Pi3K p110α/Akt signaling negatively regulates secretion of the intestinal peptide neurotensin through interference of granule transport

Molecular Endocrinology

Volumn 26, Issue 8, 2012, Pages 1380-1393

  Li, Jing ^a,b   Song, Jun ^a,b   Cassidy, Margaret G ^a,c   Rychahou, Piotr ^a,b   Starr, Marlene E ^a,b   Liu, Jianyu ^b   Li, Xin ^b   Epperly, Garretson ^b   Weiss, Heidi L ^b   Townsend, Courtney M ^b,c   Gao, Tianyan ^a   Mark Evers, B ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; MESSENGER RNA; NEUROTENSIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAB27A PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL LINE; CELL MIGRATION; CELL TRANSPORT; CONTROLLED STUDY; ENDOCRINE CELL; GRANULE CELL; HORMONE RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

MUS;

EID: 84864444538     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1024     Document Type: Article

References (109)

1. Leevers SJ, Vanhaesebroeck B, Waterfield MD 1999 Signalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr Opin Cell Biol 11:219-225
2. Ueki K, Fruman DA, Yballe CM, Fasshauer M, Klein J, Asano T, Cantley LC, Kahn CR 2003 Positive and negative roles of p85 and p85β regulatory subunits of phosphoinositide 3-kinase in insulin signaling. J Biol Chem 278:48453-48466
3. Ma XM, Blenis J 2009 Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307-318
4. Hresko RC, Mueckler M 2005 A mTOR.RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J Biol Chem 280:40406-40416
5. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM 2005 Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098-1101
6. De Camilli P, Emr SD, McPherson PS, Novick P 1996 Phosphoinositides as regulators in membrane traffic. Science 271:1533-1539
7. Corvera S, D'Arrigo A, Stenmark H 1999 Phosphoinositides in membrane traffic. Curr Opin Cell Biol 11:460-465
8. Rameh LE, Cantley LC 1999 The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274:8347-8350
9. Oda H, Murayama T, Nomura Y 1997 Inhibition of protein kinase C-dependent noradrenaline release by wortmannin in PC12 cells. Arch Biochem Biophys 337:96-102
10. Yano H, Nakanishi S, Kimura K, Hanai N, Saitoh Y, Fukui Y, Nonomura Y, Matsuda Y 1993 Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J Biol Chem 268:25846-25856
11. Rao K, Paik WY, Zheng L, Jobin RM, Tomi M, Jiang H, Nakanishi S, Stojilkovic SS 1997 Wortmannin-sensitive and-insensitive steps in calcium-controlled exocytosis in pituitary gonadotrophs: evidence that myosin light chain kinase mediates calcium-dependent and wortmannin-sensitive gonadotropin secretion. Endocrinology 138:1440-1449
12. Folli F, Alvaro D, Gigliozzi A, Bassotti C, Kahn CR, Pontiroli AE, Capocaccia L, Jezequel AM, Benedetti A 1997 Regulation of endocytic-transcytotic pathways and bile secretion by phosphatidylinositol 3-kinase in rats. Gastroenterology 113:954-965
13. Lindmo K, Stenmark H 2006 Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 119:605-614
14. Itakura M, Yamamori S, Kuwahara R, Sekiguchi M, Takahashi M 2005 Two distinct regulatory mechanisms of neurotransmitter release by phosphatidylinositol 3-kinase. J Neurochem 94:502-509
15. Kaneko K, Ueki K, Takahashi N, Hashimoto S, Okamoto M, Awazawa M, Okazaki Y, Ohsugi M, Inabe K, Umehara T, Yoshida M, Kakei M, Kitamura T, Luo J, Kulkarni RN, Kahn CR, Kasai H, Cantley LC, Kadowaki T 2010 Class IA phosphatidylinositol 3-kinase in pancreatic β cells controls insulin secretion by multiple mechanisms. Cell Metab 12:619-632
