Expression, localization, and functional role for synaptotagmins in pancreatic acinar cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 2, 2011, Pages

  Falkowski, Michelle A ^a   Thomas, Diana D H ^a   Messenger, Scott W ^a   Martin, Thomas F ^a   Groblewski, Guy E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Exocytosis; Zymogen granules

Indexed keywords

ANTIBODY; CALCIUM ION; CHOLECYSTOKININ OCTAPEPTIDE; SYNAPTOBREVIN 2; SYNAPTOTAGMIN; SYNAPTOTAGMIN 3; SYNAPTOTAGMIN 6; SYNAPTOTAGMIN 7; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ACINAR CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOPLASM; EXOCYTOSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELL MEMBRANE; FLUORESCENT ANTIBODY TECHNIQUE; MALE; PANCREAS, EXOCRINE; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SECRETORY VESICLES; SNARE PROTEINS; SYNAPTOTAGMINS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 79961017005     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00108.2011     Document Type: Article

References (62)

1. Bai J, Chapman ER. The C2 domains of synaptotagmin partners in exocytosis. Trends Biochem Sci 29: 143-151, 2004.
2. Braun JE, Fritz BA, Wong SM, Lowe AW. Identification of a vesicleassociated membrane protein (VAMP)-like membrane protein in zymogen granules of the rat exocrine pancreas. J Biol Chem 269: 5328-5335, 1994.
3. Butz S, Fernandez-Chacon R, Schmitz F, Jahn R, Sudhof TC. The subcellular localizations of atypical synaptotagmins III and VI. Synaptotagmin III is enriched in synapses and synaptic plasma membranes but not in synaptic vesicles. J Biol Chem 274: 18290-18296, 1999.
4. Chapman ER. How does synaptotagmin trigger neurotransmitter release Annu Rev Biochem 77: 615-641, 2008.
5. Chen X, Ulintz PJ, Simon ES, Williams JA, Andrews PC. Global topology analysis of pancreatic zymogen granule membrane proteins. Mol Cell Proteomics 7: 2323-2336, 2008.
6. Chen Y, Warner JD, Yule DI, Giovannucci DR. Spatiotemporal analysis of exocytosis in mouse parotid acinar cells. Am J Physiol Cell Physiol 289: C1209-C1219, 2005.
7. 2+/_ mouse parotid acini. Yonsei Med J 49: 311-321, 2008.
8. Falkowski MA, Thomas DD, Groblewski GE. Complexin 2 modulates vesicle-associated membrane protein (VAMP) 2-regulated zymogen granule exocytosis in pancreatic acini. J Biol Chem 285: 35558-35566, 2010.
9. Fukuda M, Mikoshiba K. The function of inositol high polyphosphate binding proteins. Bioessays 19: 593-603, 1997.
10. Fukuda M, Ogata Y, Saegusa C, Kanno E, Mikoshiba K. Alternative splicing isoforms of synaptotagmin VII in the mouse, rat and human. Biochem J 365: 173-180, 2002.
11. Futatsugi A, Nakamura T, Yamada MK, Ebisui E, Nakamura K, Uchida K, Kitaguchi T, Takahashi-Iwanaga H, Noda T, Aruga J, Mikoshiba K. IP3 receptor types 2 and 3 mediate exocrine secretion underlying energy metabolism. Science 309: 2232-2234, 2005.
12. Gaisano HY, Sheu L, Foskett JK, Trimble WS. Tetanus toxin light chain cleaves a vesicle-associated membrane protein (VAMP) isoform 2 in rat pancreatic zymogen granules and inhibits enzyme secretion. J Biol Chem 269: 17062-17066, 1994.
13. Gaisano HY, Sheu L, Grondin G, Ghai M, Bouquillon A, Lowe A, Beaudoin A, Trimble WS. The vesicle-associated membrane protein family of proteins in rat pancreatic and parotid acinar cells. Gastroenterology 111: 1661-1669, 1996.
