Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Involvement of the Rho/Rac family member RhoG in caveolar endocytosis

Oncogene volume 25, pages 2961–2973 (2006)Cite this article

Abstract

We show here that the GTPase RhoG is involved in caveolar trafficking. Wild-type RhoG moves sequentially to the plasma membrane, intracellular vesicles, and the Golgi apparatus along markers of this endocytic pathway. Such translocation is associated with changes in RhoG GDP/GTP levels and is highly dependent on lipid raft integrity and on the function of the GTPase dynamin2. In addition, the constitutively active RhoGQ61L mutant is preferentially located in endocytic vesicles that can be decorated with markers of the caveola-derived endocytic pathway. RhoGQ61L, but not the analogous Rac1 mutant protein, affects caveola internalization and the subsequent delivery of endocytic vesicles to the Golgi apparatus. The expression of RhoG/Rac1 chimeric proteins and RhoGQ61L effector mutants in cells induces alterations in the internalization of caveolae and severe changes in vesicle structure, respectively. However, the knockdown of endogenous rhoG transcripts using small interfering RNAs does not affect significantly the trafficking of caveola-derived vesicles, suggesting that RhoG function is dispensable for this endocytic process or, alternatively, that its function is compensated by other molecules. Taken together, these observations assign a novel function to RhoG and suggest that caveolar trafficking, as previously shown for other endocytic routes, is modulated by GTPases of the Ras superfamily.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 7
Figure 6
Figure 8

Similar content being viewed by others

References

  • Conner SD, Schmid SL . (2003). Nature 422: 37–44.

  • Cox D, Chang P, Zhang Q, Reddy PG, Bokoch GM, Greenberg S . (1997). J Exp Med 186: 1487–1494.

  • Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL . (2003). Nat Cell Biol 5: 410–421.

  • Ellis S, Mellor H . (2000). Trends Cell Biol 10: 85–88.

  • Felberbaum-Corti M, Van Der Goot FG, Gruenberg J . (2003). Nat Cell Biol 5: 382–384.

  • Filippi MD, Harris CE, Meller J, Gu Y, Zheng Y, Williams DA . (2004). Nat Immunol 5: 744–751.

  • Gauthier-Rouviere C, Vignal E, Meriane M, Roux P, Montcourier P, Fort P . (1998). Mol Biol Cell 9: 1379–1394.

  • Gonzalez-Gaitan M . (2003). Nat Rev Mol Cell Biol 4: 213–224.

  • Greenberg S . (1999). J Leukoc Biol 66: 712–717.

  • Gruenberg J . (2001). Nat Rev Mol Cell Biol 2: 721–730.

  • Henley JR, Krueger EW, Oswald BJ, McNiven MA . (1998). J Cell Biol 141: 85–99.

  • Hoppe AD, Swanson JA . (2004). Mol Biol Cell 15: 3509–3519.

  • Joneson T, McDonough M, Bar-Sagi D, Van Aelst L . (1996). Science 274: 1374–1376.

  • Katoh H, Negishi M . (2003). Nature 424: 461–464.

  • Katoh H, Yasui H, Yamaguchi Y, Aoki J, Fujita H, Mori K et al. (2000). Mol Cell Biol 20: 7378–7387.

  • Li G, Stahl PD . (1993). J Biol Chem 268: 24475–24480.

  • Massol P, Montcourrier P, Guillemot JC, Chavrier P . (1998). EMBO J 17: 6219–6229.

  • May V, Schiller MR, Eipper BA, Mains RE . (2002). J Neurosci 22: 6980–6990.

  • Nichols B . (2003). J Cell Sci 116: 4707–4714.

  • Nichols BJ . (2002). Nat Cell Biol 4: 374–378.

  • Nichols BJ, Kenworthy AK, Polishchuk RS, Lodge R, Roberts TH, Hirschberg K et al. (2001). J Cell Biol 153: 529–541.

  • Nichols BJ, Lippincott-Schwartz J . (2001). Trends Cell Biol 11: 406–412.

  • Orlandi PA, Fishman PH . (1998). J Cell Biol 141: 905–915.

  • Parton RG, Richards AA . (2003). Traffic 4: 724–738.

  • Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, Krausz E et al. (2005). Nature 436: 78–86.

  • Pelkmans L, Helenius A . (2002). Traffic 3: 311–320.

  • Pelkmans L, Zerial M . (2005). Nature 436: 128–133.

  • Prieto-Sanchez RM, Bustelo XR . (2003). J Biol Chem 278: 37916–37925.

  • Sabharanjak S, Sharma P, Parton RG, Mayor S . (2002). Dev Cell 2: 411–423.

  • Simons K, Toomre D . (2000). Nat Rev Mol Cell Biol 1: 31–39.

  • Torgersen ML, Skretting G, van Deurs B, Sandvig K . (2001). J Cell Sci 114: 3737–3747.

  • Vignal E, Blangy A, Martin M, Gauthier-Rouviere C, Fort P . (2001). Mol Cell Biol 21: 8022–8034.

  • Wennerberg K, Ellerbroek SM, Liu RY, Karnoub AE, Burridge K, Der CJ . (2002). J Biol Chem 277: 47810–47817.

  • Wu WJ, Erickson JW, Lin R, Cerione RA . (2000). Nature 405: 800–804.

  • Zerial M, McBride H . (2001). Nat Rev Mol Cell Biol 2: 107–117.

Download references

Acknowledgements

We thank M Blázquez and Dr P Fort for excellent technical assistance and the supply of anti-RhoG antibodies, respectively. We also thank Dr H Lee for the cloning of human rab cDNAs and the generation of rab point mutants. This work was supported by grants from both the US National Cancer Institute (5-R01-CA73735-08) and the Spanish Ministry of Education and Science (SAF2003-00028). RMP-S and IMB are students of the Molecular and Cellular Cancer Biology graduate program of the CIC and the University of Salamanca and are supported by FPU fellowships (AP2000-3829 and FP2000-6489; Spanish Ministry of Education and Science).

Author information

Author notes

  1. R M Prieto-Sánchez and I M Berenjeno: These two authors contributed equally to this work.

Authors and Affiliations

  1. Centro de Investigación del Cáncer, Instituto de Biología Molecular y Celular del Cáncer (IBMCC), and Red Temática Cooperativa de Centros de Cáncer, CSIC-University of Salamanca, Campus Unamuno, Salamanca, Spain

    R M Prieto-Sánchez, I M Berenjeno & X R Bustelo

Authors
  1. R M Prieto-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I M Berenjeno
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. X R Bustelo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to X R Bustelo.

Additional information

Supplementary Information accompanies the paper on Oncogene website (http://www.nature.com/onc)

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prieto-Sánchez, R., Berenjeno, I. & Bustelo, X. Involvement of the Rho/Rac family member RhoG in caveolar endocytosis. Oncogene 25, 2961–2973 (2006). https://doi.org/10.1038/sj.onc.1209333

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1209333

Keywords

This article is cited by

Search

Advanced search

Quick links