Biogenesis of secretory granules

Current Opinion in Cell Biology

Volumn 18, Issue 4, 2006, Pages 365-370

  Borgonovo, Barbara ^a   Ouwendijk, Joke ^a   Solimena, Michele ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGENESIS; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; INSULIN RELEASE; NEUROSECRETORY CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RNA STABILITY; RNA TRANSLATION; SECRETORY GRANULE; TRANSCRIPTION REGULATION;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; RNA, MESSENGER; SECRETORY VESICLES;

EID: 33745747908     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2006.06.010     Document Type: Review

References (53)

1. Glombik M.M., and Gerdes H.H. Signal-mediated sorting of neuropeptides and prohormones: secretory granule biogenesis revisited. Biochimie 82 (2000) 315-326
2. Taupenot L., Harper K.L., and O'Connor D.T. The chromogranin-secretogranin family. N Engl J Med 348 (2003) 1134-1149
3. Steiner D.F. The proprotein convertases. Curr Opin Chem Biol 2 (1998) 31-39
4. Meldolesi J., Chieregatti E., and Luisa Malosio M. Requirements for the identification of dense-core granules. Trends Cell Biol 14 (2004) 13-19
5. Perrais D., Kleppe I.C., Taraska J.W., and Almers W. Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J Physiol 560 (2004) 413-428. Combining capacitance measurements and evanescent fluorescence microscopy, the authors demonstrate that SG cargoes are discharged with different speeds, possibly because of their different ability to bind the matrix and/or the membrane of SGs.
6. Grabner C.P., Price S.D., Lysakowski A., and Fox A.P. Mouse chromaffin cells have two populations of dense core vesicles. J Neurophysiol 94 (2005) 2093-2104
7. Michael D.J., Ritzel R.A., Haataja L., and Chow R.H. Pancreatic β-cells secrete insulin in fast- and slow-release forms. Diabetes 55 (2006) 600-607
8. Duncan R.R., Greaves J., Wiegand U.K., Matskevich I., Bodammer G., Apps D.K., Shipston M.J., and Chow R.H. Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422 (2003) 176-180
9. Solimena M., and Gerdes H.H. Secretory granules: and the last shall be first. Trends Cell Biol 13 (2003) 399-402
10. Arvan P., and Halban P.A. Sorting ourselves out: seeking consensus on trafficking in the β-cell. Traffic 5 (2004) 53-61
11. Tooze S.A., Martens G.J., and Huttner W.B. Secretory granule biogenesis: rafting to the SNARE. Trends Cell Biol 11 (2001) 116-122
12. Kim T., Gondre-Lewis M.C., Arnaoutova I., and Loh Y.P. Dense-core secretory granule biogenesis. Physiology (Bethesda) 21 (2006) 124-133
13. Cool D.R., Normant E., Shen F., Chen H.C., Pannell L., Zhang Y., and Loh Y.P. Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88 (1997) 73-83
14. Day R., and Gorr S.U. Secretory granule biogenesis and chromogranin A: master gene, on/off switch or assembly factor?. Trends Endocrinol Metab 14 (2003) 10-13
15. fat mice. Endocrinology 144 (2003) 292-298
16. Cawley N.X., Zhou J., Hill J.M., Abebe D., Romboz S., Yanik T., Rodriguiz R.M., Wetsel W.C., and Loh Y.P. The carboxypeptidase E knockout mouse exhibits endocrinological and behavioral deficits. Endocrinology 145 (2004) 5807-5819
17. Kakhlon O., Sakya P., Larijani B., Watson R., and Tooze S.A. GGA function is required for maturation of neuroendocrine secretory granules. Embo J 25 (2006) 1590-1602. By inhibiting the activity and expression of the clathrin adaptor GGA, the authors further define the machinery responsible for the removal of mis-sorted proteins from immature SGs and the importance of this pathway for the correct processing of SG cargoes.
18. Ahras M., Otto G.P., and Tooze S.A. Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J Cell Biol (2006)
19. Taraska J.W., Perrais D., Ohara-Imaizumi M., Nagamatsu S., and Almers W. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci U S A 100 (2003) 2070-2075
20. Tsuboi T., McMahon H.T., and Rutter G.A. Mechanisms of dense core vesicle recapture following 'kiss and run' ('cavicapture') exocytosis in insulin-secreting cells. J Biol Chem 279 (2004) 47115-47124
21. Kim T., Tao-Cheng J.H., Eiden L.E., and Loh Y.P. Chromogranin A, an 'on/off' switch controlling dense-core secretory granule biogenesis. Cell 106 (2001) 499-509
