Artículo

Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The epsins are a family of adaptors involved in recruiting other endocytic proteins, binding of ubiquitylated cargo and induction of membrane curvature. These molecules bear a characteristic epsin N-terminal homology (ENTH) domain and multiple peptide motifs that mediate protein-protein interactions. We have previously demonstrated that the ENTH domain of epsin is involved in Cdc42 signaling regulation. Here, we present evidence that yeast epsin 2 (Ent2) plays a signaling role during cell division. We observed that overexpression of the ENTH domain of Ent2 (ENTH2), but not Ent1, promoted the formation of chains of cells and aberrant septa. This dominant-negative effect resulted from ENTH2-mediated interference with septin assembly pathways. We mapped the ENTH2 determinants responsible for induction of the phenotype and found them to be important for efficient binding to the septin regulatory protein, Bem3. Supporting a physiological role for epsin 2 in cell division, the protein localized to sites of polarized growth and cytokinesis and rescued a defect in cell division induced by Bem3 misregulation. Collectively, our findings provide a potential molecular mechanism linking endocytosis (via epsin 2) with signaling pathways regulating cell division.

Registro:

Documento: Artículo
Título:The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway
Autor:Mukherjee, D.; Coon, B.G.; Edwards III, D.F.; Hanna, C.B.; Longhi, S.A.; McCaffery, J.M.; Wendland, B.; Retegui, L.A.; Bi, E.; Aguilar, R.C.
Filiación:Department of Biological Sciences, Purdue Cancer Center, Purdue University, West Lafayette, IN 47907, United States
Departamento de Química Biológica, Universidad de Buenos Aires, Buenos Aires, Argentina
Department of Biology, The Johns Hopkins University, Baltimore, MD 21218, United States
Department of Cell and Developmental Biology, School of Medicine, University of Pennsylvania, Pennsylvania, PA 19104, United States
Instituto de Investigaciones en Ingenieria Genetica y Biologia Molecular (INGEBI-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Cell division; Endocytosis; Epsin; Septin; article; error; priority journal; Adaptor Proteins, Vesicular Transport; Amino Acid Sequence; Animals; Cell Division; Cell Polarity; Chitin Synthase; Cytokinesis; Endocytosis; Gene Expression Regulation, Fungal; Genotype; GTPase-Activating Proteins; Mice; Mice, Inbred BALB C; Molecular Sequence Data; Phenotype; Protein Structure, Tertiary; Saccharomyces cerevisiae; Saccharomyces cerevisiae Proteins; Signal Transduction; Vesicular Transport Proteins
Año:2009
Volumen:122
Número:14
Página de inicio:2453
Página de fin:2463
DOI: http://dx.doi.org/10.1242/jcs.041137
Título revista:Journal of Cell Science
Título revista abreviado:J. Cell Sci.
ISSN:00219533
CODEN:JNCSA
CAS:Adaptor Proteins, Vesicular Transport; BEM3 protein, S cerevisiae; Chitin Synthase, 2.4.1.16; ENT1 protein, S cerevisiae; ENT2 protein, S cerevisiae; GTPase-Activating Proteins; Saccharomyces cerevisiae Proteins; Vesicular Transport Proteins
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00219533_v122_n14_p2453_Mukherjee.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219533_v122_n14_p2453_Mukherjee

Referencias:

