DOI QR코드

DOI QR Code

The Unique Mechanism of SNX9 BAR Domain for Inducing Membrane Tubulation

  • Park, Joohyun (Department of Physiology and Biomedical Sciences, Seoul National University College of Medicine) ;
  • Zhao, Haiyan (Department of Physiology and Biomedical Sciences, Seoul National University College of Medicine) ;
  • Chang, Sunghoe (Department of Physiology and Biomedical Sciences, Seoul National University College of Medicine)
  • Received : 2014.08.12
  • Accepted : 2014.09.02
  • Published : 2014.10.31

Abstract

Sorting nexin 9 (SNX9) is a member of the sorting nexin family of proteins and plays a critical role in clathrinmediated endocytosis. It has a Bin-Amphiphysin-Rvs (BAR) domain which can form a crescent-shaped homodimer structure that induces deformation of the plasma membrane. While other BAR-domain containing proteins such as amphiphysin and endophilin have an amphiphatic helix in front of the BAR domain which plays a critical role in membrane penetration, SNX9 does not. Thus, whether and how SNX9 BAR domain could induce the deformation of the plasma membrane is not clear. The present study identified the internal putative amphiphatic stretch in the $1^{st}$ ${\alpha}$-helix of the SNX9 BAR domain and proved that together with the N-terminal helix ($H_0$) region, this internal putative amphiphatic stretch is critical for inducing membrane tubulation. Therefore, our study shows that SNX9 uses a unique mechanism to induce the tubulation of the plasma membrane which mediates proper membrane deformation during clathrinmediated endocytosis.

