVITY; FUNGAL GENETICS; HUMAN; INSULIN METABOLISM; INSULIN RELEASE; INSULIN SYNTHESIS; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; ANIMAL; BIOCHEMISTRY; HISTORY; METABOLISM; METHODOLOGY;

ANIMALS; BIOCHEMISTRY; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; INSULIN; ISLETS OF LANGERHANS;

EID: 79960958485     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.X111.244764     Document Type: Article

References (84)

1. Eulenburg-Wiener, R. V. (1938) Fearfully and Wonderfully Made: The Human Organism in the Light of Modern Science, Macmillan, New York
2. Steiner, D. F., and Anker, H. S. (1956) On the synthesis of antibody protein in vitro. Proc. Natl. Acad. Sci. U.S.A. 42, 580-586
3. Murnaghan, J. H., and Talalay P. (1967) John Jacob Abel and the crystallization of insulin. Perspect. Biol. Med. 10, 334-380
4. Jensen, H., and Evans, E. A., Jr. (1935) Studies on crystalline insulin. XVIII. The nature of the free amino groups in insulin and the isolation of phenylalanine and proline from crystalline insulin. J. Biol. Chem. 108, 1-9
5. Steiner, D. F., and Williams, R. H. (1958) Respiratory inhibition and hypoglycemia by biguanides and decamethylene diguanidine. Biochim. Biophys. Acta 30, 329-340
6. Wick, A. N., Larson, E. R., and Serif, G. S. (1958) A site of action of phenethylbiguanide, a hypoglycemic compound. J. Biol. Chem. 233, 296-298
7. Steiner, D. F., and Williams, R. H. (1959) Actions of phenethylbiguanide and related compounds (editorial). Diabetes 8, 154-157
8. Morgan, H. E., Cadenas, E., Regen, D. M., and Park, C. R. (1961) Regulation of glucose uptake in muscle. II. Rate-limiting steps and effects of insulin and anoxia in heart muscle from diabetic rats. J. Biol. Chem. 236, 262-268
9. Steiner, D. F., and Williams, R. H. (1959) Some observations concerning hepatic glucose 6-phosphate content in normal and diabetic rats. J. Biol. Chem. 234, 1342-1346
10. Steiner, D. F. (1978) Insulin-induced liver hyperplasia. Evidence for a negative liver-size-correcting process. CIBA Found. Symp. 55, 229-246
11. Younger, L. R., King, J., and Steiner, D. F. (1966) Hepatic proliferative response to insulin in severe alloxan diabetes. Cancer Res. 26, 1408-1414
12. Michael, M. D., Kulkarni, R. N., Postic, C., Previs, S. F., Shulman, G. I., Magnuson, M. A., and Kahn, C. R. (2000) Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol. Cell 6, 87-97
13. Steiner, D. F. (1966) Insulin and the regulation of hepatic biosynthetic activity. Vitam. Horm. 24, 1-61
14. Davoren, P. R. (1962) The isolation of insulin from a single cat pancreas. Biochim. Biophys. Acta 63, 150-153
15. Steiner, D. F., and Oyer, P. C. (1967) The biosynthesis of insulin and a probable precursor of insulin by a human islet cell adenoma. Proc. Natl. Acad. Sci. U.S.A. 57, 473-480
16. Steiner, D. F., Cunningham, D., Spigelman, L., and Aten, B. (1967) Insulin biosynthesis evidence for a precursor. Science 157, 697-700
17. Wang, S. S., and Carpenter, F. H. (1965) A compositional assay for insulin applied to a search for "proinsulin." J. Biol. Chem. 240, 1619-1625
18. Steiner, D. F., Clark, J. L., Nolan, C., Rubenstein, A. H., Margoliash, E., Aten, B., and Oyer, P. E. (1969) Proinsulin and the biosynthesis of insulin. Recent Prog. Horm. Res. 25, 207-282
