Skip to main content
Log in

Role of ARF4L in Recycling Between Endosomes and the Plasma Membrane

  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

The human ADP-ribosylation factor-like protein, ARF4L is a member of the ARF family, which are small GTP-binding proteins that play significant roles in vesicle transport and protein secretion. However, little is known about the physiological roles of ARF4L. In this study, to understand the biological functions of ARF4L, we carried out immunocytochemical analysis of ARF4L molecules with mutations in the functional domains. ARF4L was shown to be distributed to the plasma membrane following binding to GTP (Q80L), and into endosomes following binding to GDP (T35N). Moreover, the inactive-form of ARF4L (T35N) causes localization of transferrin receptors to the endosomal compartment, while the active form (Q80L) causes transport to the plasma membrane. These findings indicate that ARF4L drive the transport of cargo protein and subsequent fusion of recycling vesicles with the plasma membrane for maintenance of the cell surface.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

REFERENCES

  • Aoe, T., Cukierman, E., Lee, A., Cassel, D., Peters, P. J., and Hsu, V. W. (1997). The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1. EMBO J. 16 (24):7305-7316.

    Google Scholar 

  • D'Souza-Schorey, C., Li, G., Colombo, M. I., and Stahl, P. D. (1995). A regulatory role for ARF6 in receptor-mediated endocytosis. Science 267 (5201):1175-1178.

    Google Scholar 

  • D'Souza-Schorey, C., van Donselaar, E., Hsu, V. W., Yang, C., Stahl, P. D., and Peters, P. J. (1998). ARF6 targets recycling vesicles to the plasma membrane: Insights from an ultrastructural investigation. J. Cell Biol. 140 (3):603-616.

    Google Scholar 

  • Eugster, A., Frigerio, G., Dale, M., and Duden, R. (2000). COPI domains required for coatmer integrity, and novel interactions with ARF and ARF-GAP. EMBO J. 19 (15):3905-3917.

    Google Scholar 

  • Gaynor, E. C., and Emr S. D. (1997). COPI-independent anterograde transport: Cargo-selective ER to Golgi protein transport in yeast COPI mutants. J. Cell Biol. 136 (4):789-802.

    Google Scholar 

  • Jackson, M. R., Nilsson T., and Peterson P. A. (1990): Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J. 9 (10):3153-3162.

    Google Scholar 

  • Katayama, T., Imaizumi, K., Tsuda, M., Mori, Y., Takagi, T., and Tohyama, M. (1998): Expression of an ADP-ribosylation factor like gene, ARF4L, is induced after transient forebrain ischemia in the gerbil. Mol. Brain Res. 56(1-2):66-75.

    Google Scholar 

  • Kawamoto, K., Yoshida, Y., Tamaki, H., Torii, S., Shinotsuka, C., Yamashina, S., and Nakayama, K. (2002). GBF, a guanine nucleotide exchange factor for ADP-ribosylation factors, is localized to the cis-Golgi and involved in membrane association of the COPI coat. Traffic 3(7):483-495.

    Google Scholar 

  • Kirino, T., and Sano, K. (1984): Fine structural nature of delayed neuronal death following ischemia in the gerbil hippocampus. Acta Neuropathol. (Berl.) 62(3):209-218.

    Google Scholar 

  • Loijens, J. C., and Anderson R. A. (1996): Type I phosphatidyl inositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family. J. Biol. Chem. 271(51):32937-32943.

    Google Scholar 

  • Massenburg, D., Han, J. S., Liyanage, M., Patton, W. A., Rhee, S. G., Moss, J., and Vaughan, M. (1995). Activation of rat brain phospholipase D by ADP-ribosylation factors 1,5, and 6: Separation of ADP-ribosylation factor-dependent and oleate-dependent enzymes. Proc. Natl. Acad. Sci. 91(24):11718-11722.

    Google Scholar 

  • Nechushtan, A., Smith, C. L., Hsu, Y. T., and Youle, R. J. (1999). Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J. 18(9):2330-2341.

    Google Scholar 

  • Nilsson, T., Jackson, M., and Peterson, P. A. (1989). Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58(4):707-718.

