Aquaporins: Structure, Systematics, and Regulatory Features A

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Aquaporins: Structure, Systematics, and Regulatory Features A. Yu. Shapiguzov Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow, 127276 Russia; fax: 7 (095) 977-9372; e-mail: [email protected] Received May 13, 2003

Abstract—The review describes current views on the molecular structure, systematics, and functional regulation of aquaporins. These recently discovered channel proteins play a principal role in water transport across cell membranes in the majority of living organisms.

Key words: aquaporins - cell membranes - water relations

INTRODUCTION family—is sometimes used for aquaporins in the litera- ture. Multicellular organisms have developed specialized Presently, the number of discovered aquaporins tissues with low hindrance to water flows. Nonetheless, exceeds two hundred, and the plant aquaporins consti- the transfer of water molecules across the cell mem- tute a considerable part of this family [10]. For exam- brane is the main step in water transport [1]. ple, Arabidopsis thaliana genome contains 35 aqua- The ability of cells to control outward or inward porin genes [11Ð13], and Zea mays contains more than movement of water and solutes is a matter of principal 30 such genes [14]. significance. Cell membranes represent selective com- Water transport is extremely difficult for quantita- plex filters that regulate the transport of ions, organic tive assessment. Unlike the transmembrane ion trans- substances, and water. The current knowledge of mem- port associated with membrane potential changes, brane structure and functions is rapidly expanding [2]. water transport is normally evaluated from the osmoti- A number of transmembrane carrier proteins have been cally induced changes of the cell volume, and such discovered and characterized. However, despite this measurements are often complicated [15]. Further- progress, molecular basis of the transmembrane water more, a background component of water transport is transport remained poorly understood until recently. rather high owing to universal abundance of water and The water permeability of biological membranes was its rapid diffusion through the lipid bilayer. commonly attributed to diffusion of water across the The oocytes of a frog Xenopus played an important lipid bilayer. However, some physiological processes role in studying water carriers [16]. The membranes of are associated with translocation of large amounts of these cells feature a very low intrinsic permeability to water or with rapid changes in membrane permeability water. When mRNA is injected into the oocyte, it is nor- to water. Such phenomena cannot be explained by mally expressed as a functional protein. After the injec- water diffusion across the lipids, which implicates the tion of aqp1 gene mRNA, the water permeability of the existence of water-carrying proteins. oocyte membrane increased manyfold; the cell swelled The first of such carriers was revealed in the mam- rapidly in a hypoosmotic buffer and lysed. By compar- malian erythrocytes whose cell membrane is highly ing the kinetics of cell volume changes in untreated and permeable to water [3]. The initial observation that aqp1-expressing oocytes, it was possible to assess the activity of the protein examined. HgCl2 and organicÐmercurial substances inhibit water transport implied the involvement of protein in this pro- Another important approach to studying aquaporins cess [4]. A specific polypeptide was isolated later and is the evaluation of their activity in proteoliposomes termed CHIP28 (channel-like integral protein of 28 kD) [17]. [5, 6]. Several homological proteins were revealed in The investigation of aquaporins led to several other mammalian tissues. One of such proteins, called important conclusions. (1) Many aquaporins signifi- MIP (major intrinsic protein of lens), had been known cantly reduce the activation energy for the transmem- for a long time although its function was unclear [7]. brane water transfer. The rate of water movement Later studies demonstrated the presence and, in some across the channel approaches to the diffusion rate in cases, abundance of homological proteins in many bulk water [17, 18]. (2) Aquaporins provide for bidirec- organisms [8], and their transport activity was proven. tional passage of water, and the transport direction is A term “aquaporins” (Aqp) was adopted, and CHIP28 determined by physical conditions of the medium [19, was renamed as Aqp1 [9]. An alternative term—MIP 20]. (3) Water transport is passive: it does not require