16. Hagiwara S, Sakurai T, Tashiro F, Hashimoto Y, Matsuda Y, Nonomura Y, Miyazaki J 1995 An inhibitory role for phosphatidylinositol 3-kinase in insulin secretion from pancreatic B cell line MIN6. Biochem Biophys Res Commun 214:51-59
17. Gao Z, Konrad RJ, Collins H, Matschinsky FM, Rothenberg PL, Wolf BA 1996 Wortmannin inhibits insulin secretion in pancreatic islets and β-TC3 cells independent of its inhibition of phosphatidylinositol 3-kinase. Diabetes 45:854-862
18. Leibiger IB, Leibiger B, Moede T, Berggren PO 1998 Exocytosis of insulin promotes insulin gene transcription via the insulin receptor/PI-3 kinase/p70 s6 kinase and CaM kinase pathways. Mol Cell 1:933-938
19. da Silva Xavier G, Varadi A, Ainscow EK, Rutter GA 2000 Regulation of gene expression by glucose in pancreatic β-cells (MIN6) via insulin secretion and activation of phosphatidylinositol 3-kinase. J Biol Chem 275:36269-36277
20. Straub SG, Sharp GW 1996 A wortmannin-sensitive signal transduction pathway is involved in the stimulation of insulin release by vasoactive intestinal polypeptide and pituitary adenylate cyclaseactivating polypeptide. J Biol Chem 271:1660-1668
21. Nunoi K, Yasuda K, Tanaka H, Kubota A, Okamoto Y, Adachi T, Shihara N, Uno M, Xu LM, Kagimoto S, Seino Y, Yamada Y, Tsuda K 2000 Wortmannin, a PI3-kinase inhibitor: promoting effect on insulin secretion from pancreatic β cells through a cAMPdependent pathway. Biochem Biophys Res Commun 270:798-805
22. Zawalich WS, Tesz GJ, Zawalich KC 2002 Inhibitors of phosphatidylinositol 3-kinase amplify insulin release from islets of lean but not obese mice. J Endocrinol 174:247-258
23. Zawalich WS, Zawalich KC 2000 A link between insulin resistance and hyperinsulinemia: inhibitors of phosphatidylinositol 3-kinase augment glucose-induced insulin secretion from islets of lean, but not obese, rats. Endocrinology 141:3287-3295
24. Nogales E 2000 Structural insights into microtubule function. Annu Rev Biochem 69:277-302
25. Kapeller R, Chakrabarti R, Cantley L, Fay F, Corvera S 1993 Internalization of activated platelet-derived growth factor receptorphosphatidylinositol-3 kinase complexes: potential interactions with the microtubule cytoskeleton. Mol Cell Biol 13:6052-6063
26. Kapeller R, Toker A, Cantley LC, Carpenter CL 1995 Phosphoinositide 3-kinase binds constitutively to /β-tubulin and binds to-tubulin in response to insulin. J Biol Chem 270:25985-25991
27. Akiyama H, Kamiguchi H 2010 Phosphatidylinositol 3-kinase facilitates microtubule-dependent membrane transport for neuronal growth cone guidance. J Biol Chem 285:41740-41748
28. Piperno G, LeDizet M, Chang XJ 1987 Microtubules containing acetylatedtubulin in mammalian cells in culture. J Cell Biol 104: 289-302
29. LeDizet M, Piperno G 1987 Identification of an acetylation site of chlamydomonas-tubulin. Proc Natl Acad Sci USA 84:5720-5724
30. MacRae TH 1997 Tubulin post-translational modifications-enzymes and their mechanisms of action. Eur J Biochem 244:265-278
31. Dompierre JP, Godin JD, Charrin BC, Cordelières FP, King SJ, Humbert S, Saudou F 2007 Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27:3571-3583
32. Bulinski JC 2007 Microtubule modification: acetylation speeds anterograde traffic flow. Curr Biol 17:R18-R20
33. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ 2006 Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16:2166-2172