    Google Scholar 

  • Ooi, C. E., Dell'Angelica, E. C., and Bonifacino, J. S. (1998). ADP-ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol. 142(2):391-402.

    Google Scholar 

  • Paris, S., Beraud-Dufour, S., Robineau, S., Bigay, J., Antonny, B., Chabre, M., and Chardin, P. (1997). Role of protein-phospholipid interactions in the activation of ARF1 by the guanine nucleotide exchange factor ARNO. J. Biol. Chem. 272(35):22221-22226.

    Google Scholar 

  • Presley, J. F., Ward, T. H., Pfeifer, A. C., Siggia, E. D., Phair, R. D., and Lippincott-Schwartz, J. (2002). Dissection of COPI and ARF1 dynamics in vivo and role in Golgi membrane transport. Nature 417(6885):187-193.

    Google Scholar 

  • Radhakrishna, H., and Donaldson, J. G. (1997). ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139(1):49-61.

    Google Scholar 

  • Radhakrishna, H., Klausner, R. D., and Donaldson, J. G. (1996). Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J. Cell Biol. 134(4):935-947.

    Google Scholar 

  • Rothman, J. E (1996). The protein machinery of vesicle budding and fusion. Protein Sci. 5(2):185-194.

    Google Scholar 

  • Rothman, J. E., and Orci, L. (1992). Molecular dissection of the secretory pathway. Nature 355(6359):409-415.

    Google Scholar 

  • Schurmann, A., Breiner, M., Becker, W., Huppertz, C., Kainulainen, H., Kentrup, H., and Joost, H. G. (1994). Cloning of two novel ADP-ribosylation factor-like proteins and characterization of their differential expression in 3T3-3L1 cells. J. Biol. Chem. 269(22):15683-15688.

    Google Scholar 

  • Smith, S. A., Holik, P. R., Stevens, J., Melis, R., White, R., and Albertsen, H. (1995). Isolation and mapping of a gene encoding a novel human ADP-ribosylation factor on chromosome 17q12-q21. Genomics 28(1):113-115.

    Google Scholar 

  • Sohn, K., Orci L., Ravazzola, M., Amherdt, M., Bremser, M., Lottspeich, F., Fiedler, K., Helms, J. B., and Wieland, F. T. (1996). A major transmembrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding. J. Cell Biol. 135(5):1239-1248.

    Google Scholar 

  • Thilmann, R., Xie, Y., Kleihues P., and Kiessling, M. (1986). Persistent inhibition of protein synthesis precedes delayed neuronal death in postischemic gerbil hippocampus. Acta Neuropathol. (Berl.) 71(1-2):88-93.

    Google Scholar 

  • Tisdale, E. J., Plutner, H., Matteson, J., and Balch, W. E. (1997). p53/58 binds COPI and is required for selective transport through the early secretory pathway. J. Cell Biol. 137(3):581-593.

    Google Scholar 

  • Valencia, A., Chardin, P., Wittinghofer, A., and Sander, C. (1991). The ras protein family: Evolutionary tree and role of conserved amino acids. Biochemistry 30(19):4637-4648.

    Google Scholar 

  • Vincent, M. J., Martin, A. S., and Compans, R. W. (1998). Function of the KKXX motif in endoplasmic reticulum retrieval of a transmembrane protein depends on the length and structure of the cytoplasmic domain. J. Biol. Chem. 273(2):950-956.

    Google Scholar 

  • Vitale, N., Chasserot-Golaz, S., Bailly, Y., Morinaga, N., Frohman, M. A., and Bader, M. F. (2002). Calcium-regulated exocytosis of dense-core vesicles requires the activation of ADP-ribosylation factor (ARF)6 by ARF nucleotide binding site opener at the plasma membrane. J. Cell Biol. 159(1):79-89.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Taiichi Katayama.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katayama, T., Imaizumi, K., Yoneda, T. et al. Role of ARF4L in Recycling Between Endosomes and the Plasma Membrane. Cell Mol Neurobiol 24, 137–147 (2004). https://doi.org/10.1023/B:CEMN.0000012719.12015.ec

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:CEMN.0000012719.12015.ec

Navigation