Enlargeosome traffic: Exocytosis triggered by various signals is followed by endocytosis, membrane shedding or both

Traffic

Volumn 8, Issue 6, 2007, Pages 742-757

  Cocucci, Emanuele ^a   Racchetti, Gabriella ^b   Podini, Paola ^b   Meldolesi, Jacopo ^a,b,c,d  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c Istituto Nazionale di Neuroscienze   (Italy)

^d Research Unit of Molecular Neuroscience   (Italy)

Author keywords

ATP; Desmoyokin Ahnak; Detergent resistance; Endocytosis; Exocytosis; Ionomycin; Membrane shedding; P2Y receptors; PC12 27; PMA

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM IONOPHORE; FORMALDEHYDE; IONOMYCIN; PEROXIDASE; PHORBOL 13 ACETATE 12 MYRISTATE; PHORBOL ESTER; PURINE P2Y RECEPTOR; TRITON X 100;

ANIMAL CELL; ARTICLE; CELL LABELING; CELL MEMBRANE; CELL ORGANELLE; CELL STRAIN; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM VESICLE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; ENLARGEOSOME; EXOCYTOSIS; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CLONE CELLS; DETERGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; ENDOSOMES; EXOCYTOSIS; INTRACELLULAR MEMBRANES; IONOMYCIN; IONOPHORES; PC12 CELLS; RATS; TETRADECANOYLPHORBOL ACETATE;

EID: 34249035506     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00566.x     Document Type: Article

References (40)