128 SHAPIGUZOV energy supply, and water moves downhill the gradient proteins is an inherent homology between the halves of of water potential [20]. (4) Aquaporin channels are their molecules. The repeated sequences are oriented in highly selective. The water transport across the cell the same direction. It is likely that the aquaporin gene membrane normally occurs without a concomitant originated from the duplication of a half-sized gene [10]. transfer of any ion species, including protons [21, 22]. Six transmembrane α-helical protein domains form (5) Many aquaporins are sensitive to mercury-contain- a barrel-like configuration in the membrane plane. The ing inhibitors. The mercury atoms bind to conserved amino- and carboxy-terminal domains face the cyto- cysteine residues and are thought to block water pas- plasm and account for a specific regulation of aqua- sage through the channel by steric hindrance [23, 24]. porin activity. One of the cytoplasmic loops and one of There is evidence that mercury induces conformational the periplasmic loops comprise two short α-helical changes in aquaporins [25]. domains on the opposite sides of the “barrel.” These Some aquaporins turned out to be specific not so domains participate in the formation of the water chan- much to water as to glycerol and several other sub- nel. The tops of these domains are located in close stances [26], for example, gases [20, 27]. Some aqua- proximity to each other inside the molecule (Fig. 1). porins, including aquaporins of plant origin, are perme- Each of these tops contains an NPA (Asn-Pro-Ala) able to formamide [28] and urea [29]. The substrate motif, which is conserved for all aquaporins with rare specificity of these proteins in plants is still unknown. exceptions [14, 46]. This type of structure was called There is evidence that aquaporins are permeable to eth- the “hourglass model” [19, 47]. anol and methanol; however, the study of this phenome- When incorporated into the membrane, aquaporins non is highly complicated owing to unhampered diffu- produce homotetramers [48, 49]. Apparently, this sion of alcohols through the lipid bilayer [30]. The aqua- assemblage is required for correct folding and stability porins of Chara corallina are permeable to H2O2 [31]. of the protein, as well as for protein sorting and post- The expression of Aqp1 increases the CO2 perme- translational modifications including glycosylation. ability of the Xenopus oocyte membrane [32], although Each of the four subunits within the complex produces the significance of this property for the mammalian an independent water channel, whereas the pore for the physiology in vivo was questioned in some works [33, aforementioned cGMP-dependent ion transport is ori- 34]. Mercury-containing organic substances inhibit ented along to the tetramer axis (Fig. 2) [39]. The sta- CO2 transport across the plasma membrane in cyano- bility of the quaternary structure varies for different bacteria Synechococcus [35] and in higher plants [36]. phylogenetic clusters of aquaporins: the tetramers of This provides evidence for CO2-transporting activity of aquaporins with glycerol specificity are less stable [50]. aquaporins and suggests their involvement in photosyn- The most complete data about the structure of water thesis; nevertheless, this topic remains poorly understood. channel were obtained after crystallization of Aqp1 It is possible that some aquaporins are permeable to other [51] and its X-ray crystallographic analysis [52, 53]. gases, including O2, NH3, and NO [27]. The attempts to Most likely the structural features discovered for Aqp1 study this issue encounter the problem of high permeabil- are also valid for other water-conducting proteins of the ity of lipids to the substances mentioned [37]. family. A small part of Aqp1 molecules expressed in Xenopus The shape of the aquaporin channel is reminiscent oocytes becomes permeable to Na+ after the intracellular of a dumb-bell (Fig. 3). The channel consists of an injection of cyclic GMP [38]. Apparently, the binding of external and cytoplasmic funnels and a long selective cGMP results in the opening of the cationic channel in pore with connecting them. The funnel surface consists the aquaporin molecule. The formation of aqueous and mainly of polar amino-acid residues. Here the hydro- cationic pores seems to occur in different regions of the philic substrates undergo primary selection and their protein molecule (see below) [39]. The ionic perme- hydration shell is removed at the expense of hydrogen ability was also demonstrated for Aqp0 [40Ð42], Aqp6 bond formation with the protein atoms. The funnels of [43, 44], and plant aquaporin Nod26 [45]. Further glycerol-specific aquaporins are less hydrophilic [54]. investigation of this phenomenon could be important In the region where the outer funnel contacts the for understanding a fine regulation of the transmem- pore, the channel opening is very narrow. This region brane potentials. serves as a steric filter impermeable to large neutral molecules and ions incapable of losing their hydrated AQUAPORIN STRUCTURE shell. The diameter of the constriction allows the pene- tration of single water molecules only. In glycerol-spe- The discovery of aquaporin functional features cific aquaporins this region is modified: it has a larger raised a number of intriguing questions. It was unclear diameter and is less hydrophilic [55]. how the high rate and selectivity of water transport are A thermodynamically favorable passage of water achieved. The answers to these questions require the along the pore is provided by the formation of new understanding of aquaporin structure. hydrogen bonds between the water molecule and aqua- Aquaporins are small highly hydrophobic trans- porin atoms. The binding to the protein is due to oxy- membrane proteins. The characteristic feature of these gen atoms of the peptide groups from several sequential

