Identification of domains within the V-ATPase accessory subunit Ac45 involved in V-ATPase transport and Ca 2+-dependent exocytosis

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27537-27546

  Jansen, Eric J R ^a   Van Bakel, Nick H M ^a   Olde Loohuis, Nikkie F M ^a   Hafmans, Theo G M ^a   Arentsen, Tim ^a   Coenen, Anthon J M ^a   Scheenen, Wim J J M ^a   Martens, Gerard J M ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACCESSORY SUBUNITS; ACIDIC MICROENVIRONMENT; CELLULAR PHENOTYPES; DELETION MUTANTS; ENDOPLASMIC RETICULUM; FUNCTIONAL DOMAINS; IN-VIVO; INTRACELLULAR ORGANELLE; MEMBRANE FUSION; MEMBRANE-BOUND; N-TERMINAL DOMAINS; PEPTIDE SECRETION; SECRETORY PATHWAYS; TRANSGENICS; TRANSMEMBRANES; V-ATPASE; XENOPUS;

CELL MEMBRANES; ENZYME ACTIVITY; PLANTS (BOTANY);

CALCIUM;

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; PROTEIN AC45; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CELL ISOLATION; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; EXOCYTOSIS; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MELANOTROPH; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN TRANSPORT; WESTERN BLOTTING; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CELL MEMBRANE; ENDOPLASMIC RETICULUM; EXOCYTOSIS; PEPTIDE MAPPING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; SEQUENCE DELETION; VACUOLAR PROTON-TRANSLOCATING ATPASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84864999272     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.356105     Document Type: Article

References (53)

