PKA-independent cAMP stimulation of white adipocyte exocytosis and adipokine secretion: Modulations by Ca2+ and ATP

Journal of Physiology

Volumn 592, Issue 23, 2014, Pages 5169-5186

  Komai, Ali M ^a   Brännmark, Cecilia ^b   Musovic, Saliha ^a   Olofsson, Charlotta S ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b ASTRAZENECA R AND D   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO 2 O METHYLADENOSINE 3',5'CYCLIC MONOPHOSPHATE; 8 BROMOADENOSINE 3',5' CYCLICMONOPHOSPHOROTHIOATE; ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; ADIPOCYTOKINE; APELIN; CALCIUM ION; COMPLEMENT FACTOR D; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC NUCLEOTIDE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; EXCHANGE PROTEIN ACTIVATED BY CAMP; FORSKOLIN; IONOMYCIN; ISOBUTYLMETHYLXANTHINE; LEPTIN; MEMBRANE PROTEIN; PHOSPHODIESTERASE; RESISTIN; UNCLASSIFIED DRUG; ADIPONECTIN; CALCIUM; GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ADULT; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOKINE RELEASE; ELECTRIC CAPACITANCE; ENZYME INHIBITION; EXOCYTOSIS; FEMALE; HORMONE DETERMINATION; HORMONE RELEASE; HUMAN; HUMAN CELL; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; WHITE ADIPOCYTE; 3T3 CELL LINE; ANIMAL; BIOLOGICAL MODEL; CELL SIZE; CYTOLOGY; ENDOCYTOSIS; INTRACELLULAR FLUID; METABOLISM; MOUSE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SECRETION (PROCESS);

3T3-L1 CELLS; ADENOSINE TRIPHOSPHATE; ADIPOCYTES, WHITE; ADIPOKINES; ADIPONECTIN; ANIMALS; CALCIUM; CELL SIZE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOCYTOSIS; EXOCYTOSIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INTRACELLULAR FLUID; MICE; MODELS, BIOLOGICAL; PATCH-CLAMP TECHNIQUES;

EID: 84919348504     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.280388     Document Type: Article

References (68)