19. Steiner, D. F., Clark, J. L., Nolan, C., Rubenstein, A. H., Margoliash, E., Melani, F., and Oyer, P. E. (1970) The biosynthesis of insulin and some speculations regarding the pathogenesis of human diabetes. In: The Pathogenesis of Diabetes Mellitus. Nobel Symposium 13 (Cerasi, E., and Luft, R., eds) pp. 57-80, Almqvist and Wiksell International, Stockholm
20. Jamieson, J. D., and Palade, G. E. (1967) Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. II. Transport to condensing vacuoles and zymogen granules. J. Cell Biol. 34, 577-615
21. Orci, L., Ravazzola, M., Amherdt, M., Madsen, O., Vassalli, J. D., and Perrelet, A. (1985) Direct identification of prohormone conversion site in insulin-secreting cells. Cell 42, 671-681
22. Clark, J. L., and Steiner, D. F. (1969) Insulin biosynthesis in the rat. Demonstration of two proinsulins. Proc. Natl. Acad. Sci. U.S.A. 62, 278-285
23. Steiner, D. F., Hallund, O., Rubenstein, A., Cho, S., and Bayliss, C. (1968) Isolation and properties of proinsulin, intermediate forms, and other minor components from crystalline bovine insulin. Diabetes 17, 725-736
24. Steiner, D. F., Cho, S., Oyer, P. E., Terris, S., Peterson, J. D., and Rubenstein, A. H. (1971) Isolation and characterization of proinsulin C-peptide from bovine pancreas. J. Biol. Chem. 246, 1365-1374
25. Chance, R. E., Ellis, R. M., and Bromer, W. W. (1968) Porcine proinsulin. Characterization and amino acid sequence. Science 161, 165
26. Nolan, C., Margoliash, E., Peterson, J. D., and Steiner, D. F. (1971) Structure of bovine proinsulin. J. Biol. Chem. 246, 2780-2795
27. Rubenstein, A. H., Clark, J. L., Melani, F., and Steiner, D. F. (1969) Secretion of proinsulin C-peptide by pancreatic B cells and its circulation in blood. Nature 224, 697-699
28. Oyer, P. E., Cho, S., Peterson, J. D., and Steiner, D. F. (1971) Studies on human proinsulin. Isolation and amino acid sequence of the human pancreatic C-peptide. J. Biol. Chem. 246, 1375-1386
29. Rubenstein, A. H., Cho, S., and Steiner, D. F. (1968) Evidence for proinsulin in human urine and serum. Lancet 291, 1353-1355
30. Melani, F., Rubenstein, A. H., Oyer, P. E., and Steiner, D. F. (1970) Identification of proinsulin and C-peptide in human serum by a specific immunoassay. Proc. Natl. Acad. Sci. U.S.A. 67, 148-155
31. Polonsky, K. S., and Rubenstein, A. H. (1986) Current approaches to measurement of insulin secretion. Diabetes Metab. Rev. 2, 315-329
32. Palmer, J. P., Fleming, G. A., Greenbaum, C. J., Herold, K. C., Jansa, L. D, Kolb, H., Lachin, J. M., Polonsky, K. S., Pozzilli, P., Skyler, J. S., and Steffes, M. W. (2004) C-peptide is the appropriate outcome measure for type 1 diabetes clinical trials to preserve beta-cell function. Report of an ADA workshop, 21-22 October 2001. Diabetes 53, 250-264
33. Steiner, D. F., and Clark, J. L. (1968) The spontaneous reoxidation of reduced beef and rat proinsulins. Proc. Natl. Acad. Sci. U.S.A. 60, 622-629
34. Givol, D., Delorenzo, F., Goldberger, R. F., and Anfinsen, C. B. (1965) Disulfide interchange and the three-dimensional structure of proteins. Proc. Natl. Acad. Sci. U.S.A. 53, 676-684
35. Humbel, R. E. (1965) Biosynthesis of the two chains of insulin. Proc. Natl. Acad. Sci. U.S.A. 53, 853-859
36. Efrat, S., Linde, S., Kofod, H., Spector, D., Delannoy, M., Grant, S., Hanahan, D., and Baekkeskov, S. (1988) Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene. Proc. Natl. Acad. Sci. U.S.A. 85, 9037-9041
