A novel role for the centrosomal protein, pericentrin, in regulation of insulin secretory vesicle docking in mouse pancreatic β-cells

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Jurczyk, Agata ^a   Pino, Steven C ^a   O'sullivan Murphy, Bryan ^a   Addorio, Martha ^a   Lidstone, Erich A ^a   Dilorio, Philip ^a   Lipson, Kathryn L ^b   Standley, Clive ^a   Fogarty, Kevin ^a   Lifshitz, Lawrence ^a   Urano, Fumihiko ^a   Mordes, John P ^a   Greiner, Dale L ^a   Rossini, Aldo A ^a   Bortell, Rita ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b WESTERN NEW ENGLAND UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; GLUCOSE; INSULIN; PERICENTRIN; SMALL INTERFERING RNA; ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CENTROSOME; CONTROLLED STUDY; CYTOPLASM; GENE OVEREXPRESSION; GENE SILENCING; GLUCOSE BLOOD LEVEL; HYPOGLYCEMIA; IMPAIRED GLUCOSE TOLERANCE; IN VIVO STUDY; INSULIN RELEASE; MICROTUBULE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PANCREAS ISLET TRANSPLANTATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA INTERFERENCE; SECRETORY VESICLE; STREPTOZOCIN DIABETES; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; MALE; METABOLISM; RADIOIMMUNOASSAY; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; ULTRASTRUCTURE;

ANIMALIA; MUS;

ANIMALS; ANTIGENS; CELL LINE, TUMOR; CENTROSOME; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; RADIOIMMUNOASSAY; RNA, SMALL INTERFERING; SECRETORY VESICLES;

EID: 77955616568     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011812     Document Type: Article

References (43)

