Artículo

Jozefkowicz, C.; Sigaut, L.; Scochera, F.; Soto, G.; Ayub, N.; Pietrasanta, L.I.; Amodeo, G.; González Flecha, F.L.; Alleva, K. "PIP Water Transport and Its pH Dependence Are Regulated by Tetramer Stoichiometry" (2016) Biophysical Journal. 110(6):1312-1321
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Many plasma membrane channels form oligomeric assemblies, and heterooligomerization has been described as a distinctive feature of some protein families. In the particular case of plant plasma membrane aquaporins (PIPs), PIP1 and PIP2 monomers interact to form heterotetramers. However, the biological properties of the different heterotetrameric configurations formed by PIP1 and PIP2 subunits have not been addressed yet. Upon coexpression of tandem PIP2-PIP1 dimers in Xenopus oocytes, we can address, for the first time to our knowledge, the functional properties of single heterotetrameric species having 2:2 stoichiometry. We have also coexpressed PIP2-PIP1 dimers with PIP1 and PIP2 monomers to experimentally investigate the localization and biological activity of each tetrameric assembly. Our results show that PIP2-PIP1 heterotetramers can assemble with 3:1, 1:3, or 2:2 stoichiometry, depending on PIP1 and PIP2 relative expression in the cell. All PIP2-PIP1 heterotetrameric species localize at the plasma membrane and present the same water transport capacity. Furthermore, the contribution of any heterotetrameric assembly to the total water transport through the plasma membrane doubles the contribution of PIP2 homotetramers. Our results also indicate that plasma membrane water transport can be modulated by the coexistence of different tetrameric species and by intracellular pH. Moreover, all the tetrameric species present similar cooperativity behavior for proton sensing. These findings throw light on the functional properties of PIP tetramers, showing that they have flexible stoichiometry dependent on the quantity of PIP1 and PIP2 molecules available. This represents, to our knowledge, a novel regulatory mechanism to adjust water transport across the plasma membrane. © 2016 Biophysical Society.

Registro:

Documento: Artículo
Título:PIP Water Transport and Its pH Dependence Are Regulated by Tetramer Stoichiometry
Autor:Jozefkowicz, C.; Sigaut, L.; Scochera, F.; Soto, G.; Ayub, N.; Pietrasanta, L.I.; Amodeo, G.; González Flecha, F.L.; Alleva, K.
Filiación:Instituto de Química y Fisicoquímica Biológica Alejandro C. Paladini (IQUIFIB), Universidad de Buenos Aires, Consejo National de Investigaciones Científicas y Técnicas (UBA-CONICET), Buenos Aires, Argentina
Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Física de Buenos Aires (IFIBA), CONICET, Ciudad Universitaria, Buenos Aires, Argentina
Departamento de Fisicomatemática, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Genética Ewald A. Favret, Centro de Investigación en Ciencias Veterinarias y Agronómicas, Instituto Nacional de Tecnología Agropecuaria (INTA), Castelar, Argentina
Centro de Microscopías Avanzadas, Facultad de Ciencias Exactas y Naturales, UBA-CONICET, Buenos Aires, Argentina
Departamento de Biodiversidad y Biología Experimental, Instituto de Biodiversidad y Biología Experimental y Aplicada, Facultad de Ciencias Exactas y Naturales, UBA-CONICET, Buenos Aires, Argentina
Palabras clave:aquaporin; plant protein; proton; water; animal; cell membrane; cell membrane permeability; chemistry; metabolism; osmosis; pH; protein multimerization; transport at the cellular level; Xenopus laevis; Animals; Aquaporins; Biological Transport; Cell Membrane; Cell Membrane Permeability; Hydrogen-Ion Concentration; Osmosis; Plant Proteins; Protein Multimerization; Protons; Water; Xenopus laevis
Año:2016
Volumen:110
Número:6
Página de inicio:1312
Página de fin:1321
DOI: http://dx.doi.org/10.1016/j.bpj.2016.01.026
Título revista:Biophysical Journal
Título revista abreviado:Biophys. J.
ISSN:00063495
CODEN:BIOJA
CAS:aquaporin, 215587-75-0; proton, 12408-02-5, 12586-59-3; water, 7732-18-5; Aquaporins; Plant Proteins; Protons; Water
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00063495_v110_n6_p1312_Jozefkowicz

Referencias:

  • Shi, L.B., Skach, W.R., Verkman, A.S., Functional independence of monomeric CHIP28 water channels revealed by expression of wild-type mutant heterodimers (1994) J. Biol. Chem., 269, pp. 10417-10422
  • Abascal, F., Irisarri, I., Zardoya, R., Diversity and evolution of membrane intrinsic proteins (2014) Biochim. Biophys. Acta, 1840, pp. 1468-1481
  • Kukulski, W., Schenk, A.D., Engel, A., The 5A structure of heterologously expressed plant aquaporin SoPIP2;1 (2005) J. Mol. Biol., 350, pp. 611-616
  • Fotiadis, D., Jenö, P., Engel, A., Structural characterization of two aquaporins isolated from native spinach leaf plasma membranes (2001) J. Biol. Chem., 276, pp. 1707-1714
  • Fetter, K., Van Wilder, V., Chaumont, F., Interactions between plasma membrane aquaporins modulate their water channel activity (2004) Plant Cell, 16, pp. 215-228
  • Yaneff, A., Sigaut, L., Amodeo, G., Heteromerization of PIP aquaporins affects their intrinsic permeability (2014) Proc. Natl. Acad. Sci. USA, 111, pp. 231-236
  • Otto, B., Uehlein, N., Kaldenhoff, R., Aquaporin tetramer composition modifies the function of tobacco aquaporins (2010) J. Biol. Chem., 285, pp. 31253-31260
  • Hachez, C., Besserer, A., Chaumont, F., Insights into plant plasma membrane aquaporin trafficking (2013) Trends Plant Sci., 18, pp. 344-352
  • Zelazny, E., Miecielica, U., Chaumont, F., An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane (2009) Plant J., 57, pp. 346-355
  • Sorieul, M., Santoni, V., Luu, D.T.T., Mechanisms and effects of retention of over-expressed aquaporin AtPIP2;1 in the endoplasmic reticulum (2011) Traffic, 12, pp. 473-482
  • Chevalier, A.S., Bienert, G.P., Chaumont, F., A new LxxxA motif in the transmembrane Helix3 of maize aquaporins belonging to the plasma membrane intrinsic protein PIP2 group is required for their trafficking to the plasma membrane (2014) Plant Physiol., 166, pp. 125-138
  • Zelazny, E., Borst, J.W., Chaumont, F., FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 12359-12364
  • Jozefkowicz, C., Rosi, P., Alleva, K., Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins (2013) PLoS One, 8, p. e57993
  • Hachez, C., Heinen, R.B., Chaumont, F., The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation (2008) Plant Mol. Biol., 68, pp. 337-353
  • Hachez, C., Moshelion, M., Chaumont, F., Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers (2006) Plant Mol. Biol., 62, pp. 305-323
  • Vandeleur, R.K., Mayo, G., Tyerman, S.D., The role of plasma membrane intrinsic protein aquaporins in water transport through roots: Diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine (2009) Plant Physiol., 149, pp. 445-460
  • Bellati, J., Alleva, K., Amodeo, G., Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression (2010) Plant Mol. Biol., 74, pp. 105-118
  • Dreyer, I., Antunes, S., Hedrich, R., Plant K+ channel α-subunits assemble indiscriminately (1997) Biophys. J., 72, pp. 2143-2150
  • Geiger, D., Becker, D., Hedrich, R., Heteromeric AtKC1·AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions (2009) J. Biol. Chem., 284, pp. 21288-21295
  • Jeanguenin, L., Alcon, C., Véry, A.A., AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity (2011) Plant J., 67, pp. 570-582
  • Duby, G., Hosy, E., Thibaud, J.B., AtKC1, a conditionally targeted Shaker-type subunit, regulates the activity of plant K+ channels (2008) Plant J., 53, pp. 115-123
  • Reintanz, B., Szyroki, A., Hedrich, R., AtKC1, a silent Arabidopsis potassium channel α-subunit modulates root hair K+ influx (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 4079-4084
  • Zhang, R.B., Verkman, A.S., Water and urea permeability properties of Xenopus oocytes: Expression of mRNA from toad urinary bladder (1991) Am. J. Physiol., 260, pp. C26-C34
  • Agre, P., Mathai, J.C., Preston, G.M., Functional analyses of aquaporin water channel proteins (1999) Methods Enzymol., 294, pp. 550-572
  • Brooks, J.M., Wessel, G.M., Selective transport and packaging of the major yolk protein in the sea urchin (2003) Dev. Biol., 261, pp. 353-370
  • Kemmer, G., Keller, S., Nonlinear least-squares data fitting in Excel spreadsheets (2010) Nat. Protoc., 5, pp. 267-281
  • Cattoni, D.I., Chara, O., González Flecha, F.L., Cooperativity in binding processes: New insights from phenomenological modeling (2015) PLoS One, 10, p. e0146043
  • Naso, A., Montisci, R., Picco, C., Stoichiometry studies reveal functional properties of KDC1 in plant shaker potassium channels (2006) Biophys. J., 91, pp. 3673-3683
  • Veerappan, A., Cymer, F., Schneider, D., The tetrameric α-helical membrane protein GlpF unfolds via a dimeric folding intermediate (2011) Biochemistry, 50, pp. 10223-10230
  • Naranjo, D., Assembly of Shaker K-Channels from a random mixture of subunits carrying different mutations (1997) From Ion Channels to Cell-to-Cell Conversations, pp. 35-46. , Plenum Press New York
  • Ding, S., Ingleby, L., Horn, R., Investigating the putative glycine hinge in Shaker potassium channel (2005) J. Gen. Physiol., 126, pp. 213-226
  • Németh-Cahalan, K.L., Clemens, D.M., Hall, J.E., Regulation of AQP0 water permeability is enhanced by cooperativity (2013) J. Gen. Physiol., 141, pp. 287-295
  • Tournaire-Roux, C., Sutka, M., Maurel, C., Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins (2003) Nature, 425, pp. 393-397
  • Kerschensteiner, D., Soto, F., Stocker, M., Fluorescence measurements reveal stoichiometry of K+ channels formed by modulatory and delayed rectifier α-subunits (2005) Proc. Natl. Acad. Sci. USA, 102, pp. 6160-6165
  • Bartoi, T., Augustinowski, K., Ulbrich, M.H., Acid-sensing ion channel (ASIC) 1a/2a heteromers have a flexible 2:1/1:2 stoichiometry (2014) Proc. Natl. Acad. Sci. USA, 111, pp. 8281-8286
  • Gründer, S., Pusch, M., Biophysical properties of acid-sensing ion channels (ASICs) (2015) Neuropharmacology, 94, pp. 9-18
  • Wang, W., Xia, J., Kass, R.S., MinK-KvLQT1 fusion proteins, evidence for multiple stoichiometries of the assembled IsK channel (1998) J. Biol. Chem., 273, pp. 34069-34074
  • Barrera, N.P., Henderson, R.M., Edwardson, J.M., The stoichiometry of P2X2/6 receptor heteromers depends on relative subunit expression levels (2007) Biophys. J., 93, pp. 505-512
  • Stewart, A.P., Gómez-Posada, J.C., Edwardson, J.M., The Kv7.2/Kv7.3 heterotetramer assembles with a random subunit arrangement (2012) J. Biol. Chem., 287, pp. 11870-11877