22. Kim T., Zhang C.F., Sun Z., Wu H., and Loh Y.P. Chromogranin A deficiency in transgenic mice leads to aberrant chromaffin granule biogenesis. J Neurosci 25 (2005) 6958-6961
23. Kim T., and Loh Y.P. Protease nexin-1 promotes secretory granule biogenesis by preventing granule protein degradation. Mol Biol Cell 17 (2006) 789-798
24. Mahapatra N.R., O'Connor D.T., Vaingankar S.M., Hikim A.P., Mahata M., Ray S., Staite E., Wu H., Gu Y., Dalton N., et al. Hypertension from targeted ablation of chromogranin A can be rescued by the human ortholog. J Clin Invest 115 (2005) 1942-1952. The authors show that CgA deletion in mice increases adrenal cathecolamine secretion and causes hypertension. These data were validated by the rescue of the phenotype upon reintroduction of the CgA gene.
25. -/- mice, the size and number of their chromaffin SGs was not altered. mRNA and protein levels of other granins were instead upregulated, thereby pointing to a collective role of granins in SG biogenesis and function.
26. Huh Y.H., Jeon S.H., and Yoo S.H. Chromogranin B-induced secretory granule biogenesis: comparison with the similar role of chromogranin A. J Biol Chem 278 (2003) 40581-40589
27. Beuret N., Stettler H., Renold A., Rutishauser J., and Spiess M. Expression of regulated secretory proteins is sufficient to generate granule-like structures in constitutively secreting cells. J Biol Chem 279 (2004) 20242-20249. This study shows that various prohormones are sorted in SG-like vesicles when individually overexpressed in COS-1 fibroblasts, thus indicating that self- aggregation and self-sorting are common properties among cargoes of neuroendocrine SGs.
28. Hosaka M., Watanabe T., Sakai Y., Kato T., and Takeuchi T. Interaction between secretogranin III and carboxypeptidase E facilitates prohormone sorting within secretory granules. J Cell Sci 118 (2005) 4785-4795
29. Malosio M.L., Giordano T., Laslop A., and Meldolesi J. Dense-core granules: a specific hallmark of the neuronal/neurosecretory cell phenotype. J Cell Sci 117 (2004) 743-749
30. Turkewitz A.P. Out with a bang! Tetrahymena as a model system to study secretory granule biogenesis. Traffic 5 (2004) 63-68
31. Bowman G.R., Smith D.G., Michael Siu K.W., Pearlman R.E., and Turkewitz A.P. Genomic and proteomic evidence for a second family of dense core granule cargo proteins in Tetrahymena thermophila. J Eukaryot Microbiol 52 (2005) 291-297
32. Cowan A.T., Bowman G.R., Edwards K.F., Emerson J.J., and Turkewitz A.P. Genetic, genomic, and functional analysis of the granule lattice proteins in Tetrahymena secretory granules. Mol Biol Cell 16 (2005) 4046-4060. The authors demonstrate how genetic screenings in the unicellular organism Tetrahymena termophila can be exploited for the identification and study of proteins involved in SG assembly and function.
33. Webb G.C., Akbar M.S., Zhao C., and Steiner D.F. Expression profiling of pancreatic beta cells: glucose regulation of secretory and metabolic pathway genes. Proc Natl Acad Sci U S A 97 (2000) 5773-5778
34. Grundschober C., Malosio M.L., Astolfi L., Giordano T., Nef P., and Meldolesi J. Neurosecretion competence. A comprehensive gene expression program identified in PC12 cells. J Biol Chem 277 (2002) 36715-36724 LKDJSH
35. Borgonovo B., Racchetti G., Malosio M., Benfante R., Podini P., Rosa P., and Meldolesi J. Neurosecretion competence, an independently regulated trait of the neurosecretory cell phenotype. J Biol Chem 273 (1998) 34683-34686
36. Itoh N., and Okamoto H. Translational control of proinsulin synthesis by glucose. Nature 283 (1980) 100-102
37. Wicksteed B., Herbert T.P., Alarcon C., Lingohr M.K., Moss L.G., and Rhodes C.J. Cooperativity between the preproinsulin mRNA untranslated regions is necessary for glucose-stimulated translation. J Biol Chem 276 (2001) 22553-22558
38. Greenman I.C., Gomez E., Moore C.E., and Herbert T.P. The selective recruitment of mRNA to the ER and an increase in initiation are important for glucose-stimulated proinsulin synthesis in pancreatic β-cells. Biochem J 391 (2005) 291-300. The authors show that glucose stimulation of β-cells prompts the recruitment of ribosome-associated pro-insulin mRNA to the ER. Together with the glucose-independent increased association of ribosomes to ribosome-free mRNA, this process enhances the biosynthesis of insulin, and, conceivably, other SG cargoes.
