Impaired maturation of large dense-core vesicles in muted-deficient adrenal chromaffin cells

Journal of Cell Science

Volumn 128, Issue 7, 2015, Pages 1365-1374

  Hao, Zhenhua ^a,b   Wei, Lisi ^c   Feng, Yaqin ^a,d   Chen, Xiaowei ^c   Du, Wen ^e   Ma, Jing ^a   Zhou, Zhuan ^c   Chen, Liangyi ^c   Li, Wei ^a,f  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c PEKING UNIVERSITY   (China)

^d SHANXI MEDICAL UNIVERSITY   (China)

^e INSTITUTE OF BIOPHYSICS   (China)

^f BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

BLOC 1; CgA; Hermansky Pudlak syndrome; Large dense core vesicle; Muted protein

Indexed keywords

BIOGENESIS OF LYSOSOME RELATED ORGANELLES COMPLEX 1; CHROMOGRANIN A; PROTEIN; UNCLASSIFIED DRUG; MUTED PROTEIN, MOUSE; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL MATURATION; CELL ORGANELLE; CELL STRUCTURE; CHROMAFFIN CELL; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE; GENE MUTATION; LARGE DENSE CORE VESICLE; LYSOSOME; MALE; MOLECULAR BIOLOGY; MOUSE; MU GENE; MUTED GENE; NONHUMAN; OCULAR ALBINISM; PC12 CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADRENAL GLAND; ANIMAL; C57BL MOUSE; CYTOLOGY; DBA MOUSE; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; PROTEIN TRANSPORT; SECRETORY VESICLE; TRANSPORT AT THE CELLULAR LEVEL;

MUS;

ADRENAL GLANDS; ANIMALS; BIOLOGICAL TRANSPORT; CHROMAFFIN CELLS; CHROMOGRANIN A; DISEASE MODELS, ANIMAL; HERMANSKI-PUDLAK SYNDROME; HUMANS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; PROTEIN TRANSPORT; SECRETORY VESICLES; VESICULAR TRANSPORT PROTEINS;

EID: 84928669416     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.161414     Document Type: Article

References (50)