37. Sachs, H., and Takabatake, Y. (1964) Evidence for a precursor in vasopressin biosynthesis. Endocrinology 75, 943-948
38. Douglass, J., Civelli, O., and Herbert, E. (1984) Polyprotein gene expression. Generation of diversity of neuroendocrine peptides. Annu. Rev. Biochem. 53, 665-715
39. Zhou, A., Webb, G., Zhu, X., and Steiner, D. F. (1999) Proteolytic processing in the secretory pathway. J. Biol. Chem. 274, 20745-20748
40. Blobel, G., and Dobberstein, B. (1975) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67, 835-851
41. Blobel, G., and Dobberstein, B. (1975) Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J. Cell Biol. 67, 852-862
42. Chan, S. J., Keim, P., and Steiner, D. F. (1976) Cell-free synthesis of rat preproinsulins. Characterization and partial amino acid sequence determination. Proc. Natl. Acad. Sci. U.S.A. 73, 1964-1968
43. Shields, D., and Blobel, G. (1977) Cell-free synthesis of fish preproinsulin and processing by heterologous mammalian microsomal membranes. Proc. Natl. Acad. Sci. U.S.A. 74, 2059-2063
44. Terris, S., and Steiner, D. F. (1975) Binding and degradation of 125I-insulin by rat hepatocytes. J. Biol. Chem. 250, 8389-8398
45. Terris, S., and Steiner, D. F. (1976) Retention and degradation of 125I-Insulin by perfused rat livers. J. Clin. Invest. 57, 885-896
46. Terris, S., Hofmann, C., and Steiner, D. F. (1979) Mode of uptake and degradation of 125I-labelled insulin by isolated hepatocytes and H4 hepatoma cells. Can. J. Biochem. 57, 459-468
47. Shoelson, S., Haneda, M., Blix, P., Nanjo, A., Sanke, T., Inouye, K., Steiner, D., Rubenstein A., and Tager, H. (1983) Three mutant insulins in man. Nature 302, 540-543
48. Støy, J., Edghill, E. L., Flanagan, S. E., Ye, H., Paz, V. P., Pluzhnikov, A., Below, J. E., Hayes, M. G., Cox, N. J., Lipkind, G. M., Lipton, R. B., Greeley, S. A., Patch, A. M., Ellard, S., Steiner, D. F., Hattersley, A. T., Philipson, L. H., and Bell, G. I. (2007) Insulin gene mutations as a cause of permanent neonatal diabetes. Proc. Natl. Acad. Sci. U.S.A. 104, 15040-15044
49. Steiner, D. F., Park, S. Y., Støy, J., Philipson, L. H, and Bell, G. I. (2009) A brief perspective on insulin production. Diabetes Obes. Metab. 11, 189-196
50. Smith, B. J., Huang, K., Kong, G., Chan, S. J., Nakagawa, S., Menting, J. G., Hu, S. Q., Whittaker, J., Steiner, D. F., Katsoyannis, P. G., Ward, C. W., Weiss, M. A., and Lawrence, M. C. (2010) Structural resolution of a tandem hormone-binding element in the insulin receptor and its implications for design of peptide agonists. Proc. Natl. Acad. Sci. U.S.A. 107, 6771-6776
51. Kurose, T., Pashmforoush, M., Yoshimasa, Y., Carroll, R., Schwartz, G. P., Burke, G. T., Katsoyannis, P. G., and Steiner, D. F. (1994) Cross-linking of a B25 azidophenylalanine insulin derivative to the carboxyl-terminal region of the alpha-subunit of the insulin receptor. Identification of a new insulin-binding domain in the insulin receptor. J. Biol. Chem. 269, 29190-29197
52. Wang, S. S., and Carpenter, F. H. (1969) Kinetics of the tryptic hydrolysis of zinc-free bovine insulin. J. Biol. Chem. 244, 5537-5543
53. Kemmler, W., Peterson, J. D., and Steiner, D. F. (1971) Studies on the conversion of proinsulin to insulin. I. Conversion in vitro with trypsin and carboxypeptidase B. J. Biol. Chem. 246, 6786-6791