Citas:

---------- APA ----------
Jozefkowicz, C., Sigaut, L., Scochera, F., Soto, G., Ayub, N., Pietrasanta, L.I., Amodeo, G.,..., Alleva, K. (2016) . PIP Water Transport and Its pH Dependence Are Regulated by Tetramer Stoichiometry. Biophysical Journal, 110(6), 1312-1321.
http://dx.doi.org/10.1016/j.bpj.2016.01.026
---------- CHICAGO ----------
Jozefkowicz, C., Sigaut, L., Scochera, F., Soto, G., Ayub, N., Pietrasanta, L.I., et al. "PIP Water Transport and Its pH Dependence Are Regulated by Tetramer Stoichiometry" . Biophysical Journal 110, no. 6 (2016) : 1312-1321.
http://dx.doi.org/10.1016/j.bpj.2016.01.026
---------- MLA ----------
Jozefkowicz, C., Sigaut, L., Scochera, F., Soto, G., Ayub, N., Pietrasanta, L.I., et al. "PIP Water Transport and Its pH Dependence Are Regulated by Tetramer Stoichiometry" . Biophysical Journal, vol. 110, no. 6, 2016, pp. 1312-1321.
http://dx.doi.org/10.1016/j.bpj.2016.01.026
---------- VANCOUVER ----------
Jozefkowicz, C., Sigaut, L., Scochera, F., Soto, G., Ayub, N., Pietrasanta, L.I., et al. PIP Water Transport and Its pH Dependence Are Regulated by Tetramer Stoichiometry. Biophys. J. 2016;110(6):1312-1321.
http://dx.doi.org/10.1016/j.bpj.2016.01.026