1. Nishi, T., and Forgac, M. (2002) The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3, 94-103
2. Adams, D. S., Robinson, K. R., Fukumoto, T., Yuan, S., Albertson, R. C., Yelick, P., Kuo, L., McSweeney, M., and Levin, M. (2006) Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133, 1657-1671
3. Cruciat, C. M., Ohkawara, B., Acebron, S. P., Karaulanov, E., Reinhard, C., Ingelfinger, D., Boutros, M., and Niehrs, C. (2010) Requirement of pro-renin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling. Science 327, 459-463
4. Wagner, C. A., Finberg, K. E., Breton, S., Marshansky, V., Brown, D., and Geibel, J. P. (2004) Renal vacuolar H+-ATPase. Physiol. Rev. 84, 1263-1314
5. Paroutis, P., Touret, N., and Grinstein, S. (2004) The pH of the secretory pathway: measurement, determinants, and regulation. Physiology 19, 207-215
6. Ungermann, C., Wickner, W., and Xu, Z. (1999) Vacuole acidification is required for trans-SNARE pairing, LMA1 release, and homotypic fusion. Proc. Natl. Acad. Sci. U.S.A. 96, 11194-11199
7. Schoonderwoert, V. T., Holthuis, J. C., Tanaka, S., Tooze, S. A., and Martens, G. J. (2000) Inhibition of the vacuolar H+-ATPase perturbs the transport, sorting, processing, and release of regulated secretory proteins. Eur. J. Biochem. 267, 5646-5654
8. Tanaka, S., Yora, T., Nakayama, K., Inoue, K., and Kurosumi, K. (1997) Proteolytic processing of pro-opiomelanocortin occurs in acidifying secretory granules of AtT-20 cells. J. Histochem. Cytochem. 45, 425-436
9. Camacho, M., Machado, J. D., Montesinos, M. S., Criado, M., and Borges, R. (2006) Intragranular pH rapidly modulates exocytosis in adrenal chromaffin cells. J. Neurochem. 96, 324-334
10. Beyenbach, K. W., and Wieczorek, H. (2006) The V-type H+ ATPase: molecular structure and function, physiological roles, and regulation. J. Exp. Biol. 209, 577-589
11. Peters, C., Bayer, M. J., Bühler, S., Andersen, J. S., Mann, M., and Mayer, A. (2001) Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409, 581-588
12. Hiesinger, P. R., Fayyazuddin, A., Mehta, S. Q., Rosenmund, T., Schulze, K. L., Zhai, R. G., Verstreken, P., Cao, Y., Zhou, Y., Kunz, J., and Bellen, H. J. (2005) The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 121, 607-620
13. Sun-Wada, G. H., Toyomura, T., Murata, Y., Yamamoto, A., Futai, M., and Wada, Y. (2006) The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J. Cell Sci. 119, 4531-4540
14. Liégeois, S., Benedetto, A., Garnier, J. M., Schwab, Y., and Labouesse, M. (2006) The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173, 949-961
15. Zhang, W., Wang, D., Volk, E., Bellen, H. J., Hiesinger, P. R., and Quiocho, F. A. (2008) V-ATPase V0 sector subunit a1 in neurons is a target of calmodulin. J. Biol. Chem. 283, 294-300
16. Di Giovanni, J., Boudkkazi, S., Mochida, S., Bialowas, A., Samari, N., Lévêque, C., Youssouf, F., Brechet, A., Iborra, C., Maulet, Y., Moutot, N., Debanne, D., Seagar, M., and El Far, O. (2010) V-ATPase membrane sector associates with synaptobrevin to modulate neurotransmitter release. Neuron 67, 268-279
17. Sobota, J. A., Bäck, N., Eipper, B. A., and Mains, R. E. (2009) Inhibitors of the V0 subunit of the vacuolar H+-ATPase prevent segregation of lysosomal and secretory pathway proteins. J. Cell Sci. 122, 3542-3553
18. Feng, H., Cheng, T., Pavlos, N. J., Yip, K. H., Carrello, A., Seeber, R., Eidne, K., Zheng, M. H., and Xu, J. (2008) Cytoplasmic terminus of vacuolar type proton pump accessory subunit Ac45 is required for proper interaction with V(0) domain subunits and efficient osteoclastic bone resorption. J. Biol. Chem. 283, 13194-13204
19. Xu, J., Cheng, T., Feng, H. T., Pavlos, N. J., and Zheng, M. H. (2007) Structure and function of V-ATPases in osteoclasts: potential therapeutic targets for the treatment of osteolysis. Histol. Histopathol. 22, 443-454
20. Qin, A., Cheng, T. S., Lin, Z., Pavlos, N. J., Jiang, Q., Xu, J., Dai, K. R., and Zheng, M. H. (2011) Versatile roles of V-ATPases accessory subunit Ac45 in osteoclast formation and function. PLoS One 6, e27155
21. Holthuis, J. C., Jansen, E. J., Schoonderwoert, V. T., Burbach, J. P., and Martens, G. J. (1999) Biosynthesis of the vacuolar H+-ATPase accessory subunit Ac45 in Xenopus pituitary. Eur. J. Biochem. 262, 484-491
22. Holthuis, J. C., Jansen, E. J., van Riel, M. C., and Martens, G. J. (1995) Molecular probing of the secretory pathway in peptide hormone-producing cells. J. Cell Sci. 108, 3295-3305
23. Jansen, E. J., and Martens, G. J. (2012) Novel insights into V-ATPase functioning: distinct roles for its accessory subunits ATP6AP1/Ac45 and ATP6AP2/(pro)renin receptor. Curr. Protein Pept Sci. 13, 124-133
24. Jansen, E. J., Scheenen, W. J., Hafmans, T. G., and Martens, G. J. (2008) Accessory subunit Ac45 controls the V-ATPase in the regulated secretory pathway. Biochim. Biophys. Acta 1783, 2301-2310
25. Jansen, E. J., Hafmans, T. G., and Martens, G. J. (2010) V-ATPase-mediated granular acidification is regulated by the V-ATPase accessory subunit Ac45 in POMC-producing cells. Mol. Biol. Cell 21, 3330-3339
26. Supek, F., Supekova, L., Mandiyan, S., Pan, Y. C., Nelson, H., and Nelson, N. (1994) A novel accessory subunit for vacuolar H(+)-ATPase from chromaffin granules. J. Biol. Chem. 269, 24102-24106
27. Schoonderwoert, V. T., Jansen, E. J., and Martens, G. J. (2002) The fate of newly synthesized V-ATPase accessory subunit Ac45 in the secretory pathway. Eur. J. Biochem. 269, 1844-1853