1. Alvarez YD & Marengo FD (2011). The immediately releasable vesicle pool: highly coupled secretion in chromaffin and other neuroendocrine cells. J Neurochem 116, 155-163.
2. Astrom-Olsson K, Li L, Olofsson CS, Boren J, Ohlin H & Grip L (2012). Impact of hypoxia, simulated ischemia and reperfusion in HL-1 cells on the expression of FKBP12/FKBP12.6 and intracellular calcium dynamics. Biochem Biophys Res Commun 422, 732-738.
3. 2+ channels accounts for first-phase insulin secretion in mouse beta-cells. Diabetes 51(Suppl. 1), S74-82.
4. Barr VA, Malide D, Zarnowski MJ, Taylor SI & Cushman SW (1997). Insulin stimulates both leptin secretion and production by rat white adipose tissue. Endocrinology 138, 4463-4472.
5. Blumer RM, van Roomen CP, Meijer AJ, Houben-Weerts JH, Sauerwein HP & Dubbelhuis PF (2008). Regulation of adiponectin secretion by insulin and amino acids in 3T3-L1 adipocytes. Metabolism 57, 1655-1662.
6. Bogan JS & Lodish HF (1999). Two compartments for insulin-stimulated exocytosis in 3T3-L1 adipocytes defined by endogenous ACRP30 and GLUT4. J Cell Biol 146, 609-620.
7. Bradley RL & Cheatham B (1999). Regulation of ob gene expression and leptin secretion by insulin and dexamethasone in rat adipocytes. Diabetes 48, 272-278.
8. Burgoyne RD & Morgan A (2003). Secretory granule exocytosis. Physiol Rev 83, 581-632.
9. Carmen GY & Victor SM (2006). Signalling mechanisms regulating lipolysis. Cell Signal 18, 401-408.
10. Chepurny OG, Kelley GG, Dzhura I, Leech CA, Roe MW, Dzhura E, Li X, Schwede F, Genieser HG & Holz GG (2010). PKA-dependent potentiation of glucose-stimulated insulin secretion by Epac activator 8-pCPT-2′-O-Me-cAMP-AM in human islets of Langerhans. Am J Physiol Endocrinol Metab 298, E622-E633.
11. Chowdhury HH, Kreft M & Zorec R (2002). Rapid insulin-induced exocytosis in white rat adipocytes. Pflugers Arch 445, 352-356.
12. Cong L, Chen K, Li J, Gao P, Li Q, Mi S, Wu X & Zhao AZ (2007). Regulation of adiponectin and leptin secretion and expression by insulin through a PI3K-PDE3B dependent mechanism in rat primary adipocytes. Biochem J 403, 519-525.
13. Delporte ML, Funahashi T, Takahashi M, Matsuzawa Y & Brichard SM (2002). Pre- and post-translational negative effect of β-adrenoceptor agonists on adiponectin secretion: in vitro and in vivo studies. Biochem J 367, 677-685.
14. Eliasson L, Ma X, Renstrom E, Barg S, Berggren PO, Galvanovskis J, Gromada J, Jing X, Lundquist I, Salehi A, Sewing S & Rorsman P (2003). SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 121, 181-197.
15. Eliasson L, Proks P, Ammala C, Ashcroft FM, Bokvist K, Renstrom E, Rorsman P & Smith PA (1996). Endocytosis of secretory granules in mouse pancreatic β-cells evoked by transient elevation of cytosolic calcium. J Physiol 493, 755-767.
16. Fasshauer M, Kralisch S, Klier M, Lossner U, Bluher M, Klein J & Paschke R (2003). Adiponectin gene expression and secretion is inhibited by interleukin-6 in 3T3-L1 adipocytes. Biochem Biophys Res Commun 301, 1045-1050.
17. Fu L, Isobe K, Zeng Q, Suzukawa K, Takekoshi K & Kawakami Y (2007). β-adrenoceptor agonists downregulate adiponectin, but upregulate adiponectin receptor 2 and tumor necrosis factor-α expression in adipocytes. Eur J Pharmacol 569, 155-162.
18. Fu Y, Luo N, Klein RL & Garvey WT (2005). Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J Lipid Res 46, 1369-1379.
19. Gao Z, Young RA, Trucco MM, Greene SR, Hewlett EL, Matschinsky FM & Wolf BA (2002). Protein kinase A translocation and insulin secretion in pancreatic β-cells: studies with adenylate cyclase toxin from Bordetella pertussis. Biochem J 368, 397-404.
20. Gauthier MS, Miyoshi H, Souza SC, Cacicedo JM, Saha AK, Greenberg AS & Ruderman NB (2008). AMP-activated protein kinase is activated as a consequence of lipolysis in the adipocyte: potential mechanism and physiological relevance. J Biol Chem 283, 16514-16524.
21. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260, 3440-3450.
