Skip to main content
PMC home page
Protein & Cell logoLink to Protein & Cell
. 2011 Feb 20;2(1):74–85. doi: 10.1007/s13238-011-1008-3

HID-1 is a peripheral membrane protein primarily associated with the medial- and trans- Golgi apparatus

Lifen Wang 1,2, Yi Zhan 3, Eli Song 1, Yong Yu 1,2, Yaming Jiu 3, Wen Du 1, Jingze Lu 1, Pingsheng Liu 1, Pingyong Xu 1,✉, Tao Xu 1,3,✉
PMCID: PMC4875289  PMID: 21337012

Abstract

Caenorhabditis elegans hid-1 gene was first identified in a screen for mutants with a high-temperature-induced dauer formation (Hid) phenotype. Despite the fact that the hid-1 gene encodes a novel protein (HID-1) which is highly conserved from Caenorhabditis elegans to mammals, the domain structure, subcellular localization, and exact function of HID-1 remain unknown. Previous studies and various bioinformatic softwares predicted that HID-1 contained many transmembrane domains but no known functional domain. In this study, we revealed that mammalian HID-1 localized to the medial- and trans- Golgi apparatus as well as the cytosol, and the localization was sensitive to brefeldin A treatment. Next, we demonstrated that HID-1 was a peripheral membrane protein and dynamically shuttled between the Golgi apparatus and the cytosol. Finally, we verified that a conserved N-terminal myristoylation site was required for HID-1 binding to the Golgi apparatus. We propose that HID-1 is probably involved in the intracellular trafficking within the Golgi region.

Keywords: HID-1, Golgi, peripheral membrane protein, fluorescent recovery after photobleaching, N-myristoylation

Footnotes

These authors contributed equally to this work.

Contributor Information

Pingyong Xu, Email: pyxu@moon.ibp.ac.cn.

Tao Xu, Email: xutao@ibp.ac.cn.