1. Daniel S, Noda M, Straub SG, Sharp GW (1999) Identification of the docked granule pool responsible for the first phase of glucose-stimulated insulin secretion. Diabetes 48: 1686-1690.
2. MacDonald PE, JosephJW, Rorsman P (2005) Glucose-sensing mechanisms in pancreatic beta-cells. Philos Trans R Soc Lond B Biol Sci 360: 2211-2225.
3. Kasai K, Fujita T, Gomi H, Izumi T (2008) Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9: 1191-1203.
4. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, et al. (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 104: 19333-19338.
5. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T (2005) Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol 171: 99-109.
6. Jahn R, Sudhof TC (1999) Membrane fusion and exocytosis. Annu Rev Biochem 68: 863-911.
7. Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12: 671-682.
8. Kummel D, Heinemann U (2008) Diversity in structure and function of tethering complexes: evidence for different mechanisms in vesicular transport regulation. Curr Protein Pept Sci 9: 197-209.
9. Gromley A, Yeaman C, Rosa J, Redick S, Chen CT, et al. (2005) Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123: 75-87.
10. Griffith E, Walker S, Martin CA, Vagnarelli P, Stiff T, et al. (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat Genet 40: 232-236.
11. Rauch A, Thiel CT, Schindler D, Wick U, Crow YJ, et al. (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319: 816-819.
12. Willems M, Genevieve D, Borck G, Baumann C, Baujat G, et al. (2009) Molecular analysis of Pericentrin gene (PCNT) in a series of 24 Seckel/MOPD II families. J Med Genet.
13. Doxsey SJ, Stein P, Evans L, Calarco PD, Kirschner M (1994) Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76: 639-650.
14. Flory MR, Davis TN (2003) The centrosomal proteins pericentrin and kendrin are encoded by alternatively spliced products of one gene. Genomics 82: 401-405.
15. Miyoshi K, Asanuma M, Miyazaki I, Matsuzaki S, Tohyama M, et al. (2006) Characterization of pericentrin isoforms in vivo. Biochem Biophys Res Commun 351: 745-749.
16. Dictenberg JB, Zimmerman W, Sparks CA, Young A, Vidair C, et al. (1998) Pericentrin and gamma-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J Cell Biol 141: 163-174.
17. Zimmerman WC, Sillibourne J, Rosa J, Doxsey SJ (2004) Mitosis-specific anchoring of gamma tubulin complexes by pericentrin controls spindle organization and mitotic entry. Mol Biol Cell 15: 3642-3657.
18. Purohit A, Tynan SH, Vallee R, Doxsey SJ (1999) Direct interaction of pericentrin with cytoplasmic dynein light intermediate chain contributes to mitotic spindle organization. J Cell Biol 147: 481-492.
19. Diviani D, Langeberg LK, Doxsey SJ, Scott JD (2000) Pericentrin anchors protein kinase A at the centrosome through a newly identified RII-binding domain. Curr Biol 10: 417-420.
20. Chen D, Purohit A, Halilovic E, Doxsey SJ, Newton AC (2004) Centrosomal anchoring of protein kinase C betaII by pericentrin controls microtubule organization, spindle function, and cytokinesis. J Biol Chem 279: 4829-4839.
21. Miyoshi K, Asanuma M, Miyazaki I, Diaz-Corrales FJ, Katayama T, et al. (2004) DISC1 localizes to the centrosome by binding to kendrin. Biochem Biophys Res Commun 317: 1195-1199.
22. Li Q, Hansen D, Killilea A, Joshi HC, Palazzo RE, et al. (2001) Kendrin/ pericentrin-B, a centrosome protein with homology to pericentrin that complexes with PCM-1. J Cell Sci 114: 797-809.
23. Doxsey S, Zimmerman W, Mikule K (2005) Centrosome control of the cell cycle. Trends Cell Biol 15: 303-311.
24. Young A, Dictenberg JB, Purohit A, Tuft R, Doxsey SJ (2000) Cytoplasmic dynein-mediated assembly ofpericentrin and gamma tubulin onto centrosomes. Mol Biol Cell 11: 2047-2056.
25. Higginbotham H, Bielas S, Tanaka T, Gleeson JG (2004) Transgenic mouse line with green-fluorescent protein-labeled Centrin 2 allows visualization of the centrosome in living cells. Transgenic Res 13: 155-164.
26. Brennand K, Huangfu D, Melton D (2007) All beta cells contribute equally to islet growth and maintenance. PLoS Biol 5: e163.
27. Tsuboi T, Ravier MA, Xie H, Ewart MA, Gould GW, et al. (2005) Mammalian exocyst complex is required for the docking step of insulin vesicle exocytosis. J Biol Chem 280: 25565-25570.
28. Loncarek J, Hergert P, Magidson V, Khodjakov A (2008) Control of daughter centriole formation by the pericentriolar material. Nat Cell Biol 10: 322-328.
29. Varadi A, Tsuboi T, Johnson-Cadwell LI, Allan VJ, Rutter GA (2003) Kinesin I and cytoplasmic dynein orchestrate glucose-stimulated insulin-containing vesicle movements in clonal MIN6 beta-cells. Biochem Biophys Res Commun 311: 272-282.
30. Farshori PQ, Goode D (1994) Effects of the microtubule depolymerizing and stabilizing agents Nocodazole and taxol on glucose-induced insulin secretion from hamster islet tumor (HIT) cells. J Submicrosc Cytol Pathol 26: 137-146.
31. Asanuma N, Kitamura T, Xu X, Sumitani S, Saito H, et al. (2002) New analytical method for pancreas and liver regeneration: normalization of streptozotocin-induced hyperglycemia by retrograde injection of insulin producing cells. Endocr J49: 449-457.
32. Kubo A, Tsukita S (2003) Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J Cell Sci 116: 919-928.
33. Jurczyk A, Gromley A, Redick S, San Agustin J, Witman G, et al. (2004) Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J Cell Biol 166: 637-643.
34. Jewell JL, Luo W, Oh E, Wang Z, Thurmond DC (2008) Filamentous actin regulates insulin exocytosis through direct interaction with Syntaxin 4. J Biol Chem 283: 10716-10726.
35. Miyoshi K, Onishi K, Asanuma M, Miyazaki I, Diaz-Corrales FJ, et al. (2006) Embryonic expression ofpericentrin suggests universal roles in ciliogenesis. Dev Genes Evol 216: 537-542.
36. Endoh-Yamagami S, Karkar KM, May SR, Cobos I, Thwin MT, et al. A mutation in the pericentrin gene causes abnormal interneuron migration to the olfactory bulb in mice. Dev Biol.
37. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, et al. (2003) A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33: 401-406.
38. Parker DC, Greiner DL, Phillips NE, Appel MC, Steele AW, et al. (1995) Survival of mouse pancreatic islet allografts in recipients treated with allogeneic small lymphocytes and antibody to CD40 ligand. Proc Natl Acad Sci U S A 92: 9560-9564.
39. Lipson KL, Fonseca SG, Ishigaki S, Nguyen LX, Foss E, et al. (2006) Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 4: 245-254.
40. Leonard D, Hayakawa A, Lawe D, Lambright D, Bellve KD, et al. (2008) Sorting of EGF and transferrin at the plasma membrane and by cargo-specific signaling to EEA1-enriched endosomes. J Cell Sci 121: 3445-3458.
41. Coda L, Salcini AE, Confalonieri S, Pelicci G, Sorkina T, et al. (1998) Eps15R is a tyrosine kinase substrate with characteristics of a docking protein possibly involved in coated pits-mediated internalization. J Biol Chem 273: 3003-3012.
42. Buchanan TA (2001) Pancreatic B-cell defects in gestational diabetes: implications for the pathogenesis and prevention of type 2 diabetes. J Clin Endocrinol Metab 86: 989-993.
43. Hayat MA (1986) Basic Techniques for Transmission Electron Microscopy; Academic Press I, editor. Orlando.