  • Adams, A.E., Pringle, J.R., Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae (1984) J. Cell Biol, 98, pp. 934-945
  • Aguilar, R.C., Watson, H.A., Wendland, B., The yeast Epsin Ent1 is recruited to membranes through multiple independent interactions (2003) J. Biol. Chem, 278, pp. 10737-10743
  • Aguilar, R.C., Longhi, S.A., Shaw, J.D., Yeh, L.Y., Kim, S., Schon, A., Freire, E., Watson, H.A., Epsin N-terminal homology domains perform an essential function regulating Cdc42 through binding Cdc42 GTPase-activating proteins (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 4116-4121
  • Baggett, J. J., Shaw, J. D., Sciambi, C. J., Watson, H. A. and Wendland, B. (2003). Fluorescent labeling of yeast. Curr. Protoc. Cell Biol. Chapter 4, Unit 4 13; Bi, E., Maddox, P., Lew, D.J., Salmon, E.D., McMillan, J.N., Yeh, E., Pringle, J.R., Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis (1998) J. Cell Biol, 142, pp. 1301-1312
  • Boucrot, E., Kirchhausen, T., Endosomal recycling controls plasma membrane area during mitosis (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 7939-7944
  • Bouquin, N., Barral, Y., Courbeyrette, R., Blondel, M., Snyder, M., Mann, C., Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae (2000) J. Cell Sci, 113, pp. 1435-1445
  • Cabib, E., Roh, D.H., Schmidt, M., Crotti, L.B., Varma, A., The yeast cell wall and septum as paradigms of cell growth and morphogenesis (2001) J. Biol. Chem, 276, pp. 19679-19682
  • Caviston, J.P., Longtine, M., Pringle, J.R., Bi, E., The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast (2003) Mol. Biol. Cell, 14, pp. 4051-4066
  • Cid, V.J., Adamikova, L., Cenamor, R., Molina, M., Sanchez, M., Nombela, C., Cell integrity and morphogenesis in a budding yeast septin mutant (1998) Microbiology, 144, pp. 3463-3474
  • Collins, C.S., Kalish, J.E., Morrell, J.C., McCaffery, J.M., Gould, S.J., The peroxisome biogenesis factors pex4p, pex22p, pex1p, and pex6p act in the terminal steps of peroxisomal matrix protein import (2000) Mol. Cell. Biol, 20, pp. 7516-7526
  • Di Guglielmo, G.M., Le Roy, C., Goodfellow, A.F., Wrana, J.L., Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover (2003) Nat. Cell Biol, 5, pp. 410-421
  • Ford, M.G., Mills, I.G., Peter, B.J., Vallis, Y., Praefcke, G.J., Evans, P.R., McMahon, H.T., Curvature of clathrin-coated pits driven by epsin (2002) Nature, 419, pp. 361-366
  • Gladfelter, A.S., Bose, I., Zyla, T.R., Bardes, E.S., Lew, D.J., Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p (2002) J. Cell Biol, 156, pp. 315-326
  • Gonzalez-Gaitan, M., Signal dispersal and transduction through the endocytic pathway (2003) Nat. Rev. Mol. Cell. Biol, 4, pp. 213-224
  • Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S., Takenawa, T., Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis (2001) Science, 291, pp. 1047-1051
  • Iwase, M., Toh-e, A., Nis1 encoded by YNL078W: A new neck protein of Saccharomyces cerevisiae (2001) Genes Genet. Syst, 76, pp. 335-343
  • Iwase, M., Luo, J., Nagaraj, S., Longtine, M., Kim, H.B., Haarer, B.K., Caruso, C., Bi, E., Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site (2006) Mol. Biol. Cell, 17, pp. 1110-1125
  • Jenna, S., Hussain, N.K., Danek, E.I., Triki, I., Wasiak, S., McPherson, P.S., Lamarche-Vane, N., The activity of the GTPase-activating protein CdGAP is regulated by the endocytic protein intersectin (2002) J. Biol. Chem, 277, pp. 6366-6373
  • Kadota, J., Yamamoto, T., Yoshiuchi, S., Bi, E., Tanaka, K., Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae (2004) Mol. Biol. Cell, 15, pp. 5329-5345
  • Kaksonen, M., Toret, C.P., Drubin, D.G., A modular design for the clathrin-and actin-mediated endocytosis machinery (2003) Cell, 123, pp. 305-320
  • Knaus, M., Pelli-Gulli, M.P., van Drogen, F., Springer, S., Jaquenoud, M., Peter, M., Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence (2007) EMBO J, 26, pp. 4501-4513
  • Longtine, M.S., Bi, E., Regulation of septin organization and function in yeast (2003) Trends Cell Biol, 13, pp. 403-409
  • Longtine, M.S., Theesfeld, C.L., McMillan, J.N., Weaver, E., Pringle, J.R., Lew, D.J., Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae (2000) Mol. Cell. Biol, 20, pp. 4049-4061
  • Luo, J.Y., Vallen, E.A., Dravis, C., Tcheperegine, S.E., Drees, B., Bi, E.F., Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae (2004) J. Cell Biol, 165, pp. 843-855
  • Maldonado-Baez, L., Dores, M.R., Perkins, E.M., Drivas, T.G., Hicke, L., Wendland, B., Interaction between Epsin/Yap180 adaptors and the scaffolds Ede1/Pan1 is required for endocytosis (2008) Mol. Biol. Cell, 19, pp. 2936-2948
  • Marco, E., Wedlich-Soldner, R., Li, R., Altschuler, S.J., Wu, L.F., Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity (2007) Cell, 129, pp. 411-422
  • Nichols, J.T., Miyamoto, A., Weinmaster, G., Notch signaling-constantly on the move (2007) Traffic, 8, pp. 959-969
  • Niswonger, M.L., O'Halloran, T.J., A novel role for clathrin in cytokinesis (1997) Proc. Natl. Acad. Sci. USA, 94, pp. 8575-8578
  • Okuzaki, D., Tanaka, S., Kanazawa, H., Nojima, H., Gin4 of S-cerevisiae is a bud neck protein that interacts with the Cdc28 complex (1997) Genes Cells, 2, pp. 753-770
  • Ozbudak, E.M., Becskei, A., van Oudenaarden, A., A system of counteracting feedback loops regulates Cdc42p activity during spontaneous cell polarization (2005) Dev. Cell, 9, pp. 565-571
  • Richman, T.J., Johnson, D.I., Saccharomyces cerevisiae cdc42p GTPase is involved in preventing the recurrence of bud emergence during the cell cycle (2000) Mol. Cell. Biol, 20, pp. 8548-8559
  • Richman, T.J., Sawyer, M.M., Johnson, D.I., The Cdc42p GTPase is involved in a G2/M morphogenetic checkpoint regulating the apical-isotropic switch and nuclear division in yeast (1999) J. Biol. Chem, 274, pp. 16861-16870
  • Richman, T.J., Sawyer, M.M., Johnson, D.I., Saccharomyces cerevisiae Cdc42p localizes to cellular membranes and clusters at sites of polarized growth (2002) Eukaryot. Cell, 1, pp. 458-468
  • Roh, D.H., Bowers, B., Schmidt, M., Cabib, E., The septation apparatus, an autonomous system in budding yeast (2002) Mol. Biol. Cell, 13, pp. 2747-2759
  • Rönicke, V., Graulich, W., Mumberg, D., Müller, R., Funk, M., Use of conditional promoters for expression of heterologous proteins in Saccharomyces cerevisiae (1997) Methods Enzymol, 283, pp. 313-322
  • Rosenthal, J.A., Chen, H., Slepnev, V.I., Pellegrini, L., Salcini, A.E., Di Fiore, P.P., De Camilli, P., The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module (1999) J. Biol. Chem, 274, pp. 33959-33965
  • Schmidt, M., Varma, A., Drgon, T., Bowers, B., Cabib, E., Septins, under Cla4p regulation, and the chitin ring are required for neck integrity in budding yeast (2003) Mol. Biol. Cell, 14, pp. 2128-2141
  • Sikorski, R.S., Hieter, P., A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae (1989) Genetics, 122, pp. 19-27
  • Smith, G.R., Givan, S.A., Cullen, P., Sprague Jr, G.F., GTPase-activating proteins for Cdc42 (2002) Eukaryot. Cell, 1, pp. 469-480
  • Takahashi, S., Pryciak, P.M., Identification of novel membrane-binding domains in multiple yeast Cdc42 effectors (2007) Mol. Biol. Cell, 18, pp. 4945-4956
  • Tang, H.Y., Cai, M., The EH-domain-containing protein Pan1 is required for normal organization of the actin cytoskeleton in Saccharomyces cerevisiae (1996) Mol. Cell. Biol, 16, pp. 4897-4914
  • Tolliday, N., Pitcher, M., Li, R., Direct evidence for a critical role of myosin II in budding yeast cytokinesis and the evolvability of new cytokinetic mechanisms in the absence of myosin II (2003) Mol. Biol. Cell, 14, pp. 798-809
  • Toret, C.P., Lee, L., Sekiya-Kawasaki, M., Drubin, D.G., Multiple pathways regulate endocytic coat disassembly in Saccharomyces cerevisiae for optimal downstream trafficking (2008) Traffic, 9, pp. 848-859
  • Urbanowski, J.L., Piper, R.C., Ubiquitin sorts proteins into the intralumenal degradative compartment of the late-endosome/vacuole (2001) Traffic, 2, pp. 622-630
  • Versele, M., Thorner, J., Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4 (2004) J. Cell Biol, 164, pp. 701-715
  • Versele, M., Thorner, J., Some assembly required: Yeast septins provide the instruction manual (2005) Trends Cell Biol, 15, pp. 414-424
  • von Zastrow, M., Sorkin, A., Signaling on the endocytic pathway (2007) Curr. Opin. Cell Biol, 19, pp. 436-445
  • Watson, H.A., Cope, M.J., Groen, A.C., Drubin, D.G., Wendland, B., In vivo role for actin-regulating kinases in endocytosis and yeast epsin phosphorylation (2001) Mol. Biol. Cell, 12, pp. 3668-3679
  • Wendland, B., Epsins: Adaptors in endocytosis? (2002) Nat. Rev. Mol. Cell. Biol, 3, pp. 971-977
  • Ziman, M., O'Brien, J.M., Ouellette, L.A., Church, W.R., Johnson, D.I., Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity (1991) Mol. Cell. Biol, 11, pp. 3537-3544