54. Kemmler, W., Steiner, D. F., and Borg, J. (1973) Studies on the conversion of proinsulin to insulin. III. Studies in vitro with a crude secretion granule fraction isolated from rat islets of Langerhans. J. Biol. Chem. 248, 4544-4551
55. Chance, R. E., and Frank, B. H. (1993) Research, development, production, and safety of biosynthetic human insulin. Diabetes Care 16, Suppl. 3, 133-142
56. Zühlke, H., Steiner, D. F., Lernmark, A., and Lipsey, C. (1976) Carboxypeptidase B-like and trypsin-like activities in isolated rat pancreatic islets. CIBA Found. Symp. 41, 183-195
57. Fricker, L. D., Evans, C. J., Esch, F. S., and Herbert, E. (1986) Cloning and sequence analysis of cDNA for bovine carboxypeptidase E. Nature 323, 461-464
58. Naggert, J. K., Fricker, L. D., Varlamov, O., Nishina, P. M., Rouille, Y., Steiner, D. F., Carroll, R. J., Paigen, B. J., and Leiter, E. H. (1995) Hyperproinsulinaemia in obese fat/fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat. Genet. 10, 135-142
59. Day, R., Lazure, C., Basak, A., Boudreault, A., Limperis, P., Dong, W., and Lindberg, I. (1998) Prodynorphin processing by proprotein convertase 2. Cleavage at single basic residues and enhanced processing in the presence of carboxypeptidase activity. J. Biol. Chem. 273, 829-836
60. Docherty, K., Carroll, R., and Steiner, D. F. (1983) Identification of a 31,500 molecular weight islet cell protease as cathepsin B. Proc. Natl. Acad. Sci. U.S.A. 80, 3245-3249
61. Kuliawat, R., Klumperman, J., Ludwig, T., and Arvan, P. (1997) Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic beta-cells. J. Cell Biol. 137, 595-608
62. Julius, D., Brake, A., Blair, L., Kunisawa, R., and Thorner, J. (1984) Isolation of the putative structural gene for the lysine-arginine-cleaving endopeptidase required for processing of yeast prepro-alpha factor. Cell 37, 1075-1089
63. Mizuno, K., Nakamura, T., Ohshima, T., Tanaka, S., and Matsuo H. (1988) Yeast Kex2 gene encodes an endopeptidase homologous to subtilisin-like serine proteases. Biochem. Biophys. Res. Commun. 156, 246-254
64. Smeekens, S. P., and Steiner, D. F. (1990) Identification of a human insulinoma cDNA encoding a novel mammalian protein structurally related to the yeast dibasic processing protease Kex2. J. Biol. Chem. 265, 2997-3000
65. Smeekens, S. P., Avruch, A. S., LaMendola, J., Chan, S. J., and Steiner, D. F. (1991) Identification of a cDNA encoding a second putative prohormone convertase related to PC2 in AtT20 cells and islets of Langerhans. Proc. Natl. Acad. Sci. U.S.A. 88, 340-344
66. Steiner, D. F., Smeekens, S. P., Ohagi, S., and Chan, S. J. (1992) The new enzymology of precursor processing endoproteases. J. Biol. Chem. 267, 23435-23438
67. Davidson, H. W., Rhodes, C. J., and Hutton, J. C. (1988) Intraorganellar calcium and pH control proinsulin cleavage in the pancreatic beta cell via two distinct site-specific endopeptidases. Nature 333, 93-96
68. Fuller, R. S., Brake, A. J., and Thorner, J. (1989) Intracellular targeting and structural conservation of a prohormone-processing endoprotease. Science 246, 482-486
69. Seidah, N. G., Mayer, G., Zaid, A., Rousselet, E., Nassoury, N., Poirier, S., Essalmani, R., and Prat, A. (2008) The activation and physiological functions of the proprotein convertases. Int. J. Biochem. Cell Biol. 40, 1111-1125