28. Jansen, E. J., Holthuis, J. C., McGrouther, C., Burbach, J. P., and Martens, G. J. (1998) Intracellular trafficking of the vacuolar H+-ATPase accessory subunit Ac45. J. Cell Sci. 111, 2999-3006
29. Kroll, K. L., and Amaya, E. (1996) Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122, 3173-3183
30. Collin, R. W., and Martens, G. J. (2006) The coding sequence of amyloid-β precursor protein APP contains a neural-specific promoter element. Brain Res. 1087, 41-51
31. Jansen, E. J., Holling, T. M., van Herp, F., and Martens, G. J. (2002) Transgene-driven protein expression specific to the intermediate pituitary melanotrope cells of Xenopus laevis. FEBS Lett. 516, 201-207
32. Cuppen, E., Wijers, M., Schepens, J., Fransen, J., Wieringa, B., and Hendriks, W. (1999) A FERM domain governs apical confinement of PTP-BL in epithelial cells. J. Cell Sci. 112, 3299-3308
33. Berghs, C. A., Tanaka, S., Van Strien, F. J., Kurabuchi, S., and Roubos, E. W. (1997) The secretory granule and pro-opiomelanocortin processing in Xenopus melanotrope cells during background adaptation. J. Histochem. Cytochem. 45, 1673-1682
34. Beggah, A. T., and Geering, K. (1997) α and β subunits of Na, K-ATPase interact with BiP and calnexin. Ann. N.Y. Acad. Sci. 834, 537-539
35. Braks, J. A., and Martens, G. J. (1994) 7B2 is a neuroendocrine chaperone that transiently interacts with prohormone convertase PC2 in the secretory pathway. Cell 78, 263-273
36. Zhang, H. Y., Langeslag, M., Voncken, M., Roubos, E. W., and Scheenen, W. J. (2005) Melanotrope cells of Xenopus laevis express multiple types of high-voltage-activated Ca2+ channels. J. Neuroendocrinol. 17, 1-9
37. Martens, G. J. (1986) Expression of two proopiomelanocortin genes in the pituitary gland of Xenopus laevis: complete structures of the two preprohormones. Nucleic Acids Res. 14, 3791-3798
38. Roubos, E. W. (1997) Background adaptation by Xenopus laevis: a model for studying neuronal information processing in the pituitary pars intermedia. Comp Biochem. Physiol. A. Physiol. 118, 533-550
39. Getlawi, F., Laslop, A., Schägger, H., Ludwig, J., Haywood, J., and Apps, D. (1996) Chromaffin granule membrane glycoprotein IV is identical with Ac45, a membrane-integral subunit of the granule's H(+)-ATPase. Neurosci. Lett. 219, 13-16
40. Scheenen, W. J., Jenks, B. G., Roubos, E. W., and Willems, P. H. (1994) Spontaneous calcium oscillations in Xenopus laevis melanotrope cells are mediated by omega-conotoxin sensitive calcium channels. Cell Calcium 15, 36-44
41. Shibuya, I., and Douglas, W. W. (1993) Spontaneous cytosolic calcium pulsing detected in Xenopus melanotrophs: modulation by secreto-inhibitory and stimulant ligands. Endocrinology 132, 2166-2175
42. Jenks, B. G., Roubos, E. W., and Scheenen, W. J. (2003) Ca2+ oscillations in melanotropes of Xenopus laevis: their generation, propagation, and function. Gen. Comp. Endocrinol. 131, 209-219
43. Louagie, E., Taylor, N. A., Flamez, D., Roebroek, A. J., Bright, N. A., Meulemans, S., Quintens, R., Herrera, P. L., Schuit, F., Van de Ven, W. J., and Creemers, J. W. (2008) Role of furin in granular acidification in the endocrine pancreas: identification of the V-ATPase subunit Ac45 as a candidate substrate. Proc. Natl. Acad. Sci. U.S.A. 105, 12319-12324
44. Thomas, G. (2002) Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3, 753-766
45. Bass, J., Turck, C., Rouard, M., and Steiner, D. F. (2000) Furin-mediated processing in the early secretory pathway: sequential cleavage and degradation of misfolded insulin receptors. Proc. Natl. Acad. Sci. U.S.A. 97, 11905-11909
46. Roth, J. (2002) Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. Chem. Rev. 102, 285-303
47. Alam, M. R., Caldwell, B. D., Johnson, R. C., Darlington, D. N., Mains, R. E., and Eipper, B. A. (1996) Novel proteins that interact with the COOH-terminal cytosolic routing determinants of an integral membrane peptide-processing enzyme. J. Biol. Chem. 271, 28636-28640
48. Mains, R. E., Alam, M. R., Johnson, R. C., Darlington, D. N., Bäck, N., Hand, T. A., and Eipper, B. A. (1999) Kalirin, a multifunctional PAM COOH-terminal domain interactor protein, affects cytoskeletal organization and ACTH secretion from AtT-20 cells. J. Biol. Chem. 274, 2929-2937
49. Burgos, P. V., Mardones, G. A., Rojas, A. L., daSilva, L. L., Prabhu, Y., Hurley, J. H., and Bonifacino, J. S. (2010) Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev. Cell 18, 425-436
50. Kuan, Y. H., Gruebl, T., Soba, P., Eggert, S., Nesic, I., Back, S., Kirsch, J., Beyreuther, K., and Kins, S. (2006) PAT1a modulates intracellular transport and processing of amyloid precursor protein (APP), APLP1, and APLP2. J. Biol. Chem. 281, 40114-40123
51. Lieste, J. R., Koopman, W. J., Reynen, V. C., Scheenen, W. J., Jenks, B. G., and Roubos, E. W. (1998) Action currents generate stepwise intracellular Ca2+ patterns in a neuroendocrine cell. J. Biol. Chem. 273, 25686-25694
52. Zhang, H., Jenks, B. G., Ciccarelli, A., Roubos, E. W., and Scheenen, W. J. (2004) Dopamine D2-receptor activation differentially inhibits N- and R-type Ca2+ channels in Xenopus melanotrope cells. Neuroendocrinology 80, 368-378
53. Van Herp, F., Coenen, T., Geurts, H. P., Janssen, G. J., and Martens, G. J. (2005) A fast method to study the secretory activity of neuroendocrine cells at the ultrastructural level. J. Microsc. 218, 79-83