34. Hammond JW, Cai D, Verhey KJ 2008 Tubulin modifications and their cellular functions. Curr Opin Cell Biol 20:71-76
35. Karcher RL, Deacon SW, Gelfand VI 2002 Motor-cargo interactions: the key to transport specificity. Trends Cell Biol 12:21-27
36. Hirokawa N 1998 Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519-526
37. Marx A, Müller J, Mandelkow EM, Hoenger A, Mandelkow E 2006 Interaction of kinesin motors, microtubules, and MAPs. J Muscle Res Cell Motil 27:125-137
38. Verhey KJ, Kaul N, Soppina V 2011 Kinesin assembly and movement in cells. Annu Rev Biophys 40:267-288
39. Rorsman P, Renström E 2003 Insulin granule dynamics in pancreatic β cells. Diabetologia 46:1029-1045
40. Varadi A, Ainscow EK, Allan VJ, Rutter GA 2002 Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic β-cells. J Cell Sci 115: 4177-4189
41. Balczon R, Overstreet KA, Zinkowski RP, Haynes A, Appel M 1992 The identification, purification, and characterization of a pancreatic β-cell form of the microtubule adenosine triphosphatase kinesin. Endocrinology 131:331-336
42. Meng YX, Wilson GW, Avery MC, Varden CH, Balczon R 1997 Suppression of the expression of a pancreatic β-cell form of the kinesin heavy chain by antisense oligonucleotides inhibits insulin secretion from primary cultures of mouse β-cells. Endocrinology 138:1979-1987
43. Montague W, Howell SL, Green IC 1975 Insulin release and the microtubular system of the islets of Langerhans. Identification and characterization of tubulin-like protein. Biochem J 148:237-243
44. Pouli AE, Emmanouilidou E, Zhao C, Wasmeier C, Hutton JC, Rutter GA 1998 Secretory-granule dynamics visualized in vivo with a phogrin-green fluorescent protein chimaera. Biochem J 333(Pt 1):193-199
45. Stinchcombe JC, Barral DC, Mules EH, Booth S, Hume AN, Machesky LM, Seabra MC, Griffiths GM 2001 Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152: 825-834
46. Haddad EK, Wu X, Hammer 3rd JA, Henkart PA 2001 Defective granule exocytosis in Rab27a-deficient lymphocytes from ashen mice. J Cell Biol 152:835-842
47. Chiang L, Ngo J, Schechter JE, Karvar S, Tolmachova T, Seabra MC, Hume AN, Hamm-Alvarez SF 2011 Rab27b regulates exocy-tosis of secretory vesicles in acinar epithelial cells from the lacrimal gland. Am J Physiol Cell Physiol 301:C507-C521
48. Bolasco G, Tracey-White DC, Tolmachova T, Thorley AJ, Tetley TD, Seabra MC, Hume AN 2011 Loss of Rab27 function results in abnormal lung epithelium structure in mice. Am J Physiol Cell Physiol 300:C466-476
49. Johnson JL, Brzezinska AA, Tolmachova T, Munafo DB, Ellis BA, Seabra MC, Hong H, Catz SD 2010 Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic 11:533-547
50. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C 2010 Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12:19-30; sup 11-13
51. Arimura N, Kimura T, Nakamuta S, Taya S, Funahashi Y, Hattori A, Shimada A, Ménager C, Kawabata S, Fujii K, Iwamatsu A, Segal RA, Fukuda M, Kaibuchi K 2009 Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev Cell 16:675-686
52. Tsuboi T, Fukuda M 2006 Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J Cell Sci 119:2196-2203
53. Zhao S, Torii S, Yokota-Hashimoto H, Takeuchi T, Izumi T 2002 Involvement of Rab27b in the regulated secretion of pituitary hormones. Endocrinology 143:1817-1824
54. Waselle L, Coppola T, Fukuda M, Iezzi M, El-Amraoui A, Petit C, Regazzi R 2003 Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol Biol Cell 14:4103-4113
