Sorting mechanism of peptide hormones and biogenesis mechanism of secretory granules by secretogranin III, a cholesterol-binding protein, in endocrine cells

Current Diabetes Reviews

Volumn 4, Issue 1, 2008, Pages 31-38

  Takeuchi, Toshiyuki S ^a   Hosaka, Masahiro ^a  

^a GUNMA UNIVERSITY   (Japan)

Author keywords

Carboxypeptidase E; Cholesterol; Chromogranin A; Secretogranin III; Secretory granules; Sorting

Indexed keywords

ALPHA 1 ANTITRYPSIN; CALCIUM; CARBOXYPEPTIDASE H; CHOLESTEROL; CHROMOGRANIN A; COMPLEMENTARY DNA; HORMONE PRECURSOR; INSULIN; LIPID BINDING PROTEIN; PEPTIDE HORMONE; PROINSULIN; SECRETOGRANIN III; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BINDING AFFINITY; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CHOLESTEROL SYNTHESIS; DNA LIBRARY; ENDOCRINE CELL; ENZYME ACTIVITY; EXOCRINE CELL; GENETIC TRANSCRIPTION; HORMONE RELEASE; HUMAN; HYPOTHALAMUS; HYPOTHESIS; INSULIN RELEASE; MEMBRANE BINDING; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REVIEW; SECRETORY GRANULE; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; CARBOXYPEPTIDASE H; CHROMOGRANIN A; CHROMOGRANINS; ENDOPLASMIC RETICULUM; HUMANS; INSULIN-SECRETING CELLS; NEUROENDOCRINE CELLS; PEPTIDE HORMONES; PROINSULIN; PROTEIN PRECURSORS; SECRETORY VESICLES;

EID: 38949193301     PISSN: 15733998     EISSN: None     Source Type: Journal    
DOI: 10.2174/157339908783502406     Document Type: Review

References (92)