Keywords

References

  1. Childress, C., Lin, Q., and Yang, W. (2006). Dimerization is required for SH3PX1 tyrosine phosphorylation in response to epidermal growth factor signalling and interaction with ACK2. Biochem. J. 394, 693-698. https://doi.org/10.1042/BJ20050576
  2. Dawson, J.C., Legg, J.A., and Machesky, L.M. (2006). Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16, 493-498. https://doi.org/10.1016/j.tcb.2006.08.004
  3. Fernandes, F., Loura, L.M., Chichon, F.J., Carrascosa, J.L., Fedorov, A., and Prieto, M. (2008). Role of helix 0 of the N-BAR domain in membrane curvature generation. Biophys. J. 94, 3065-3073. https://doi.org/10.1529/biophysj.107.113118
  4. Futterer, K., and Machesky, L.M. (2007). "Wunder" F-BAR domains: going from pits to vesicles. Cell 129, 655-657. https://doi.org/10.1016/j.cell.2007.05.006
  5. Gallop, J.L., and McMahon, H.T. (2005). BAR domains and membrane curvature: bringing your curves to the BAR. Biochem. Soc. Symp. 2005, 223-231.
  6. Gallop, J.L., Jao, C.C., Kent, H.M., Butler, P.J., Evans, P.R., Langen, R., and McMahon, H.T. (2006). Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25, 2898-2910. https://doi.org/10.1038/sj.emboj.7601174
  7. Gallop, J.L., Walrant, A., Cantley, L.C., and Kirschner, M.W. (2013). Phosphoinositides and membrane curvature switch the mode of actin polymerization via selective recruitment of toca-1 and Snx9. Proc. Natl. Acad. Sci. USA 110, 7193-7198. https://doi.org/10.1073/pnas.1305286110
  8. Habermann, B. (2004). The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5, 250-255. https://doi.org/10.1038/sj.embor.7400105
  9. Howard, L., Nelson, K.K., Maciewicz, R.A., and Blobel, C.P. (1999). Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J. Biol. Chem. 274, 31693-31699. https://doi.org/10.1074/jbc.274.44.31693
  10. Itoh, T., and De Camilli, P. (2006). BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912. https://doi.org/10.1016/j.bbalip.2006.06.015
  11. Lin, Q., Lo, C.G., Cerione, R.A., and Yang, W. (2002). The Cdc42 target ACK2 interacts with sorting nexin 9 (SH3PX1) to regulate epidermal growth factor receptor degradation. J. Biol. Chem. 277, 10134-10138. https://doi.org/10.1074/jbc.M110329200
  12. Low, C., Weininger, U., Lee, H., Schweimer, K., Neundorf, I., Beck-Sickinger, A.G., Pastor, R.W., and Balbach, J. (2008). Structure and dynamics of helix-0 of the N-BAR domain in lipid micelles and bilayers. Biophys. J. 95, 4315-4323. https://doi.org/10.1529/biophysj.108.134155
  13. Lundmark, R., and Carlsson, S.R. (2003). Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J. Biol. Chem. 278, 46772-46781. https://doi.org/10.1074/jbc.M307334200
  14. Lundmark, R., and Carlsson, S.R. (2009). SNX9 - a prelude to vesicle release. J. Cell Sci. 122, 5-11. https://doi.org/10.1242/jcs.037135
  15. Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., and Mochizuki, N. (2006). Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25, 2889-2897. https://doi.org/10.1038/sj.emboj.7601176
  16. McMahon, H.T., and Gallop, J.L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596. https://doi.org/10.1038/nature04396
  17. Peter, B.J., Kent, H.M., Mills, I.G., Vallis, Y., Butler, P.J., Evans, P.R., and McMahon, H.T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499. https://doi.org/10.1126/science.1092586
  18. Pylypenko, O., Lundmark, R., Rasmuson, E., Carlsson, S.R., and Rak, A. (2007). The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J. 26, 4788-4800. https://doi.org/10.1038/sj.emboj.7601889
  19. Ren, G., Vajjhala, P., Lee, J.S., Winsor, B., and Munn, A.L. (2006). The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70, 37-120. https://doi.org/10.1128/MMBR.70.1.37-120.2006
  20. Shin, N., Lee, S., Ahn, N., Kim, S.A., Ahn, S.G., YongPark, Z., and Chang, S. (2007). Sorting nexin 9 interacts with dynamin 1 and N-WASP and coordinates synaptic vesicle endocytosis. J. Biol. Chem. 282, 28939-28950. https://doi.org/10.1074/jbc.M700283200
  21. Shin, N., Ahn, N., Chang-Ileto, B., Park, J., Takei, K., Ahn, S.G., Kim, S.A., Di Paolo, G., and Chang, S. (2008). SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J. Cell Sci. 121, 1252-1263. https://doi.org/10.1242/jcs.016709
  22. Soulet, F., Yarar, D., Leonard, M., and Schmid, S.L. (2005). SNX9 regulates dynamin assembly and is required for efficient clathrinmediated endocytosis. Mol. Biol. Cell 16, 2058-2067. https://doi.org/10.1091/mbc.E04-11-1016
  23. Wang, Q., Kaan, H.Y., Hooda, R.N., Goh, S.L., and Sondermann, H. (2008). Structure and plasticity of endophilin and sorting nexin 9. Structure 16, 1574-1587. https://doi.org/10.1016/j.str.2008.07.016
  24. Wang, Q., Navarro, M.V., Peng, G., Molinelli, E., Goh, S.L., Judson, B.L., Rajashankar, K.R., and Sondermann, H. (2009). Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc. Natl. Acad. Sci. USA 106, 12700-12705. https://doi.org/10.1073/pnas.0902974106
  25. Yarar, D., Waterman-Storer, C.M., and Schmid, S.L. (2007). SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell 13, 43-56. https://doi.org/10.1016/j.devcel.2007.04.014
  26. Zimmerberg, J., and Kozlov, M.M. (2006). How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19. https://doi.org/10.1038/nrm1784

Cited by

  1. Reduced expression of SETD2 and SNX9 proteins in chemically induced mammary tumorigenesis in Wistar rats: a prognostic histological and proteomic study vol.254, pp.3, 2017, https://doi.org/10.1007/s00709-016-1035-2