55. Cheviet S, Coppola T, Haynes LP, Burgoyne RD, Regazzi R 2004 The Rab-binding protein Noc2 is associated with insulin-containing secretory granules and is essential for pancreatic β-cell exocytosis. Mol Endocrinol 18:117-126
56. Torii S, Zhao S, Yi Z, Takeuchi T, Izumi T 2002 Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a. Mol Cell Biol 22:5518-5526
57. Izumi T, Gomi H, Kasai K, Mizutani S, Torii S 2003 The roles of Rab27 and its effectors in the regulated secretory pathways. Cell Struct Funct 28:465-474
58. Bracale A, Cesca F, Neubrand VE, Newsome TP, Way M, Schiavo G 2007 Kidins220/ARMS is transported by a kinesin-1-based mechanism likely to be involved in neuronal differentiation. Mol Biol Cell 18:142-152
59. Iglesias T, Cabrera-Poch N, Mitchell MP, Naven TJ, Rozengurt E, Schiavo G 2000 Identification and cloning of Kidins220, a novel neuronal substrate of protein kinase D. J Biol Chem 275:40048-40056
60. Higuero AM, Sánchez-Ruiloba L, Doglio LE, Portillo F, Abad-Rodríguez J, Dotti CG, Iglesias T 2010 Kidins220/ARMS modulates the activity of microtubule-regulating proteins and controls neuronal polarity and development. J Biol Chem 285:1343-1357
61. Evers BM 2006 Neurotensin and growth of normal and neoplastic tissues. Peptides 27:2424-2433
62. Evers BM 2002 Endocrine gene neurotensin: molecular mechanisms and a model of intestinal differentiation. World J Surg 26: 799-805
63. Hyun S, Lee JH, Jin H, Nam J, Namkoong B, Lee G, Chung J, Kim VN 2009 Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139:1096-1108
64. Knight ZA, Gonzalez B, Feldman ME, Zunder ER, Goldenberg DD, Williams O, Loewith R, Stokoe D, Balla A, Toth B, Balla T, Weiss WA, Williams RL, Shokat KM 2006 A pharmacological map of the PI3-K family defines a role for p110 in insulin signaling. Cell 125:733-747
65. Jackson SP, Schoenwaelder SM, Goncalves I, Nesbitt WS, Yap CL, Wright CE, Kenche V, Anderson KE, Dopheide SM, Yuan Y, Sturgeon SA, Prabaharan H, Thompson PE, Smith GD, Shepherd PR, Daniele N, Kulkarni S, Abbott B, Saylik D, Jones C, Lu L, Giuliano S, Hughan SC, Angus JA, Robertson AD, Salem HH 2005 PI 3-kinase p110β: a new target for antithrombotic therapy. Nat Med 11:507-514
66. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB 2005 Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Discov 4:988-1004
67. Barnett SF, Bilodeau MT, Lindsley CW 2005 The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation. Curr Top Med Chem 5:109-125
68. Zhao Z, Leister WH, Robinson RG, Barnett SF, Defeo-Jones D, Jones RE, Hartman GD, Huff JR, Huber HE, Duggan ME, Lindsley CW 2005 Discovery of 2,3,5-trisubstituted pyridine derivatives as potent Akt1 and Akt2 dual inhibitors. Bioorg Med Chem Lett 15: 905-909
69. Calleja V, Laguerre M, Parker PJ, Larijani B 2009 Role of a novel PH-kinase domain interface in PKB/Akt regulation: structural mechanism for allosteric inhibition. PLoS Biol 7:e17
70. Zhu P, Sang Y, Xu R, Zhao J, Li C, Zhao S 2002 The interaction between ADAM22 and 14-3-3β. Sci China C Life Sci 45:577-582
71. Li J, Liu J, Song J, Wang X, Weiss HL, Townsend Jr CM, Gao T, Evers BM 2011 mTORC1 inhibition increases neurotensin secretion and gene expression through activation of the MEK/ERK/c-Jun pathway in the human endocrine cell line BON. Am J Physiol Cell Physiol 301:C213-C226