1. Halban PA, Irminger J-C. Sorting and processing of secretory proteins. Biochem J 1994; 299: 1-18.
2. Tooze SA. Biogenesis of secretary granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim Biophys Acta 1998; 1404: 231-244.
3. Dannies PS. Protein hormone storage in secretory granules: Mechanisms for concentration and sorting. Endocr Rev 1999; 20: 3-21.
4. Glombik MM, Gerdes H-H. Signal-mediated sorting of neuropeptides and prohormones: Secretory granule biogenesis revisited. Biochimie 2000; 82: 315-326.
5. Tooze SA, Martens GJM, Huttner WB. Secretury granule biogenesis: Rafting to the sNARE. Trends Cell Biol 2001; 11: 116-122.
6. Burgoyne RD, Morgan A. Secretory granule exocytosis. Physiol Rev 2003; 83: 581-632.
7. Meldolesi J, Chiaregatti E, Malosio ML. Requirements for the identification of dense-core granules. Trends Cell Biol 2004; 14: 13-19.
8. fat mice. Cell 1997; 88: 73-83.
9. Kim T, Tao-Cheng J-H, Eiden LE, Loh YP. Chromogranin A, an "On/ off" Switch controlling dense-core secretory granule biogeriesis. Cell 2001; 106: 499-509.
10. Hosaka M, Watanabe T, Sakai Y, Uchiyama Y, Takeuchi T. Identification of a chromogranin A domain that mediates binding to secretogranin. III and targeting to secretory granules in pituitary cells and pancreatic -cells. Mol Biol Cell 2002; 13: 3388-3399.
11. Hosaka M, Suda M, Sakai Y, et al. Sercretogranin III binds to cholesterol in the secretory granule membrane as an adapter for chromogranin A. J Biol Chem 2004; 279: 3627-3634.
12. Hosaka M, Watanabe T, Sakai Y, Kato T, Takeuchi T. Interaction between secretogranin III and carboxypeptidase E facilitates prohormone sorting within secretory granules. J Cell Sci 2005; 118: 4785-4795.
13. Wang R, Hosaka M, Han L, et al. Molecular probes for sensing the cholesterol composition of subcellular organelle membranes. Biochim Biophys Acta 2006; 1761: 1169-1181.
14. Dikeakos JD, Reudelhuber TL. Sending proteins to dense core secretory granules: still a lot to sort out. J Cell Biol 2007; 177: 191-196.
15. Chance RE, Ellis RM, Bromer WW. Porcine proinsulin: Characterization and amon acid sequence. Science 1968; 16: 165-167.
16. Steiner DF, Cho S, Oyer PE, et al. Isolation and characterization of proinsulin c-peptide from bovine pancreas. J Biol Chem 1971; 246: 1365-1374.
17. Bell GI, Swain WF, Pictet F, et a. Nucleotide sequence of a cDNA clone encoding human preproinsulin. Nature 1979; 282: 525-527.
18. Docherty K, Steiner DF. Post-translational proteolysis in polypeptide hormone biosynthesis. Ann Rev Physiol 1982; 44: 625-638.
19. Davidson HW, Rhodes CJ, Hutton JC. Intraorganellar calcium and pH oontrol proinsulin cleavage in the pancreatic cell via two distinct site-specific endopeptidases. Nature 1988; 333: 93-96.
20. Seidah NG, Chrétien M. Proprotern and prohormone convertases of the subtilisin family recent developments and future perspectives. Trends Endocrinol Metab 1992; 3: 133-140.
21. Smeekens SP. Processing of protein precursors by a novel family of subtilisin-related mammalian endoproteases. Biotechnology 1993; 11: 182-186.
22. Zhou A, Webb G, Zhu X, Steiner DF. Proteolytic processing in the secretory pathway. J Biol Chem 1999; 274: 20745-20748.
23. Orci L, Ravazzola M, Amherdt M, et al. Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. J Cell Biol 1986; 103: 2273-2281.
24. Orci L, Ravazzola M, Storch MJ, et al. Proteolytic maturation of insulin is a post-Golgi event which occurs in acidifying clathrin-coated secretory vesicles. Cell 1987; 49: 865-868.
25. Anderson RGW, Orci L. View of acidic intracellular compartments. J Cell Sci 1988; 106: 539-543.
26. Orci L, Halban P, Perrelet A, et al. pH-dependent and -dependent cleavage of proinsulin in the same secretary vesicle. J Cell Biol 1994; 126: 1149-1156.
27. Schoonderwoert VTG, Martens GJM. Proton pumping in the secretory pathway. J Membr Biol 2001; 182: 159-169.
28. Moore H-PH, Walker MD, Lee F, Kelly RB. Expressing a human proinsulin cDNA in a mouse ACTH-secreting cell. Intracellular storage, proteolytic processing, and secretion on stimulation. Cell 1983; 35: 531-538.
29. Gerdes H-H, Rosa P, Phillips E, et al. The primary structure of human secretogranin II, a widespread tyrosine-sulfated secretory granule protein that exhibits low pH-and calcium-induced aggregation. J Biol Chem 1989; 264: 12009-12015.
30. You SH. Ph-dependent association of chromogranin A with secretory vesicle membrane and a putative membrane binding region of chromogranin A. Biochemistry 1993; 32: 8213-8219.
31. 2+ -dependent aggregation property of secretory vesicle matrix proteins and the potential role of chromogranins A and B in secretory vesicle biogenesis. J Biol Chem 1996; 271: 1558-1565.
32. Colomer V, Kicska GA, Rindler MJ. Secretory granule content and the luminal domains granule membrane proteins aggregate in vitro at mildly acidic pH. J Biol Chem 1996; 271: 48-55.
33. Rindler MJ. Carboxypeptidase E, a peripheral membrane protein implicated in the targeting of hormones to secretory granules, co-aggregates with granule content proteins at acidic pH. J Biol Chem 1998; 273: 31180-31185.