1. Angers, C. G. and Merz, A. J. (2009). HOPS interacts with Apl5 at the vacuole membrane and is required for consumption of AP-3 transport vesicles. Mol. Biol. Cell 20, 4563-4574.
2. Arvan, P. and Castle, D. (1998). Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem. J. 332, 593-610.
3. Asensio, C. S., Sirkis, D. W. and Edwards, R. H. (2010). RNAi screen identifies a role for adaptor protein AP-3 in sorting to the regulated secretory pathway. J. Cell Biol. 191, 1173-1187.
4. Asensio, C. S., Sirkis, D. W., Maas, J. W., Jr, Egami, K., To, T. L., Brodsky, F. M., Shu, X., Cheng, Y. and Edwards, R. H. (2013). Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway. Dev. Cell 27, 425-437.
5. Cai, Q., Lu, L., Tian, J. H., Zhu, Y. B., Qiao, H. and Sheng, Z. H. (2010). Snapinregulated late endosomal transport is critical for efficient autophagy-lysosomal function in neurons. Neuron 68, 73-86.
6. Chen, X.W., Feng, Y. Q., Hao, C. J., Guo, X. L., He, X., Zhou, Z. Y., Guo, N., Huang, H. P., Xiong, W., Zheng, H. et al. (2008). DTNBP1, a schizophrenia susceptibility gene, affects kinetics of transmitter release. J. Cell Biol. 181, 791-801.
7. Ciciotte, S. L., Gwynn, B., Moriyama, K., Huizing, M., Gahl, W. A., Bonifacino, J. S. and Peters, L. L. (2003). Cappuccino, a mouse model of Hermansky-Pudlak syndrome, encodes a novel protein that is part of the pallidin-muted complex (BLOC-1). Blood 101, 4402-4407.
8. Duncan, R. R., Greaves, J., Wiegand, U. K., Matskevich, I., Bodammer, G., Apps, D. K., Shipston, M. J. and Chow, R. H. (2003). Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422, 176-180.
9. Falcón-Pérez, J. M., Starcevic, M., Gautam, R. and Dell'Angelica, E. C. (2002). BLOC-1, a novel complex containing the pallidin and muted proteins involved in the biogenesis of melanosomes and platelet-dense granules. J. Biol. Chem. 277,28191-28199.
10. Feng, Y. Q., Zhou, Z. Y., He, X., Wang, H., Guo, X. L., Hao, C. J., Guo, Y., Zhen, X. C. and Li, W. (2008). Dysbindin deficiency in sandy mice causes reduction of snapin and displays behaviors related to schizophrenia. Schizophr. Res. 106, 218-228.
11. Gerrish, A., Williams, H., Moskvina, V., Owen, M. J., O'Donovan, M. C. and Williams, N. M. (2009). An examination of MUTED as a schizophrenia susceptibility gene. Schizophr. Res. 107, 110-111.
12. Ghiani, C. A. and Dell'Angelica, E. C. (2011). Dysbindin-containing complexes and their proposed functions in brain: from zero to (too) many in a decade. ASN Neuro 3, e00058.
13. Grabner, C. P., Price, S. D., Lysakowski, A. and Fox, A. P. (2005). Mouse chromaffin cells have two populations of dense core vesicles. J. Neurophysiol. 94,2093-2104.
14. Grabner, C. P., Price, S. D., Lysakowski, A., Cahill, A. L. and Fox, A. P. (2006). Regulation of large dense-core vesicle volume and neurotransmitter content mediated by adaptor protein 3. Proc. Natl. Acad. Sci. USA 103, 10035-10040.
15. Gwynn, B., Martina, J. A., Bonifacino, J. S., Sviderskaya, E. V., Lamoreux, M. L., Bennett, D. C., Moriyama, K., Huizing, M., Helip-Wooley, A., Gahl, W. A. et al. (2004). Reduced pigmentation (rp), a mouse model of Hermansky-Pudlak syndrome, encodes a novel component of the BLOC-1 complex. Blood 104, 3181-3189.
16. Hayes, M. J., Bryon, K., Satkurunathan, J. and Levine, T. P. (2011). Yeast homologues of three BLOC-1 subunits highlight KxDL proteins as conserved interactors of BLOC-1. Traffic 12, 260-268.
17. John Peter, A. T., Lachmann, J., Rana, M., Bunge, M., Cabrera, M. and Ungermann, C. (2013). The BLOC-1 complex promotes endosomal maturation by recruiting the Rab5 GTPase-activating protein Msb3. J. Cell Biol. 201, 97-111.