References

  1. Ailion M., Thomas J.H. Isolation and characterization of high-temperature-induced Dauer formation mutants in Caenorhabditis elegans. Genetics. 2003;165:127–144. doi: 10.1093/genetics/165.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anders N., Jürgens G. Large ARF guanine nucleotide exchange factors in membrane trafficking. Cell Mol Life Sci. 2008;65:3433–3445. doi: 10.1007/s00018-008-8227-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Apfeld J., Kenyon C. Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell. 1998;95:199–210. doi: 10.1016/S0092-8674(00)81751-1. [DOI] [PubMed] [Google Scholar]
  4. Birnby D.A., Link E.M., Vowels J.J., Tian H., Colacurcio P.L., Thomas J.H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in caenorhabditis elegans. Genetics. 2000;155:85–104. doi: 10.1093/genetics/155.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown E.J., Albers M.W., Shin T.B., Ichikawa K., Keith C.T., Lane W.S., Schreiber S.L. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature. 1994;369:756–758. doi: 10.1038/369756a0. [DOI] [PubMed] [Google Scholar]
  6. Campellone K.G., Webb N.J., Znameroski E.A., Welch M.D. WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell. 2008;134:148–161. doi: 10.1016/j.cell.2008.05.032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cassada R.C., Russell R.L. The dauerlarva, a postembryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol. 1975;46:326–342. doi: 10.1016/0012-1606(75)90109-8. [DOI] [PubMed] [Google Scholar]
  8. Choi J., Chen J., Schreiber S.L., Clardy J. Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science. 1996;273:239–242. doi: 10.1126/science.273.5272.239. [DOI] [PubMed] [Google Scholar]
  9. Cohn D.H., Ehtesham N., Krakow D., Unger S., Shanske A., Reinker K., Powell B.R., Rimoin D.L. Mental retardation and abnormal skeletal development (Dyggve-Melchior-Clausen dysplasia) due to mutations in a novel, evolutionarily conserved gene. Am J Hum Genet. 2003;72:419–428. doi: 10.1086/346176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Colombo M.I., Gelberman S.C., Whiteheart S.W., Stahl P.D. N-ethylmaleimide-sensitive factor-dependent alpha-SNAP release, an early event in the docking/fusion process, is not regulated by Rab GTPases. J Biol Chem. 1998;273:1334–1338. doi: 10.1074/jbc.273.3.1334. [DOI] [PubMed] [Google Scholar]
  11. de Jonge, H.R., Hogema, B., and Tilly, B.C. (2000). Protein N-myristoylation: critical role in apoptosis and salt tolerance. Sci STKE 2000, pe1. [DOI] [PubMed]
  12. Dimitrov A., Paupe V., Gueudry C., Sibarita J.B., Raposo G., Vielemeyer O., Gilbert T., Csaba Z., Attie-Bitach T., Cormier-Daire V., et al. The gene responsible for Dyggve-Melchior-Clausen syndrome encodes a novel peripheral membrane protein dynamically associated with the Golgi apparatus. Hum Mol Genet. 2009;18:440–453. doi: 10.1093/hmg/ddn371. [DOI] [PubMed] [Google Scholar]
  13. Dube D.H., de Graffenried C.L., Kohler J.J. Regulating cell surface glycosylation with a small-molecule switch. Methods Enzymol. 2006;415:213–229. doi: 10.1016/S0076-6879(06)15014-4. [DOI] [PubMed] [Google Scholar]
  14. El Ghouzzi V., Dagoneau N., Kinning E., Thauvin-Robinet C., Chemaitilly W., Prost-Squarcioni C., Al-Gazali L.I., Verloes A., Le Merrer M., Munnich A., et al. Mutations in a novel gene Dymeclin (FLJ20071) are responsible for Dyggve-Melchior-Clausen syndrome. Hum Mol Genet. 2003;12:357–364. doi: 10.1093/hmg/ddg029. [DOI] [PubMed] [Google Scholar]
  15. Fielenbach N., Antebi A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev. 2008;22:2149–2165. doi: 10.1101/gad.1701508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gleeson P.A., Teasdale R.D., Burke J. Targeting of proteins to the Golgi apparatus. Glycoconj J. 1994;11:381–394. doi: 10.1007/BF00731273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Humphrey J.S., Peters P.J., Yuan L.C., Bonifacino J.S. Localization of TGN38 to the trans-Golgi network: involvement of a cytoplasmic tyrosine-containing sequence. J Cell Biol. 1993;120:1123–1135. doi: 10.1083/jcb.120.5.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Inoue T., Thomas J.H. Suppressors of transforming growth factor-beta pathway mutants in the Caenorhabditis elegans dauer formation pathway. Genetics. 2000;156:1035–1046. doi: 10.1093/genetics/156.3.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Inoue T., Thomas J.H. Targets of TGF-beta signaling in Caenorhabditis elegans dauer formation. Dev Biol. 2000;217:192–204. doi: 10.1006/dbio.1999.9545. [DOI] [PubMed] [Google Scholar]
  20. Killisch I., Steinlein P., Römisch K., Hollinshead R., Beug H., Griffiths G. Characterization of early and late endocytic compartments of the transferrin cycle. Transferrin receptor antibody blocks erythroid differentiation by trapping the receptor in the early endosome. J Cell Sci. 1992;103:211–232. doi: 10.1242/jcs.103.1.211. [DOI] [PubMed] [Google Scholar]
  21. Kjer-Nielsen L., van Vliet C., Erlich R., Toh B.H., Gleeson P.A. The Golgi-targeting sequence of the peripheral membrane protein p230. J Cell Sci. 1999;112:1645–1654. doi: 10.1242/jcs.112.11.1645. [DOI] [PubMed] [Google Scholar]