34. Huttner WB, Gerdes H-H, Rosa P. The granin (chromogranin/ secretogranin) family. Trends Biochem Sci 1991; 16: 27-30.
35. Chanat E, Weiss U, Huttner WB, Tooze SA. Reduction of the disulfide bond of chromogranin B (secretogranin I) in the trans-Golgi network causes its missorting to the constitutive secretory pathway. EMBO J 1993; 12: 2159-2168.
36. Kromer A, Glombik MM, Huttner WB, Gerdes H-H. Essential role of the dusulfide-bonded loop of chromogranin B for sorting to secretory granules is revealed by expression of a deletion mutant in the absense of endogenous granin synthesis. J Cell Biol 1998; 140: 1331-1346.
37. Glombik MM, Kromer A, Salm T, Huttner WB, Gerdes H-H. The disulfide-bonded loop of chromogranin B mediates membrane binding and directs sorting from the trans-Golgi network to secretary grnaules. EMBO J 1999; 18: 1059-1070.
38. Yoo SH, So SH, Kweon HS, et al. Coupling of the inositol 1,4,5-trisphosphate receptor and chromogranins A and B in secretory granules. J Biol Chem 2000; 275: 12553-12559.
39. 2+ storage protein of secretory granules. J Biol Chem 2000; 275: 15067-15073.
40. Blondel O, Takada J, Janssen H, Seino S, Bell GI. Sequence and functional characterization of a third inositol trisphosphate receptor subtype, IP3R-3, expressed in pancreatic islets, kidney, gastrointestinal tract, and other tissues. J Biol Chem 1993; 268: 11356-11363.
41. Blondel O, Moody MM, Depaoli AM, et al. Localization of inositol trisphosphate receptor subtype 3 to insulin and somatostatin secretory granules and regulation of expression in islets and insulinoma cells. Proc Natl Acad Sci U S A 1994; 91: 7777-7781.
42. Vermassen E, Parys JB, Mauger J-P. Subcellular distribution of the inositol 1,4,5-triphosphate receptors: functional relevance and molecular determinants. Biol Cell 2004; 96: 3-17.
43. fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat Genet 1995; 10: 135-142.
44. Zhang C-F, Snell CR, Loh YP. Identification of a novel prohormone sorting signal-binding site on carboxypeptidase E, a regulated secretory pathway-sorting receptor. Mol Endocrinol 1999; 13: 527-536.
45. fat mice. J Biol Chem 1997; 272: 37532-27534.
46. fat mice are defective in carboxypeptidase E and proinsulin processing. Endocrinology 1997; 138: 4833-4892.
47. Normant E, Loh YP. Depletion of carboxypeptidase E, a regulated secretory pathway sorting receptor, causes misrounting and constituitive secretion of proinsulin and proenkephalin, but not chromogranin A. Endocrinology 1998; 139: 2137-2145.
48. Winkler H, Fischer-Colbrie R. The chromogranins A and B: The first 25 years and future perspective. Neuroscience 1992; 49: 497-528.
49. Natori S, Huttner WB. Chromogranin B (secretogranin I) promotes sorting to the regulated secretory pathway of processing intermediates derived from a peptide hormone precursor. Proc Natl Acad Sci U S A 1996; 93: 4431-4436.
50. Yoo SH, Lewis MS. Interaction of chromogranin B and the near N-terminal region of chromogranin B with an intraluminal loop peptide of the inositol 1,4,5-triphosphate receptor. J Biol Chem 2000; 275: 30293-30300.
51. Taupenot L, Harper KL, Mahapatra NR, et al. Identification of a novel sorting determinant for the regulated pathway in the secretory protein chromogranin A. J Cell Sci 2002; 115: 4827-4841.
52. Loh YP, Kim T, Rodriguez YM, Cawley NZ. Secretory granule biogenesis and neuropeptide sorting to the regulated secretory pathway in neuroendocrine cells. J Mol Neurosci 2003; 22: 63-71.
53. Day R, Gorr S-U. Secretory granule biogenesis and chromogranin A:master gene, on/off switch or assembly factor? Trends Endocrinol Metab 2003; 14: 10-13.
54. Huh YH, Jeon SH, Yoo SH. Chromogranin B-induced secretory granule biogenesis. J Biol Chem 2003; 278: 40581-40589.
55. Beuret N, Stettler H, Renold A, Rutishauser J, Spiess M. Expression of regulated secretory proteins is sufficient to generate granule-like structures in constitutively secreting cells. J Biol Chem 2004; 279: 20242-20249.
56. Mahapatra NR, O'Connor DT, Vaingankar SM, et al. Hypertension from targeted ablation of chromogranin A can be rescued by the human ortholog. J Clin Invest 2005; 115: 1942-1952.
57. Kim T, Loh YP. Chromogranin A: a surprising link between granule biogenesis and hypertension. J Clin Invest 2005; 115: 1711-1713.
58. Kim T, Zhang C-F, Sun Z, Wu H, Loh YP. Chromogranin A deficiency in transgenic mice leads to aberrant chromaffin granule biogenesis. J Neurosci 2005; 25: 6958-6961.
59. Malosio ML, Giordano T, Laslop A, Meldolesi J. Dense-core granules: specific hallmark of the neuronal/neurosecretory cell phenotype. J Cell Sci 2004; 117: 743-749.
60. Hendy GN, Li T, Girard M, et al. Targeted ablation of the chromogranin A (Chga) gene: Normal neuroendocrine dense-core secretory granules and increased expression of other granins. Mol Endocrinol 2006; 20: 1935-1947.
61. Sakai Y, Hosaka M, Hira Y, et al. Immunocytochemical localization of secretogranin III in the anterior lobe of male rat pituitary glands. J Histochem Cytochem 2003; 51: 227-238.