18. Kim, T., Tao-Cheng, J. H., Eiden, L. E. and Loh, Y. P. (2001). Chromogranin A, an "on/off" switch controlling dense-core secretory granule biogenesis. Cell 106, 499-509.
19. Kim, T., Gondré-Lewis, M. C., Arnaoutova, I. and Loh, Y. P. (2006). Dense-core secretory granule biogenesis. Physiology (Bethesda) 21, 124-133.
20. Koshimizu, H., Kim, T., Cawley, N. X. and Loh, Y. P. (2010). Chromogranin A: a new proposal for trafficking, processing and induction of granule biogenesis. Regul. Pept. 160, 153-159.
21. Li, W., Zhang, Q., Oiso, N., Novak, E. K., Gautam, R., O'Brien, E. P., Tinsley, C. L., Blake, D. J., Spritz, R. A., Copeland, N. G. et al. (2003). Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat. Genet. 35,84-89.
22. Li, W., Rusiniak, M. E., Chintala, S., Gautam, R., Novak, E. K. and Swank, R. T. (2004). Murine Hermansky-Pudlak syndrome genes: regulators of lysosome-related organelles. BioEssays 26, 616-628.
23. Li, W., Feng, Y., Hao, C., Guo, X., Cui, Y., He, M. and He, X. (2007). The BLOC interactomes form a network in endosomal transport. J. Genet. Genomics 34, 669-682.
24. Mahapatra, N. R., O'Connor, D. T., Vaingankar, S. M., Hikim, A. P., Mahata, M., Ray, S., Staite, E., Wu, H., Gu, Y., Dalton, N. et al. (2005). Hypertension from targeted ablation of chromogranin A can be rescued by the human ortholog. J. Clin. Invest. 115, 1942-1952.
25. Morris, D. W., Murphy, K., Kenny, N., Purcell, S. M., McGhee, K. A., Schwaiger, S., Nangle, J. M., Donohoe, G., Clarke, S., Scully, P. et al. (2008). Dysbindin (DTNBP1) and the biogenesis of lysosome-related organelles complex 1 (BLOC-1): main and epistatic gene effects are potential contributors to schizophrenia susceptibility. Biol. Psychiatry 63, 24-31.
26. Orci, L., Ravazzola, M., Amherdt, M., Louvard, D. and Perrelet, A. (1985a). Clathrin-immunoreactive sites in the Golgi apparatus are concentrated at the trans pole in polypeptide hormone-secreting cells. Proc. Natl. Acad. Sci. USA 82,5385-5389.
27. Orci, L., Ravazzola, M., Amherdt, M., Madsen, O., Vassalli, J. D. and Perrelet, A. (1985b). Direct identification of prohormone conversion site in insulinsecreting cells. Cell 42, 671-681.
28. Pan, P. Y., Tian, J. H. and Sheng, Z. H. (2009). Snapin facilitates the synchronization of synaptic vesicle fusion. Neuron 61, 412-424.
29. Portela-Gomes, G. M. and Stridsberg, M. (2001). Selective processing of chromogranin A in the different islet cells in human pancreas. J. Histochem. Cytochem. 49, 483-490.
30. Rehling, P., Darsow, T., Katzmann, D. J. and Emr, S. D. (1999). Formation of AP-3 transport intermediates requires Vps41 function. Nat. Cell Biol. 1, 346-353.
31. Scott, I., Webster, B. R., Chan, C. K., Okonkwo, J. U., Han, K. and Sack, M. N. (2014). GCN5-like protein 1 (GCN5L1) controls mitochondrial content through coordinated regulation of mitochondrial biogenesis and mitophagy. J. Biol. Chem. 289, 2864-2872.
32. Sørensen, J. B., Nagy, G., Varoqueaux, F., Nehring, R. B., Brose, N., Wilson, M. C. and Neher, E. (2003). Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 114, 75-86.
33. Starcevic, M. and Dell'Angelica, E. C. (2004). Identification of snapin and three novel proteins (BLOS1, BLOS2, and BLOS3/reduced pigmentation) as subunits of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J. Biol. Chem. 279, 28393-28401.
34. Swank, R. T., Novak, E. K., McGarry, M. P., Rusiniak, M. E. and Feng, L. (1998). Mouse models of Hermansky Pudlak syndrome: a review. Pigment Cell Res. 11, 60-80.