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C N

Fig. 1. Diagram of the tertiary structure of aquaporin molecule. The transmembrane α-helices are specified with numbers. Two short α-helical domains are depicted in the connecting loops. The channel region is indicated with arrow. amino-acid residues. These oxygen atoms are arranged DIVERSITY OF AQUAPORINS in two chains along the internal surface of the pore, whereas the rest part of the pore is hydrophobic. The The aquaporin family remained highly conserved chains begin at the external and cytoplasmic surfaces, during the evolution. Apparently, the reason behind this respectively, and project towards the pore center. These phenomenon resides in strict structural requirements, the violation of which leads to functional disturbance. chains are formed by amino acids of the loops that con- α Homological aquaporins were discovered in phyloge- tain two short -helical domains. The distance between netically distant organisms, which led to the conclusion the hydrophilic regions is of great thermodynamical significance: more densely spaced hydrophilic regions would have increased the number of intermediary transport stages, whereas a scarce disposition would have increased the activation energy for the transitions between separate stages. In both cases, the rate of water transport would have decreased. The center of protein molecule contains two NPA motifs with closely positioned asparagine residues, and these residues form the pore middle region. The amide groups of these residues also form hydrophilic areas over the channel surface. Upon the transfer of water molecule from one asparagine residue to an other, this molecule is released from a continuous hydrogen bond system formed by a file of water molecules moving along the water pore [56]. Thus, an inflexion of the pore and the geometrical pattern of hydrophilic regions pro- mote the disruption of the hydrogen bond network. The disruption of the continuous transmembrane system of hydrogen bonds plays a crucial role in providing the channel selectivity, because a chain of water molecules can make a path for proton movement. The proton Fig. 2. Diagram of the quaternary structure of the Aqp1 tet- migration would have resulted in the collapse of the ramer. The water channels within the monomers are indicated with transmembrane electrochemical proton gradient and black circles, and the supposed region of the ionic channel the uncoupling of oxidative phosphorylation [57]. is marked with cross.

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Asn Asn

Fig. 3. Schematic sectional view of the Aqp1 channel. The internal surface of the channel is marked with a dashed line. Oxygen atoms of carbonyl groups line the hydrophilic regions along the water pore. In the central part of the pore, the asparagine residues (Asn) of two NPA motifs are positioned in close proximity to each other. A serum atom (S) serves as a target for mercurial inhibitors. that aquaporins constitute an ancient protein family. To comparatively low [26]. Some of these aquaporins are date the sequences have been determined for more than capable of transporting antimonite, Sb(OH)3, as well as two hundred aquaporin genes from bacteria and arsenic and antimony salts [63], the compounds appar- eukaryotic organisms. A recent discovery of aquaporins ently mimicking glycerol. The aquaglyceroporins in Archaea proved the ubiquitous occurrence of aqua- include the GlpF protein from Escherichia coli, Aqp3, porins in the biotic world [58]. Aqp7, Aqp9, and, possibly, Aqp10 identified recently in At present, there is no unanimous opinion about mammals. This group also includes several proteins phylogenetic relations between the representatives of from a nematode Caenorhabditis elegans and a the aquaporin family. Consequently, several homolog from yeast [55, 64]. No plant aquaglyceropor- approaches were proposed to the systematics of these ins have been discovered. proteins. Some classifications are based on the sub- (2) Aquaporins of multicellular animals are abun- strate specificity and the localization of aquaporins in dant in mammalian tissues and are characterized by cells and tissues [59, 60]. Another approach is a preferential specificity for water. The representatives of mathematical analysis of the aquaporin gene sequences this subfamily have been under study in three-quarter without taking into account the functional properties of of all scientific publications dealing with aquaporins. aquaporins [61]. These analyses led to the identification This group includes mammalian Aqp0 (MIP), Aqp1, of several independent phylogenetic clusters, but the Aqp2, Aqp4, Aqp5, Aqp6, and their homologs from supposed number of such clusters varied in different Arthropoda. publications. (1) Aquaglyceroporin cluster. The majority of these (3) Homologs of mammalian Aqp3 comprise a dif- channel proteins are permeable to water as well as to ferent phylogenetic cluster. The substrate specificity of glycerol and urea [62]; moreover, water permeability is these proteins is unclear. Possibly, they facilitate the