62. Dhanvantari S, Loh YP. Lipid raft association of carboxypeptidase E is necessary for its function as a regulated secretory pathway sorting receptor. J Biol Chem 2000; 275: 29887-29893.
63. Huang J, Feigenson GW. A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys J 1999; 76: 2142-2157.
64. Ohvo-Rekilä H, Ramstedt B, Leppimäki P, Slotte J. Cholesterol interactions with phospholipids in membranes. Prog Lipid Res 2002; 41: 66-97.
65. Bretscher MS, Munro S. Cholesterol and the Golgi apparatus. Science 1993; 261: 1280-1281.
66. Simons IL, Ikonen E. How cells handle cholesterol. Science 2000; 220: 1721-1726.
67. Arnaoutova I, Smith AM, Coates LC, et al. The prohormone processing enzyme PC3 is a lipid raft-associated transmembrane protein. Biochemistry 2003; 42: 10445-10455.
68. Blázquez M, Thiele C, Huttner WB, Docherty Y, Shennan KIJ. Involvement of the membrane lipid bilayer in sorting prohormone convertase 2 into the regulated sccretory pathway. Biochem J 2000; 349: 843-852.
69. Assadi M, Sharpe JC, Snell C, Loh YP. The C-terminus of prohormone oonvertase 2 is sufficient and necessary for raft association and sorting to the regulated secretory pathway. Biochemistry 2004; 43: 7798-7807.
70. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2000; 2: 42-49.
71. Mitter D, Reisinger C, Hinz B, et al. The synaptophysin/ synaptobrevin interaction critically depends on the cholesterol content. J Neurochem 2003; 84: 35-42.
72. Ottiger H-P, Battenberg EF, Tsou A-P, Bloom FE, Sutcliffe JG. 1B1075: A brain- and pituitary-specific mRNA that encodes a novel chromogranin/ secretogranin-like component of intracellular vesicles. J Neurosci 1990; 10: 3135-3147.
73. Kingsley DM, Rinchik EM, Russell LB, et al. Genetic ablation of a mouse gene expressed specifically in brain. EMBO J 1990; 9: 395-399.
74. Holthuis JCM, Martens GJM. The neuroendocrine proteins secretogranin II and III are regionally conserved and coordinately expressed with proopiomelanocortin in Xenopus intermediate pituitary. J Neurochem 1996; 66: 2248-2256.
75. Knoch K-P, Bergert H, Borgonovo P, et al. Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis. Nat Cell Biol 2004; 6: 207-214.
76. 2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J Cell Biol 2001; 155: 41-51.
77. Tanabe A, Yanagiya T, Iida A, et al. Functional single-nucleotide polymorphisms in the secretogranin III (SCG3) gene that form secretory granules with appetite-related neuropeptides are associated with obesity. J Clin Endocrinol Metab 2007; 92: 1145-1154.
78. Taupenot L, Harper KL, O'Connor DT. The chromogranin-secretogranin family. N Engl J Med 2003; 348: 1134-1149.
79. Mitra A, Song L, Fricker LD. The C-terminal region of carboxypeptidase E is involved in membrane binding and intracellular routing in AtT-20 cells. J Biol Chem 1994; 269: 19876-19881.
80. Eipper BA, Stoffers DA, Mains RE. The biosynthesis of neuropeptides: Peptide -amidation. Annu Rev Neurosci 1992; 15: 57-85.
81. Brown H, Meister B, Deeney J, et al. Synaptotagmin III isoform is compart-mentalized in pancreatic -cells and has a functional role in exocytosis. Diabetes 2000; 49: 383-391.
82. Wasmeier C, Hutton JC. Molecular cloning of phogrin, a protein-tyrosine phosphatase homologue localized to insulin secratory granule membranes. J Biol Chem 1996; 271: 18161-18170.
83. Solimena M, Dirkx R Jr., Hermel J-M, et al. ICA 512, an autoantigen of type I diabetes, is an intrinsic membrane protein of neurosecretory granules. EMBO J 1996; 15: 2102-2114.
84. 2+ storage proteins chromogranins A and B in secretory granules. TINS 2000; 23: 424-428.
85. 2+ transporters but control glucose-evoked granule recruitment. J Cell Sci 2005; 118: 5647-5659.
86. Konstantinova I, Nikolova G, Ohara-Imaizumi M, et al. Epha-ephrin-a-mediated cell communication regulates insulin secretion from pancreatic islets. Cell 2007; 129: 359-370.
87. Wang J, Takeuchi T, Yokota H, Izumi T. Novel rabphilin-3-like protein associates with insulin-containing granules in pancreatic beta cells. J Biol Chem 1999; 274: 28542-28548.
88. Yi Z, Yokota H, Torii S, et al. The rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol Cell Biol 2002; 22: 1858-1867.
89. Easom RA. CaM kinase II:A protein kinase with extraordinary talents germane to insulin exocytosis. Diabetes 1999; 48: 675-684.
90. Arden C, Harbottle A, Baltrusch S, Tiedge M, Agius L. Glucokinase is an integral component of the insulin granules in glucose-responsive insulin secretory cells and does not translocate during glucose stimulation. Diabetes 2004; 53: 2346-2352.
91. Varadi A, Tsuboi T, Rutter GA. Myosin va transports dense core secretory vesicles in pancreatic MIN6 -cells. Mol Biol Cell 2005; 16: 2670-2680.
92. Cheviet S, Coppola T, P.Haynes L, Burgoyne RD, Regazzi R. The rab-binding protein Noc2 is associated with insulin-conaining secretory granules and is essential for pancreatic β-cell exocytosis. Mol Endocrinol 2004; 18(1): 117-26.