39. Goodge K.A., and Hutton J.C. Translational regulation of proinsulin biosynthesis and proinsulin conversion in the pancreatic β-cell. Semin Cell Dev Biol 11 (2000) 235-242
40. 2+/μ-calpain-mediated cleavage of ICA512 upon stimulation of insulin secretion. Embo J 20 (2001) 4013-4023
41. Knoch K.P., Bergert H., Borgonovo B., Saeger H.D., Altkruger A., Verkade P., and Solimena M. Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis. Nat Cell Biol 6 (2004) 207-214. The authors shows that glucose-induced nucleocytoplasmic translocation of PTB increases the stability and translation of mRNA for SG genes. This is the first study to provide insight into the molecular mechanisms involved in the rapid post-transcriptional up-regulation of SG biogenesis in response to an agent inducing secretion.
42. Knoch K.P., Meisterfeld R., Kersting S., Bergert H., Altkruger A., Wegbrod C., Jager M., Saeger H.D., and Solimena M. cAMP-dependent phosphorylation of PTB1 promotes the expression of insulin secretory granule proteins in beta cells. Cell Metab 3 (2006) 123-134
43. Tillmar L., Carlsson C., and Welsh N. Control of insulin mRNA stability in rat pancreatic islets. Regulatory role of a 3′-untranslated region pyrimidine-rich sequence. J Biol Chem 277 (2002) 1099-1106
44. Haddad A., and Turkewitz A.P. Analysis of exocytosis mutants indicates close coupling between regulated secretion and transcription activation in Tetrahymena. Proc Natl Acad Sci U S A 94 (1997) 10675-10680
45. Berggren P.O., and Leibiger I.B. Novel aspects on signal-transduction in the pancreatic β-cell. Nutr Metab Cardiovasc Dis 16 Suppl 1 (2006) S7-S10
46. Wicksteed B., Alarcon C., Briaud I., Lingohr M.K., and Rhodes C.J. Glucose-induced translational control of proinsulin biosynthesis is proportional to preproinsulin mRNA levels in islet β-cells but not regulated via a positive feedback of secreted insulin. J Biol Chem 278 (2003) 42080-42090
47. Otani K., Kulkarni R.N., Baldwin A.C., Krutzfeldt J., Ueki K., Stoffel M., Kahn C.R., and Polonsky K.S. Reduced beta-cell mass and altered glucose sensing impair insulin-secretory function in betaIRKO mice. Am J Physiol Endocrinol Metab 286 (2004) E41-E49
48. Lan M.S., Lu J., Goto Y., and Notkins A.L. Molecular cloning and identification of a receptor-type protein tyrosine phosphatase, IA-2, from human insulinoma. DNA Cell Biol 13 (1994) 505-514
49. Solimena M., Dirkx Jr. R., Hermel J.M., Pleasic-Williams S., Shapiro J.A., Caron L., and Rabin D.U. ICA, 512 an autoantigen of type I diabetes, is an intrinsic membrane protein of neurosecretory granules. Embo J 15 (1996) 2102-2114
50. 2+-dependent cleavage of the ICA512/IA-2 cytoplasmic tail following SG exocytosis is targeted to the nucleus where it enhances the expression of SG genes. This novel retrograde pathway can therefore couple granule biogenesis with consumption.
51. Mziaut H., Trajkovski M., Kersting S., Ehninger A., Altkruger A., Lemaitre R.P., Schmidt D., Saeger H.D., Lee M.S., Drechsel D.N., et al. Synergy of glucose and growth hormone signalling in islet cells through ICA512 and STAT5. Nat Cell Biol 8 (2006) 435-445. This study elucidates that the cleaved intracellular fragment of ICA512/IA-2 is a nuclear decoy tyrosine phosphatase that protects STAT5 from tyrosine dephosphorylation, thereby enhancing its transcription of SG genes in pancreatic β-cells.
52. Saeki K., Zhu M., Kubosaki A., Xie J., Lan M.S., and Notkins A.L. Targeted disruption of the protein tyrosine phosphatase-like molecule IA-2 results in alterations in glucose tolerance tests and insulin secretion. Diabetes 51 (2002) 1842-1850
53. Harashima S., Clark A., Christie M.R., and Notkins A.L. The dense core transmembrane vesicle protein IA-2 is a regulator of vesicle number and insulin secretion. Proc Natl Acad Sci U S A 102 (2005) 8704-8709. Evidence for increased or decreased SG number and insulin secretion in mouse insulinoma MIN6 cells transfected with either cDNA or siRNA for ICA512/IA-2, respectively, leads the authors to the conclusion that this gene acts as a regulator of SG number and exocytosis.