Identification of the Functional Domain of the Dense Core Vesicle Biogenesis Factor HID-1

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2023 Sep 26

PMID 37751424

Authors

Blake H Hummer

Theodore Carter

Breanna L Sellers

Jenna D Triplett

Cedric S Asensio

Affiliations

Soon will be listed here.

Abstract

Large dense core vesicles (LDCVs) mediate the regulated release of neuropeptides and peptide hormones. HID-1 is a trans-Golgi network (TGN) localized peripheral membrane protein contributing to LDCV formation. There is no information about HID-1 structure or domain architecture, and thus it remains unknown how HID-1 binds to the TGN and performs its function. We report that the N-terminus of HID-1 mediates membrane binding through a myristoyl group with a polybasic amino acid patch but lacks specificity for the TGN. In addition, we show that the C-terminus serves as the functional domain. Indeed, this isolated domain, when tethered to the TGN, can rescue the neuroendocrine secretion and sorting defects observed in HID-1 KO cells. Finally, we report that a point mutation within that domain, identified in patients with endocrine and neurological deficits, leads to loss of function.

References

Monies D, Abouelhoda M, AlSayed M, Alhassnan Z, Alotaibi M, Kayyali H . The landscape of genetic diseases in Saudi Arabia based on the first 1000 diagnostic panels and exomes. Hum Genet. 2017; 136(8):921-939. PMC: 5502059. DOI: 10.1007/s00439-017-1821-8. View

Hummer B, de Leeuw N, Burns C, Chen L, Joens M, Hosford B . HID-1 controls formation of large dense core vesicles by influencing cargo sorting and -Golgi network acidification. Mol Biol Cell. 2017; 28(26):3870-3880. PMC: 5739301. DOI: 10.1091/mbc.E17-08-0491. View

Lundmark R, Doherty G, Vallis Y, Peter B, McMahon H . Arf family GTP loading is activated by, and generates, positive membrane curvature. Biochem J. 2008; 414(2):189-94. PMC: 2518064. DOI: 10.1042/BJ20081237. View

Farazi T, Waksman G, Gordon J . The biology and enzymology of protein N-myristoylation. J Biol Chem. 2001; 276(43):39501-4. DOI: 10.1074/jbc.R100042200. View

Yu Y, Wang L, Jiu Y, Zhan Y, Liu L, Xia Z . HID-1 is a novel player in the regulation of neuropeptide sorting. Biochem J. 2011; 434(3):383-90. DOI: 10.1042/BJ20110027. View

Sirkis D, Edwards R, Asensio C . Widespread dysregulation of peptide hormone release in mice lacking adaptor protein AP-3. PLoS Genet. 2013; 9(9):e1003812. PMC: 3784564. DOI: 10.1371/journal.pgen.1003812. View

Cao M, Mao Z, Kam C, Xiao N, Cao X, Shen C . PICK1 and ICA69 control insulin granule trafficking and their deficiencies lead to impaired glucose tolerance. PLoS Biol. 2013; 11(4):e1001541. PMC: 3635858. DOI: 10.1371/journal.pbio.1001541. View

Richter C, Woods I, Schier A . Neuropeptidergic control of sleep and wakefulness. Annu Rev Neurosci. 2014; 37:503-31. DOI: 10.1146/annurev-neuro-062111-150447. View

Gehart H, Goginashvili A, Beck R, Morvan J, Erbs E, Formentini I . The BAR domain protein Arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network. Dev Cell. 2012; 23(4):756-68. DOI: 10.1016/j.devcel.2012.07.019. View

10.

Tooze S . Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim Biophys Acta. 1998; 1404(1-2):231-44. PMC: 7126647. DOI: 10.1016/s0167-4889(98)00059-7. View

11.

Borgonovo B, Ouwendijk J, Solimena M . Biogenesis of secretory granules. Curr Opin Cell Biol. 2006; 18(4):365-70. DOI: 10.1016/j.ceb.2006.06.010. View

12.

Takeuchi T, Hosaka M . Sorting mechanism of peptide hormones and biogenesis mechanism of secretory granules by secretogranin III, a cholesterol-binding protein, in endocrine cells. Curr Diabetes Rev. 2008; 4(1):31-8. DOI: 10.2174/157339908783502406. View

13.

Klumperman J, Kuliawat R, Griffith J, Geuze H, Arvan P . Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J Cell Biol. 1998; 141(2):359-71. PMC: 2148452. DOI: 10.1083/jcb.141.2.359. View

14.

Zhang X, Jiang S, Mitok K, Li L, Attie A, Martin T . BAIAP3, a C2 domain-containing Munc13 protein, controls the fate of dense-core vesicles in neuroendocrine cells. J Cell Biol. 2017; 216(7):2151-2166. PMC: 5496627. DOI: 10.1083/jcb.201702099. View

15.

Asensio C, Sirkis D, Maas Jr J, Egami K, To T, Brodsky F . Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway. Dev Cell. 2013; 27(4):425-37. PMC: 3974617. DOI: 10.1016/j.devcel.2013.10.007. View

16.

Ahras M, Otto G, Tooze S . Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J Cell Biol. 2006; 173(2):241-51. PMC: 2063815. DOI: 10.1083/jcb.200506163. View

17.

Hummer B, Maslar D, Soltero-Gutierrez M, de Leeuw N, Asensio C . Differential sorting behavior for soluble and transmembrane cargoes at the -Golgi network in endocrine cells. Mol Biol Cell. 2019; 31(3):157-166. PMC: 7001476. DOI: 10.1091/mbc.E19-10-0561. View

18.

Dittie A, Hajibagheri N, Tooze S . The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP-ribosylation factor. J Cell Biol. 1996; 132(4):523-36. PMC: 2199873. DOI: 10.1083/jcb.132.4.523. View

19.

Takamitsu E, Otsuka M, Haebara T, Yano M, Matsuzaki K, Kobuchi H . Identification of Human N-Myristoylated Proteins from Human Complementary DNA Resources by Cell-Free and Cellular Metabolic Labeling Analyses. PLoS One. 2015; 10(8):e0136360. PMC: 4550359. DOI: 10.1371/journal.pone.0136360. View

20.

Topalidou I, Cattin-Ortola J, Hummer B, Asensio C, Ailion M . EIPR1 controls dense-core vesicle cargo retention and EARP complex localization in insulin-secreting cells. Mol Biol Cell. 2019; 31(1):59-79. PMC: 6938272. DOI: 10.1091/mbc.E18-07-0469. View