70. Docherty, K., and Steiner, D. F. (1982) Post-translational proteolysis in polypeptide hormone biosynthesis. Annu. Rev. Physiol. 44, 625-638
71. Nolan, C., Novoa, W. B., Krebs, E. G., and Fischer, E. H. (1964) Further studies on the site phosphorylated in the phosphorylase B to A reaction. Biochemistry 3, 542-551
72. Peinado, J. R., Laurent, V., Lee, S. N., Peng, B. W., Pintar, J. E., Steiner, D. F., and Lindberg, I. (2005) Strain-dependent influences on the hypothalamo-pituitaryadrenal axis profoundly affect the 7B2 and PC2 null phenotypes. Endocrinology 146, 3438-3444
73. Zhu, X., Zhou, A., Dey, A., Norrbom, C., Carroll, R., Zhang, C., Laurent, V., Lindberg, I., Ugleholdt, R., Holst, J. J., and Steiner, D. F. (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
74. Scamuffa, N., Calvo, F., Chrétien, M., Seidah, N. G., and Khatib, A. M. (2006) Proprotein convertases. Lessons from knockouts. FASEB J. 20, 1954-1963
75. Czyzyk, T. A., Ning, Y., Hsu, M. S., Peng, B., Mains, R. E., Eipper, B. A., and Pintar, J. E. (2005) Deletion of peptide amidation enzymatic activity leads to edema and embryonic lethality in the mouse. Dev. Biol. 287, 301-313
76. Louagie, E., Taylor, N. A., Flamez, D., Roebroek, A. J., Bright, N. A., Meulemans, S., Quintens, R., Herrera, P. L., Schuit, F., Van de Ven, W. J., and Creemers, J. W. (2008) Role of furin in granular acidification in the endocrine pancreas. Identification of the V-ATPase subunit Ac45 as a candidate substrate. Proc. Natl. Acad. Sci. U.S.A. 105, 12319-12324
77. Zhang, X., Pan, H., Peng, B., Steiner, D. F., Pintar, J. E., and Fricker, L. D. (2010) Neuropeptidomic analysis establishes a major role for prohormone convertase-2 in neuropeptide biosynthesis. J. Neurochem. 112, 1168-1179
78. Remacle, A. G., Shiryaev, S. A., Oh, E. S., Cieplak, P., Srinivasan, A., Wei, G., Liddington, R. C., Ratnikov, B. I., Parent, A., Desjardins, R., Day, R., Smith, J. W., Lebl, M., and Strongin, A. Y. (2008) Substrate cleavage analysis of furin and related proprotein convertases. A comparative study. J. Biol. Chem. 283, 20897-20906
79. Zhu, X., Orci, L., Carroll, R., Norrbom, C., Ravazzola, M., and Steiner, D. F. (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
80. Cameron, A., Apletalina, E. V., and Lindberg, I. (2001) The enzymology of PC1 and PC2. In: The Enzymes, Vol. XXII, Academic Press, New York
81. Nishi, M., Sanke, T., Nagamatsu, S., Bell, G. I., and Steiner, D. F. (1990) Islet amyloid polypeptide. A new beta 61476 cell secretory product related to islet amyloid deposits. J. Biol. Chem. 265, 4173-4176
82. Marzban, L., Rhodes, C. J., Steiner, D. F., Haataja, L., Halban, P. A., and Verchere, C. B. (2006) Impaired NH2-terminal processing of human proislet amyloid polypeptide by the prohormone convertase PC2 leads to amyloid formation and cell death. Diabetes 55, 2192-2201
83. Chan, S. J., Cao, Q. P., and Steiner, D. F. (1990) Evolution of the insulin superfamily. Cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus. Proc. Natl. Acad. Sci. U.S.A. 87, 9319-9323
84. Furuta, M., Carroll, R., Martin, S., Swift, H. H., Ravazzola, M., Orci, L., and Steiner, D. F. (1998) Incomplete processing of proinsulin to insulin accompanied by elevation of des-31, 32 proinsulin intermediates in islets of mice lacking active PC2. (1998) J. Biol. Chem. 273, 3431-3437