Citas:

---------- APA ----------
Mukherjee, D., Coon, B.G., Edwards III, D.F., Hanna, C.B., Longhi, S.A., McCaffery, J.M., Wendland, B.,..., Aguilar, R.C. (2009) . The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway. Journal of Cell Science, 122(14), 2453-2463.
http://dx.doi.org/10.1242/jcs.041137
---------- CHICAGO ----------
Mukherjee, D., Coon, B.G., Edwards III, D.F., Hanna, C.B., Longhi, S.A., McCaffery, J.M., et al. "The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway" . Journal of Cell Science 122, no. 14 (2009) : 2453-2463.
http://dx.doi.org/10.1242/jcs.041137
---------- MLA ----------
Mukherjee, D., Coon, B.G., Edwards III, D.F., Hanna, C.B., Longhi, S.A., McCaffery, J.M., et al. "The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway" . Journal of Cell Science, vol. 122, no. 14, 2009, pp. 2453-2463.
http://dx.doi.org/10.1242/jcs.041137
---------- VANCOUVER ----------
Mukherjee, D., Coon, B.G., Edwards III, D.F., Hanna, C.B., Longhi, S.A., McCaffery, J.M., et al. The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway. J. Cell Sci. 2009;122(14):2453-2463.
http://dx.doi.org/10.1242/jcs.041137