22. Herfindal L, Nygaard G, Kopperud R, Krakstad C, Doskeland SO & Selheim F (2013). Off-target effect of the Epac agonist 8-pCPT-2′-O-Me-cAMP on P2Y12 receptors in blood platelets. Biochem Biophys Res Commun 437, 603-608.
23. Hevener AL & Febbraio MA (2009). The 2009 Stock Conference Report: Inflammation, obesity and metabolic disease. Obes Rev 11, 635-644.
24. Hoffstedt J, Arvidsson E, Sjolin E, Wahlen K & Arner P (2004). Adipose tissue adiponectin production and adiponectin serum concentration in human obesity and insulin resistance. J Clin Endocrinol Metab 89, 1391-1396.
25. Huang P, Altshuller YM, Hou JC, Pessin JE & Frohman MA (2005). Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1. Mol Biol Cell 16, 2614-2623.
26. Janke J, Engeli S, Gorzelniak K, Luft FC & Sharma AM (2002). Resistin gene expression in human adipocytes is not related to insulin resistance. Obes Res 10, 1-5.
27. Jernas M, Palming J, Sjoholm K, Jennische E, Svensson PA, Gabrielsson BG, Levin M, Sjogren A, Rudemo M, Lystig TC, Carlsson B, Carlsson LM & Lonn M (2006). Separation of human adipocytes by size: hypertrophic fat cells display distinct gene expression. FASEB J 20, 1540-1542.
28. Juan CC, Chuang TY, Chang CL, Huang SW & Ho LT (2007). Endothelin-1 regulates adiponectin gene expression and secretion in 3T3-L1 adipocytes via distinct signaling pathways. Endocrinology 148, 1835-1842.
29. Kasai H, Takahashi N & Tokumaru H (2012). Distinct initial SNARE configurations underlying the diversity of exocytosis. Physiol Rev 92, 1915-1964.
30. Kitagawa K, Rosen BS, Spiegelman BM, Lienhard GE & Tanner LI (1989). Insulin stimulates the acute release of adipsin from 3T3-L1 adipocytes. Biochim Biophys Acta 1014, 83-89.
31. Kits KS & Mansvelder HD (2000). Regulation of exocytosis in neuroendocrine cells: spatial organization of channels and vesicles, stimulus-secretion coupling, calcium buffers and modulation. Brain Research Brain Research Reviews 33, 78-94.
32. Kohn AD, Summers SA, Birnbaum MJ & Roth RA (1996). Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J Biol Chem 271, 31372-31378.
33. Kovacova Z, Tencerova M, Roussel B, Wedellova Z, Rossmeislova L, Langin D, Polak J & Stich V (2012). The impact of obesity on secretion of adiponectin multimeric isoforms differs in visceral and subcutaneous adipose tissue. Int J Obes (Lond) 36, 1360-1365.
34. Lafontan M, Barbe P, Galitzky J, Tavernier G, Langin D, Carpene C, Bousquet-Melou A & Berlan M (1997). Adrenergic regulation of adipocyte metabolism. Human Reproduction 12 (Suppl. 1), 6-20.
35. Lazar MA (2007). Resistin- and obesity-associated metabolic diseases. Horm Metab Res 39, 710-716.
36. Lindau M & Neher E (1988). Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch 411, 137-146.
37. Liu LB, Omata W, Kojima I & Shibata H (2003). Insulin recruits GLUT4 from distinct compartments via distinct traffic pathways with differential microtubule dependence in rat adipocytes. J Biol Chem 278, 30157-30169.
38. MacDougald OA, Hwang CS, Fan H & Lane MD (1995). Regulated expression of the obese gene product (leptin) in white adipose tissue and 3T3-L1 adipocytes. Proc Natl Acad Sci U S A 92, 9034-9037.
39. Mansvelder HD & Kits KS (1998). The relation of exocytosis and rapid endocytosis to calcium entry evoked by short repetitive depolarizing pulses in rat melanotropic cells. J Neurosci 18, 81-92.
40. Maury E & Brichard SM (2010). Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 314, 1-16.
41. Nakagaki I, Sasaki S, Yahata T, Takasaki H & Hori S (2005). Cytoplasmic and mitochondrial Ca levels in brown adipocytes. Acta Physiol Scand 183, 89-97.
42. Norman D, Isidori AM, Frajese V, Caprio M, Chew SL, Grossman AB, Clark AJ, Michael Besser G & Fabbri A (2003). ACTH and α-MSH inhibit leptin expression and secretion in 3T3-L1 adipocytes: model for a central-peripheral melanocortin-leptin pathway. Mol Cell Endocrinol 200, 99-109.