1. Chieregatti E, Meldolesi J. Regulated exocytosis: New organelles for non-secretory purposes. Nat Rev Mol Cell Biol 2005; 6: 181-187.
2. Kasai H, Kishimoto T, Liu TT, Miyashita Y, Podini P, Grohovaz F, Meldolesi J. Multiple and diverse forms of regulated exocytosis in wild-type and defective PC12 cells. Proc Natl Acad Sci U S A 1999; 96: 945-949.
3. Borgonovo B, Cocucci E, Racchetti G, Podini P, Bachi A, Meldolesi J. Regulated exocytosis: A novel, widely expressed system. Nat Cell Biol 2002; 4: 955-962.
4. Cocucci E, Racchetti G, Podini P, Rupnik M, Meldolesi J. Enlargeosome, an exocytic vesicle resistant to nonionic detergents, undergoes endocytosis via a nonacidic route. Mol Biol Cell 2004; 15: 5356-5368.
5. Falcone S, Cocucci E, Podini P, Kirchhausen T, Clementi E, Meldolesi J. Macropinocytosis: Regulated coordination of endocytic and exocytic membrane traffic events. J Cell Sci 2006; 119: 4758-4769.
6. Lorusso A, Covino C, Priori G, Bachi A, Meldolesi J, Chieregatti E. Annexin2 coating the surface of enlargeosomes is needed for their regulated exocytosis. EMBO J 2006; 25: 5443-5456.
7. Shtivelman E, Bishop JM. The human gene AHNAK encodes a large phosphoprotein located primarily in the nucleus. J Cell Biol 1993; 120: 625-630.
8. Gentil BJ, Delphin C, Benaud C, Baudier J. Expression of the giant protein AHNAK (desmoyokin) in muscle and lining epithelial cells. J Histochem Cytochem 2003; 51: 339-348.
9. Parsons TD, Coorssen JR, Horstmann H, Almers W. Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 1995; 15: 1085-1096.
10. Malosio ML, Benfante R, Racchetti G, Borgonovo B, Rosa P, Meldolesi J. Neurosecretory cells without neurosecretion: Evidence of an independently regulated trait of the cell phenotype. J Physiol 1999; 520: 43-52.
11. Grundschober C, Malosio ML, Astolfi L, Giordano T, Nef P, Meldolesi J. Neurosecretion competence. A comprehensive gene expression program identified in PC12 cells. J Biol Chem 2002; 277: 36715-36724.
12. Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 2004; 27: 509-547.
13. Wooten MW. Differential expression of PKC isoforms and PC12 cell differentiation. Exp Cell Res 1992; 199: 111-119.
14. Wooten MW, Seibenhener ML, Neidigh KB, Vandenplas ML. Mapping of atypical protein kinase C within the nerve growth factor signaling cascade: relationship to differentiation and survival of PC12 cells. Mol Cell Biol 2000; 20: 4494-4504.
15. 2 homeostasis studied by videoimaging. Pharmacol Res 1992; 25: 93-94.
16. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA. International Union of Pharmacology LVIII: Update on the P2Y G protein-coupled nucleotide receptors: From molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 2006; 58: 281-341.
17. Pizzirani C, Ferrari D, Chiozzi P, Adinolfi E, Sandona D, Savaglio E, Di Virgilio F. Stimulation of P2 receptors causes release of IL-1{beta}-loaded microvesicles from human dendritic cells. Blood 2007, in press.
18. Kishimoto T, Liu TT, Hatakeyama H, Nemoto T, Takahashi N, Kasai H. Sequential compound exocytosis of large dense-core vesicles in PC12 cells studied with TEPIQ (two-photon extracellular polar-tracer imaging-based quantification) analysis. J Physiol 2005; 568: 905-915.
19. Graham RC Jr, Karnovsky MJ. Glomerular permeability. Ultrastructural cytochemical studies using peroxidases as protein tracers. J Exp Med 1966; 124: 1123-1134.
20. Ceccarelli B, Hurlbut WP, Mauro A. Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J Cell Biol 1972; 54: 30-38.
21. Jacobson KA, Costanzi S, Ohno M, Joshi BV, Besada P, Xu B, Tchilibon S. Molecular recognition at purine and pyrimidine nucleotide (P2) receptors. Curr Top Med Chem 2004; 4: 671-686.
22. Nagy G, Matti U, Nehring RB, Binz T, Rettig J, Neher E, Sorensen JB. Protein kinase C-dependent phosphorylation of synaptosome-associated protein of 25 kDa at Ser187 potentiates vesicle recruitment. J Neurosci 2002; 22: 9278-9286.
23. Polgar J, Lane WS, Chung SH, Houng AK, Reed GL. Phosphorylation of SNAP-23 in activated human platelets. J Biol Chem 2003; 278: 44369-44376.
24. Morgan A, Burgoyne RD, Barclay JW, Craig TJ, Prescott GR, Ciufo LF, Evans GJ, Graham ME. Regulation of exocytosis by protein kinase C. Biochem Soc Trans 2005; 33: 1341-1344.
25. Ashery U, Varoqueaux F, Voets T, Betz A, Thakur P, Koch H, Neher E, Brose N, Rettig J. Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J 2000; 19: 3586-3596.
26. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Sudhof TC, Takahashi M, Rosenmund C, Brose N. Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 2002; 108: 121-133.
27. Brose N, Rosenmund C. Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci 2002; 115: 4399-4411.
28. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004; 5: 121-132.
29. Harata NC, Aravanis AM, Tsien RW. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J Neurochem 2006; 97: 1546-1570.
30. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: Two sides of the coin. Physiology (Bethesda) 2005; 20: 22-27.
31. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: Important and underappreciated mediators of cell-to-cell communication. Leukemia 2006; 20: 1487-1495.
32. Dolo V, Ginestra A, Cassara D, Violini S, Lucania G, Torrisi MR, Nagase H, Canevari S, Pavan A, Vittorelli ML. Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells. Cancer Res 1998; 58: 4468-4474.
33. Dolo V, Li R, Dillinger M, Flati S, Manela J, Taylor BJ, Pavan A, Ladisch S. Enrichment and localization of ganglioside G(D3) and caveolin-1 in shed tumor cell membrane vesicles. Biochim Biophys Acta 2000; 1486: 265-274.
34. Taverna S, Ghersi G, Ginestra A, Rigogliuso S, Pecorella S, Alaimo G, Saladino F, Dolo V, Dell'Era P, Pavan A, Pizzolanti G, Mignatti P, Presta M, Vittorelli ML. Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells. J Biol Chem 2003; 278: 51911-51919.
35. Gutwein P, Mechtersheimer S, Riedle S, Stoeck A, Gast D, Joumaa S, Zentgraf H, Fogel M, Altevogt DP. ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB J 2003; 17: 292-294.
36. Bianco F, Pravettoni E, Colombo A, Schenk U, Moller T, Matteoli M, Verderio C. Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J Immunol 2005; 174: 7268-7277.
37. Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106: 1604-1611.
38. Pilzer D, Fishelson Z. Mortalin/GRP75 promotes release of membrane vesicles from immune attacked cells and protection from complement-mediated lysis. Int Immunol 2005; 17: 1239-1248.
39. van der Wijk T, Tomassen SF, Houtsmuller AB, de Jonge HR, Tilly BC. Increased vesicle recycling in response to osmotic cell swelling. Cause and consequence of hypotonicity-provoked ATP release. J Biol Chem 2003; 278: 40020-40025.
40. Ochs RL, Press RI. Centromere autoantigens are associated with the nucleolus. Exp Cell Res 1992; 200: 339-350.