72. Ohara-Imaizumi M, Nishiwaki C, Kikuta T, Nagai S, Nakamichi Y, Nagamatsu S 2004 TIRF imaging of docking and fusion of single insulin granule motion in primary rat pancreatic β-cells: different behaviour of granule motion between normal and Goto-Kakizaki diabetic rat β-cells. Biochem J 381:13-18
73. Rizzoli SO, Betz WJ 2004 The structural organization of the readily releasable pool of synaptic vesicles. Science 303:2037-2039
74. Horwitz SB 1992 Mechanism of action of taxol. Trends Pharmacol Sci 13:134-136
75. Vasquez RJ, Howell B, Yvon AM, Wadsworth P, Cassimeris L 1997 Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol Biol Cell 8:973-985
76. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP 2002 HDAC6 is a microtubule associated deacetylase. Nature 417:455-458
77. Zhang Y, Li N, Caron C, Matthias G, Hess D, Khochbin S, Matthias P 2003 HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 22:1168-1179
78. Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, Horinouchi S, Yoshida M 2002 In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21: 6820-6831
79. Boyault C, Sadoul K, Pabion M, Khochbin S 2007 HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene 26:5468-5476
80. Kasai K, Ohara-Imaizumi M, Takahashi N, Mizutani S, Zhao S, Kikuta T, Kasai H, Nagamatsu S, Gomi H, Izumi T 2005 Rab27a mediates the tight docking of insulin granules onto the plasma membrane during glucose stimulation. J Clin Invest 115:388-396
81. Li J, Chen LA, Townsend Jr CM, Evers BM 2008 PKD1, PKD2, and their substrate Kidins220 regulate neurotensin secretion in the BON human endocrine cell line. J Biol Chem 283:2614-2621
82. Adler J, Parmryd I 2010 Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry A 77:733-742
83. Eto K, Yamashita T, Tsubamoto Y, Terauchi Y, Hirose K, Kubota N, Yamashita S, Taka J, Satoh S, Sekihara H, Tobe K, Iino M, Noda M, Kimura S, Kadowaki T 2002 Phosphatidylinositol 3-kinase suppresses glucose-stimulated insulin secretion by affecting post-cytosolic [Ca(2)] elevation signals. Diabetes 51:87-97
84. Powis G, Bonjouklian R, Berggren MM, Gallegos A, Abraham R, Ashendel C, Zalkow L, Matter WF, Dodge J, Grindey G, et al 1994 Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res 54:2419-2423
85. Vlahos CJ, Matter WF, Hui KY, Brown RF 1994 A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl4H-1-benzopyran-4-one (LY294002). J Biol Chem 269:5241-5248
86. Ptasznik A, Beattie GM, Mally MI, Cirulli V, Lopez A, Hayek A 1997 Phosphatidylinositol 3-kinase is a negative regulator of cellular differentiation. J Cell Biol 137:1127-1136
87. Kulkarni RN, Brüning JC, Winnay JN, Postic C, Magnuson MA, Kahn CR 1999 Tissue-specific knockout of the insulin receptor in pancreatic β cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 96:329-339
88. Ueki K, Okada T, Hu J, Liew CW, Assmann A, Dahlgren GM, Peters JL, Shackman JG, Zhang M, Artner I, Satin LS, Stein R, Holzenberger M, Kennedy RT, Kahn CR, Kulkarni RN 2006 Total insulin and IGF-I resistance in pancreatic β cells causes overt diabetes. Nat Genet 38:583-588
89. Kulkarni RN, Holzenberger M, Shih DQ, Ozcan U, Stoffel M, Magnuson MA, Kahn CR 2002 β-Cell-specific deletion of the Igf1 receptor leads to hyperinsulinemia and glucose intolerance but does not alter β-cell mass. Nat Genet 31:111-115
90. Kulkarni RN, Winnay JN, Daniels M, Brüning JC, Flier SN, Hanahan D, Kahn CR 1999 Altered function of insulin receptor substrate-1-deficient mouse islets and cultured β-cell lines. J Clin Invest 104:R69-R75