35. Talbot, K., Ong, W. Y., Blake, D. J., Tang, J., Louneva, N., Carlson, G. C. and Arnold, S. E. (2009). Dysbindin-1 and its protein family with special attention to the potential role of dysbindin-1 in neuronal functions and the pathophysiology of schizophrenia. In Handbook of Neurochemistry and Molecular Neurobiology: Schizophrenia, 3rd edn, Vol. 27 (ed. D. Javitt and J. Kantrowitz), pp. 107-241. New York, NY: Springer Science.
36. Tian, J. H., Wu, Z. X., Unzicker, M., Lu, L., Cai, Q., Li, C., Schirra, C., Matti, U., Stevens, D., Deng, C. et al. (2005). The role of Snapin in neurosecretion: snapin knock-out mice exhibit impaired calcium-dependent exocytosis of large dense-core vesicles in chromaffin cells. J. Neurosci. 25, 10546-10555.
37. Tooze, J. and Tooze, S. A. (1986). Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. J. Cell Biol. 103, 839-850.
38. Tooze, S. A., Martens, G. J. and Huttner, W. B. (2001). Secretory granule biogenesis: rafting to the SNARE. Trends Cell Biol. 11, 116-122.
39. Voets, T., Neher, E. and Moser, T. (1999). Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23, 607-615.
40. Walter, A. M., Kurps, J., de Wit, H., Schöning, S., Toft-Bertelsen, T. L., Lauks, J., Ziomkiewicz, I., Weiss, A. N., Schulz, A., Fischer von Mollard, G. et al. (2014). The SNARE protein vti1a functions in dense-core vesicle biogenesis. EMBO J. 33, 1681-1697.
41. Wang, H., Yuan, Y., Zhang, Z., Yan, H., Feng, Y. and Li, W. (2014). Dysbindin-1C is required for the survival of hilar mossy cells and the maturation of adult newborn neurons in dentate gyrus. J. Biol. Chem. 289, 29060-29072.
42. Watanabe, T., Uchiyama, Y. and Grube, D. (1991). Topology of chromogranin A and secretogranin II in the rat anterior pituitary: potential marker proteins for distinct secretory pathways in gonadotrophs. Histochemistry 96, 285-293.
43. Wei, A. H. and Li, W. (2013). Hermansky-Pudlak syndrome: pigmentary and nonpigmentary defects and their pathogenesis. Pigment Cell Melanoma Res. 26, 176-192.
44. Wilkin, M., Tongngok, P., Gensch, N., Clemence, S., Motoki, M., Yamada, K., Hori, K., Taniguchi-Kanai, M., Franklin, E., Matsuno, K. et al. (2008). Drosophila HOPS and AP-3 complex genes are required for a Deltex-regulated activation of notch in the endosomal trafficking pathway. Dev. Cell 15, 762-772.
45. Yang, Q., He, X., Yang, L., Zhou, Z., Cullinane, A. R., Wei, A., Zhang, Z., Hao, Z., Zhang, A., He, M. et al. (2012). The BLOS1-interacting protein KXD1 is involved in the biogenesis of lysosome-related organelles. Traffic 13, 1160-1169.
46. Yu, Y., Wang, L., Jiu, Y., Zhan, Y., Liu, L., Xia, Z., Song, E., Xu, P. and Xu, T. (2011). HID-1 is a novel player in the regulation of neuropeptide sorting. Biochem. J. 434, 383-390.
47. Yuan, Y., Wang, H., Wei, Z. and Li, W. (2015). Impaired autophagy in hilar mossy cells of the dentate gyrus and its implication in schizophrenia. J. Genet. Genomics 42, 1-8.
48. Zhang, Q., Li, W., Novak, E. K., Karim, A., Mishra, V. S., Kingsmore, S. F., Roe, B. A., Suzuki, T. and Swank, R. T. (2002). The gene for the muted (mu) mouse, a model for Hermansky-Pudlak syndrome, defines a novel protein which regulates vesicle trafficking. Hum. Mol. Genet. 11, 697-706.
49. Zhang, A., He, X., Zhang, L., Yang, L., Woodman, P. and Li, W. (2014). Biogenesis of lysosome-related organelles complex-1 subunit 1 (BLOS1) interacts with sorting nexin 2 and the endosomal sorting complex required for transport-I (ESCRT-I) component TSG101 to mediate the sorting of epidermal growth factor receptor into endosomal compartments. J. Biol. Chem. 289, 29180-29194.
50. Zhou, Z. and Misler, S. (1996). Amperometric detection of quantal secretion from patch-clamped rat pancreatic beta-cells. J. Biol. Chem. 271, 270-277.