  22. Koh S., Yamamoto A., Inoue A., Inoue Y., Akagawa K., Kawamura Y., Kawamoto K., Tashiro Y. Immunoelectron microscopic localization of the HPC-1 antigen in rat cerebellum. J Neurocytol. 1993;22:995–1005. doi: 10.1007/BF01218356. [DOI] [PubMed] [Google Scholar]
  23. Lewis J.L., Dong M., Earles C.A., Chapman E.R. The transmembrane domain of syntaxin 1A is critical for cytoplasmic domain protein-protein interactions. J Biol Chem. 2001;276:15458–15465. doi: 10.1074/jbc.M011687200. [DOI] [PubMed] [Google Scholar]
  24. Liang Z., Li G. Mouse prenylated Rab acceptor is a novel Golgi membrane protein. Biochem Biophys Res Commun. 2000;275:509–516. doi: 10.1006/bbrc.2000.3316. [DOI] [PubMed] [Google Scholar]
  25. Lippincott-Schwartz J., Yuan L., Tipper C., Amherdt M., Orci L., Klausner R.D. Brefeldin A’s effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell. 1991;67:601–616. doi: 10.1016/0092-8674(91)90534-6. [DOI] [PubMed] [Google Scholar]
  26. Lodge J.K., Jackson-Machelski E., Devadas B., Zupec M.E., Getman D.P., Kishore N., Freeman S.K., McWherter C.A., Sikorski J.A., Gordon J.I. N-myristoylation of Arf proteins in Candida albicans: an in vivo assay for evaluating antifungal inhibitors of myristoyl-CoA: protein N-myristoyltransferase. Microbiology. 1997;143:357–366. doi: 10.1099/00221287-143-2-357. [DOI] [PubMed] [Google Scholar]
  27. Lorenz H., Hailey D.W., Wunder C., Lippincott-Schwartz J. The fluorescence protease protection (FPP) assay to determine protein localization and membrane topology. Nat Protoc. 2006;1:276–279. doi: 10.1038/nprot.2006.42. [DOI] [PubMed] [Google Scholar]
  28. Luo X., Feng L., Jiang X., Xiao F., Wang Z., Feng G.S., Chen Y. Characterization of the topology and functional domains of RKTG. Biochem J. 2008;414:399–406. doi: 10.1042/BJ20080948. [DOI] [PubMed] [Google Scholar]
  29. Luzio J.P., Brake B., Banting G., Howell K.E., Braghetta P., Stanley K.K. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38) Biochem J. 1990;270:97–102. doi: 10.1042/bj2700097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mironov A., Pavelka M. The Golgi Apparatus: State of the Art 110 Years After Camillo Golgi’s Discovery. New York: Springer-Verlag Gmbh, Wien; 2008. [Google Scholar]
  31. Nakamura N., Rabouille C., Watson R., Nilsson T., Hui N., Slusarewicz P., Kreis T.E., Warren G. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol. 1995;131:1715–1726. doi: 10.1083/jcb.131.6.1715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ponnambalam S., Girotti M., Yaspo M.L., Owen C.E., Perry A.C., Suganuma T., Nilsson T., Fried M., Banting G., Warren G. Primate homologues of rat TGN38: primary structure, expression and functional implications. J Cell Sci. 1996;109:675–685. doi: 10.1242/jcs.109.3.675. [DOI] [PubMed] [Google Scholar]
  33. Riddle D. C. elegans II. New York: CSHL Press; 1997. [Google Scholar]
  34. Robinson M.S., Sahlender D.A., Foster S.D. Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev Cell. 2010;18:324–331. doi: 10.1016/j.devcel.2009.12.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Standaert R.F., Galat A., Verdine G.L., Schreiber S.L. Molecular cloning and overexpression of the human FK506-binding protein FKBP. Nature. 1990;346:671–674. doi: 10.1038/346671a0. [DOI] [PubMed] [Google Scholar]
  36. Suh B.C., Inoue T., Meyer T., Hille B. Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science. 2006;314:1454–1457. doi: 10.1126/science.1131163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Trus M., Wiser O., Goodnough M.C., Atlas D. The transmembrane domain of syntaxin 1A negatively regulates voltage-sensitive Ca(2 +) channels. Neuroscience. 2001;104:599–607. doi: 10.1016/S0306-4522(01)00083-5. [DOI] [PubMed] [Google Scholar]
  38. Waters M.G., Clary D.O., Rothman J.E. A novel 115-kD peripheral membrane protein is required for intercisternal transport in the Golgi stack. J Cell Biol. 1992;118:1015–1026. doi: 10.1083/jcb.118.5.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wright M.H., Heal W.P., Mann D.J., Tate E.W. Protein myristoylation in health and disease. J Chem Biol. 2009;3:19–35. doi: 10.1007/s12154-009-0032-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yamaguchi N., Fukuda M.N. Golgi retention mechanism of beta-1,4-galactosyltransferase. Membrane-spanning domaindependent homodimerization and association with alpha- and beta-tubulins. J Biol Chem. 1995;270:12170–12176. doi: 10.1074/jbc.270.20.12170. [DOI] [PubMed] [Google Scholar]
  41. Yu, Y., Wang, L.F., Jiu, Y.M., Zhan, Y., Liu, L., Xia, Z.P., Song, E.L., Xu, P.Y., Xu, T. (2011). HID-1 is a novel player in the regulation of neuropeptide sorting. Biochem J. Doi: 10.1042/BJ20110027. [DOI] [PubMed]
  42. Zerial M., Melancon P., Schneider C., Garoff H. The transmembrane segment of the human transferrin receptor functions as a signal peptide. EMBO J. 1986;5:1543–1550. doi: 10.1002/j.1460-2075.1986.tb04395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Protein & Cell are provided here courtesy of Oxford University Press

RESOURCES