91. Dhakal BK, Mulvey MA 2009 Uropathogenic Escherichia coli invades host cells via an HDAC6-modulated microtubule-dependent pathway. J Biol Chem 284:446-454
92. Chen CS, Weng SC, Tseng PH, Lin HP, Chen CS 2005 Histone acetylation-independent effect of histone deacetylase inhibitors on Akt through the reshuffling of protein phosphatase 1 complexes. J Biol Chem 280:38879-38887
93. Tolmachova T, Anders R, Stinchcombe J, Bossi G, Griffiths GM, Huxley C, Seabra MC 2004 A general role for Rab27a in secretory cells. Mol Biol Cell 15:332-344
94. Aizawa T, Komatsu M 2005 Rab27a: a new face in β cell metabolism-secretion coupling. J Clin Invest 115:227-230
95. Johnson JL, Pacquelet S, Lane WS, Eam B, Catz SD 2005 Akt regulates the subcellular localization of the Rab27a-binding protein JFC1 by phosphorylation. Traffic 6:667-681
96. Yi Z, Yokota H, Torii S, Aoki T, Hosaka M, Zhao S, Takata K, Takeuchi T, Izumi T 2002 The Rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol Cell Biol 22:1858-1867
97. Wang H, Ishizaki R, Kobayashi E, Fujiwara T, Akagawa K, Izumi T 2011 Loss of granuphilin and loss of syntaxin-1A cause differential effects on insulin granule docking and fusion. J Biol Chem 286:32244-32250
98. Torii S, Takeuchi T, Nagamatsu S, Izumi T 2004 Rab27 effector granuphilin promotes the plasma membrane targeting of insulin granules via interaction with syntaxin 1a. J Biol Chem 279:22532-22538
99. Fukuda M, Kanno E, Saegusa C, Ogata Y, Kuroda TS 2002 Slp4a/granuphilin-a regulates dense-core vesicle exocytosis in PC12 cells. J Biol Chem 277:39673-39678
100. Fukuda M 2003 Slp4-a/granuphilin-a inhibits dense-core vesicle exocytosis through interaction with the GDP-bound form of Rab27A in PC12 cells. J Biol Chem 278:15390-15396
101. 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
102. de Oliveira CA, Latorraca MQ, de Mello MA, Carneiro EM 2011 Mechanisms of insulin secretion in malnutrition: modulation by amino acids in rodent models. Amino Acids 40:1027-1034
103. Hou JC, Min L, Pessin JE 2009 Insulin granule biogenesis, trafficking and exocytosis. Vitam Horm 80:473-506
104. Evers BM, Townsend Jr CM, Upp JR, Allen E, Hurlbut SC, Kim SW, Rajaraman S, Singh P, Reubi JC, Thompson JC 1991 Establishment and characterization of a human carcinoid in nude mice and effect of various agents on tumor growth. Gastroenterology 101:303-311
105. Parekh D, Ishizuka J, Townsend Jr CM, Haber B, Beauchamp RD, Karp G, Kim SW, Rajaraman S, Greeley Jr G, Thompson JC 1994 Characterization of a human pancreatic carcinoid in vitro: morphology, amine and peptide storage, and secretion. Pancreas 9:83-90
106. Doihara H, Nozawa K, Kojima R, Kawabata-Shoda E, Yokoyama T, Ito H 2009 QGP-1 cells release 5-HT via TRPA1 activation; a model of human enterochromaffin cells. Mol Cell Biochem 331: 239-245
107. Li J, O'Connor KL, Cheng X, Mei FC, Uchida T, Townsend Jr CM, Evers BM 2007 Cyclic adenosine 5-monophosphate-stimulated neurotensin secretion is mediated through Rap1 downstream of both Epac and protein kinase A signaling pathways. Mol Endocrinol 21:159-171
108. Li J, O'Connor KL, Greeley Jr GH, Blackshear PJ, Townsend Jr CM, Evers BM 2005 Myristoylated alanine-rich C kinase substrate-mediated neurotensin release via protein kinase C-down-stream of the Rho/ROK pathway. J Biol Chem 280:8351-8357
109. Li J, Hellmich MR, Greeley Jr GH, Townsend Jr CM, Evers BM 2002 Phorbol ester-mediated neurotensin secretion is dependent on the PKCand-isoforms. Am J Physiol Gastrointest Liver Physiol 283:G1197-G1206