14. 2+-induced insulin secretion in pancreatic islet beta-cells. J Biol Chem 275: 36079-36085, 2000.
15. Giraudo CG, Eng WS, Melia TJ, Rothman JE. A clamping mechanism involved in SNARE-dependent exocytosis. Science 313: 676-680, 2006.
16. Green SA, Zimmer KP, Griffiths G, Mellman I. Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins. J Cell Biol 105: 1227-1240, 1987.
17. Grimberg E, Peng Z, Hammel I, Sagi-Eisenberg R. Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size. J Cell Sci 116: 145-154, 2003.
18. Groblewski GE, Wishart MJ, Yoshida M, Williams JA. Purification and identification of a 28-kDa calcium-regulated heat-stable protein. A novel secretagogue-regulated phosphoprotein in exocrine pancreas. J Biol Chem 271: 31502-31507, 1996.
19. 2+-induced glucagon exocytosis in pancreas. J Physiol 587:1169-1178, 2009.
20. Gut A, Kiraly CE, Fukuda M, Mikoshiba K, Wollheim CB, Lang J. Expression and localisation of synaptotagmin isoforms in endocrine betacells: their function in insulin exocytosis. J Cell Sci 114: 1709-1716, 2001.
21. Hansen NJ, Antonin W, Edwardson JM. Identification of SNAREs involved in regulated exocytosis in the pancreatic acinar cell. J Biol Chem 274: 22871-22876, 1999.
22. Haucke V, De Camilli P. AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285: 1268-1271, 1999.
23. Heuck AP, Tweten RK, Johnson AE. Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J Biol Chem 278: 31218-31225, 2003.
24. Heuck AP, Tweten RK, Johnson AE. Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40: 9065-9073, 2001.
25. Imai A, Nashida T, Shimomura H. mRNA expression of membranefusion- related proteins in rat parotid gland. Arch Oral Biol 46: 955-962, 2001.
26. 2+-dependent synaptotagmin isoforms in mouse and rat parotid acinar cells. Yonsei Med J 47: 70-77, 2006.
27. Karim S, Essenberg RC, Dillwith JW, Tucker JS, Bowman AS, Sauer JR. Identification of SNARE and cell trafficking regulatory proteins in the salivary glands of the lone star tick, Amblyomma americanum (L.). Insect Biochem Mol Biol 32: 1711-1721, 2002.
28. Levius O, Feinstein N, Linial M. Expression and localization of synaptotagmin I in rat parotid gland. Eur J Cell Biol 73: 81-92, 1997.
29. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375: 594-599, 1995.
30. Llinas RR, Sugimori M, Moran KA, Moreira JE, Fukuda M. Vesicular reuptake inhibition by a synaptotagmin I C2B domain antibody at the squid giant synapse. Proc Natl Acad Sci USA 101: 17855-17860, 2004.
31. Lynch KL, Gerona RR, Kielar DM, Martens S, McMahon HT, Martin TF. Synaptotagmin-1 utilizes membrane bending and SNARE binding to drive fusion pore expansion. Mol Biol Cell 19: 5093-5103, 2008.
32. 2+-triggered vesicle exocytosis. Mol Biol Cell 18: 4957-4968, 2007.
33. 2+-dependent exocytosis of lysosomes in fibroblasts. J Cell Biol 148: 1141-1149, 2000.
34. Michaut M, De Blas G, Tomes CN, Yunes R, Fukuda M, Mayorga LS. Synaptotagmin VI participates in the acrosome reaction of human spermatozoa. Dev Biol 235: 521-529, 2001.
35. Mizuta M, Kurose T, Miki T, Shoji-Kasai Y, Takahashi M, Seino S, Matsukura S. Localization and functional role of synaptotagmin III in insulin secretory vesicles in pancreatic beta-cells. Diabetes 46: 2002-2006, 1997.
36. 2+-induced endocytosis by recruitment of AP2 and clathrin. Am J Physiol Gastrointest Liver Physiol 292: G1549-G1558, 2007.