43. Olofsson CS, Gopel SO, Barg S, Galvanovskis J, Ma X, Salehi A, Rorsman P & Eliasson L (2002). Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells. Pflugers Arch 444, 43-51.
44. - mice due to defective reorganization of the submembrane F-actin network. Endocrinology 150, 3067-3075.
45. Parsons TD, Coorssen JR, Horstmann H & Almers W (1995). Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15, 1085-1096.
46. 2+- and GTP-dependent exocytosis in mouse pancreatic β-cells involves both common and distinct steps. J Physiol 496, 255-264.
47. Ramm G, Slot JW, James DE & Stoorvogel W (2000). Insulin recruits GLUT4 from specialized VAMP2-carrying vesicles as well as from the dynamic endosomal/trans-Golgi network in rat adipocytes. Mol Biol Cell 11, 4079-4091.
48. Renstrom E, Eliasson L & Rorsman P (1997). Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J Physiol 502, 105-118.
49. Robertson RP, Harmon J, Tran PO, Tanaka Y & Takahashi H (2003). Glucose toxicity in β-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 52, 581-587.
50. Roh C, Thoidis G, Farmer SR & Kandror KV (2000). Identification and characterization of leptin-containing intracellular compartment in rat adipose cells. Am J Physiol Endocrinol Metab 279, E893-E899.
51. Rorsman P & Renstrom E (2003). Insulin granule dynamics in pancreatic β-cells. Diabetologia 46, 1029-1045.
52. Seino S & Shibasaki T (2005). PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85, 1303-1342.
53. Skurk T, Alberti-Huber C, Herder C & Hauner H (2007). Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 92, 1023-1033.
54. Spranger J, Kroke A, Mohlig M, Bergmann MM, Ristow M, Boeing H & Pfeiffer AF (2003). Adiponectin and protection against type 2 diabetes mellitus. Lancet 361, 226-228.
55. Stenkula KG, Lizunov VA, Cushman SW & Zimmerberg J (2010). Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab 12, 250-259.
56. Stockli J, Fazakerley DJ & James DE (2011). GLUT4 exocytosis. J Cell Sci 124, 4147-4159.
57. Stralfors P & Honnor RC (1989). Insulin-induced dephosphorylation of hormone-sensitive lipase. Correlation with lipolysis and cAMP-dependent protein kinase activity. Eur J Biochem 182, 379-385.
58. Szaszak M, Christian F, Rosenthal W & Klussmann E (2008). Compartmentalized cAMP signalling in regulated exocytic processes in non-neuronal cells. Cell Signal 20, 590-601.
59. Szkudelski T (2007). Intracellular mediators in regulation of leptin secretion from adipocytes. Physiol Res 56, 503-512.
60. Szkudelski T, Nogowski L & Szkudelska K (2011). Short-term regulation of adiponectin secretion in rat adipocytes. Physiol Res 60, 521-530.
61. Than A, Tee WT & Chen P (2012). Apelin secretion and expression of apelin receptors in 3T3-L1 adipocytes are differentially regulated by angiotensin type 1 and type 2 receptors. Mol Cell Endocrinol 351, 296-305.
62. 2+, exocytosis, and endocytosis in single melanotrophs of the rat pituitary. Neuron 5, 723-733.
63. Trujillo ME & Scherer PE (2006). Adipose tissue-derived factors: impact on health and disease. Endocr Rev 27, 762-778.
64. Valet P, Grujic D, Wade J, Ito M, Zingaretti MC, Soloveva V, Ross SR, Graves RA, Cinti S, Lafontan M & Lowell BB (2000). Expression of human α2-adrenergic receptors in adipose tissue of β3-adrenergic receptor-deficient mice promotes diet-induced obesity. J Biol Chem 275, 34797-34802.
65. van Baak MA (2001). The peripheral sympathetic nervous system in human obesity. Obes Rev 2, 3-14.
66. Xie L, O'Reilly CP, Chapes SK & Mora S (2008). Adiponectin and leptin are secreted through distinct trafficking pathways in adipocytes. Biochim Biophys Acta 1782, 99-108.
67. Ye F, Than A, Zhao Y, Goh KH & Chen P (2010). Vesicular storage, vesicle trafficking, and secretion of leptin and resistin: the similarities, differences, and interplays. J Endocrinol 206, 27-36.
68. Zhong Q, Lin CY, Clarke KJ, Kemppainen RJ, Schwartz DD & Judd RL (2002). Endothelin-1 inhibits resistin secretion in 3T3-L1 adipocytes. Biochem Biophys Res Commun 296, 383-387.