37. Musch MW, Arvans DL, Wang Y, Nakagawa Y, Solomaha E, Chang EB. Cyclic AMP-mediated endocytosis of intestinal epithelial NHE3 requires binding to synaptotagmin 1. Am J Physiol Gastrointest Liver Physiol 298: G203-G211, 2010.
38. Nicholson-Tomishima K, Ryan TA. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc Natl Acad Sci USA 101: 16648-16652, 2004.
39. 2+-triggered exocytosis. Curr Opin Cell Biol 22: 496-505, 2010.
40. Poskanzer KE, Marek KW, Sweeney ST, Davis GW. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426: 559-563, 2003.
41. 2+-regulated exocytosis of lysosomes. Cell 106: 157-169, 2001.
42. Rindler MJ, Xu CF, Gumper I, Smith NN, Neubert TA. Proteomic analysis of pancreatic zymogen granules: identification of new granule proteins. J Proteome Res 6: 2978-2992, 2007.
43. Segovia M, Ales E, Montes MA, Bonifas I, Jemal I, Lindau M, Maximov A, Sudhof TC, Alvarez de Toledo G. Push-and-pull regulation of the fusion pore by synaptotagmin-7. Proc Natl Acad Sci USA 107: 19032-19037, 2010.
44. Singh P, Asada I, Owlia A, Collins TJ, Thompson JC. Somatostatin inhibits VIP-stimulated amylase release from perifused guinea pig pancreatic acini. Am J Physiol Gastrointest Liver Physiol 254: G217-G223, 1988.
45. Sudhof TC. Synaptotagmins: why so many J Biol Chem 277: 7629-7632, 2002.
46. 2+ sensor in exocytosis. Neuron 30: 459-473, 2001.
47. 2+ affinities. EMBO J 21: 270-280, 2002.
48. 2+ sensitivity of the fusion process. J Cell Sci 118: 2239-2246, 2005.
49. 2+-sensitive CRHSP-28- binding protein in pancreatic acinar cells. J Biol Chem 277: 35496-35502, 2002.
50. 2+-stimulated secretion in permeabilized acinar cells. J Biol Chem 276: 28866-28872, 2001.
51. Thomas DD, Weng N, Groblewski GE. Secretagogue-induced translocation of CRHSP-28 within an early apical endosomal compartment in acinar cells. Am J Physiol Gastrointest Liver Physiol 287: G253-G263, 2004.
52. Tokumaru H, Umayahara K, Pellegrini LL, Ishizuka T, Saisu H, Betz H, Augustine GJ, Snare TA, complex oligomerization by synaphin/ complexin is essential for synaptic vesicle exocytosis. Cell 104: 421-432, 2001.
53. 2+-triggered exocytosis. Biochem J 366: 1-13, 2002.
54. Tucker WC, Edwardson JM, Bai J, Kim HJ, Martin TF, Chapman ER. Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J Cell Biol 162: 199-209, 2003.
55. Ullrich B, Li C, Zhang JZ, McMahon H, Anderson RG, Geppert M, Sudhof TC. Functional properties of multiple synaptotagmins in brain. Neuron 13: 1281-1291, 1994.
56. Walther K, Diril MK, Jung N, Haucke V. Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc Natl Acad Sci USA 101: 964-969, 2004.
57. Wang P, Chicka MC, Bhalla A, Richards DA, Chapman ER. Synaptotagmin VII is targeted to secretory organelles in PC12 cells, where it functions as a high-affinity calcium sensor. Mol Cell Biol 25: 8693-8702, 2005.
58. 2+-dependent secretion from acinar cells. Am J Physiol Gastrointest Liver Physiol 296: G1030-G1039, 2009.
59. Weng N, Thomas DD, Groblewski GE. Pancreatic acinar cells express vesicle-associated membrane protein 2- and 8-specific populations of zymogen granules with distinct and overlapping roles in secretion. J Biol Chem 282: 9635-9645, 2007.
60. 2+ stimulate SNARE-mediated membrane fusion. Nat Struct Mol Biol 15: 707-713, 2008.
61. Zhang JZ, Davletov BA, Sudhof TC, Anderson RG. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78: 751-760, 1994.
62. +/- mice. EMBO J 20: 2680-2689, 2001.