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AQUAPORINS: STRUCTURE, SYSTEMATICS, AND REGULATORY FEATURES 131 transport of water and urea, but the physiological role tion of nodulins is not restricted to being a symbiosome of this transport remains unresolved [65]. constituent [59]. (4) A separate cluster is assigned to prokaryotic (9) A recently discovered AqpM of archaebacteria aquaporins specific to water transport, e.g., AqpZ from occupies a special place in the evolution of aquaporins. E. coli [66]. It bears a certain resemblance to prokaryotic aquapor- Plant aquaporins are classified as follows: ins, as well as to plant nodulins [58]. AqpM is perme- (5) Aquaporins of the plasma membrane, PIP able to water and is moderately permeable to glycerol (plasma membrane intrinsic proteins). Actually, these and, possibly, to CO2. Taking into account sharp dis- proteins are located not only in the cytoplasmic mem- tinctions in the membrane structure and properties for brane. This cluster is comparatively young and includes archaebacteria and other groups of organisms, it should aquaporins with the least degree of variability. Appar- be noted that the studies of AqpM could shed new light ently, the divergence of PIP proteins is related to the on the biology of aquaporins. evolutionary progress of higher plants and to the appearing specialized tissues. The PIP proteins are REGULATION OF AQUAPORIN FUNCTIONING characterized by a high variability of terminal domains and by an enlarged N-terminus. These properties are Aquaporins do not only facilitate the transmem- related to the specific regulation of their functioning. brane transport of various substances but also coordi- The cluster is conventionally divided in two groups, nate the transport rates. The regulated operation of PIP1 and PIP2, with the length of N-terminal domain as aquaporins ensures the control over permeability of a distinctive feature. This domain is larger in PIP1 certain membranes to water and other substrates and group [67]. allows the redistribution of water fluxes at the cell and tissue levels. This regulation occurs at the transcrip- (6) The tonoplast aquaporins, TIP (tonoplast intrin- tional or posttranslational stages. sic proteins) play an important role in maintaining cell turgor and water potential of the cytoplasm. The water The aquaporin genes are either expressed constitu- permeability of the tonoplast is much higher than that tively [75] or induced in response to certain stimuli: of the plasma membrane; therefore, the tonoplast rap- hormones [76Ð78], blue light [77], salt and osmotic idly equilibrates osmotic and hydraulic disturbances stresses, and drought [79]. induced in the cytoplasm by external treatments [68]. Plant hormones controlling aquaporin expression The phylogenetic divergence of the TIP cluster include GA, ABA, and, possibly, brassinosteroids [80]. occurred at early stages of eukaryote evolution and was The γ-tip gene of A. thaliana is induced by GA [76], concurrent with the formation of various intracellular and the pip1b gene is induced by blue light, GA, and compartments. These aquaporins can serve as markers ABA. Furthermore, the levels of these two hormones for different types of vacuoles [69Ð71]. The majority of are strictly balanced to ensure regulated gene expres- this cluster representatives belong to one of three large sion [77]. The expression of tobRB7 gene in tobacco groups: αTIP, γTIP, and δTIP. roots can be activated by nematodes that infest plants The clusters PIP and TIP, and water-specific aqua- and provoke the formation of feeding zones [30, 81]. porin cluster of animals are evolutionary related [61]. Transcriptional regulation of aquaporin expression, (7) Small basic membrane proteins of plants, SIP probably related to ABA accumulation, is observed in (small basic intrinsic proteins) [72]. The properties of some plants experiencing water deficit [82, 83]. The these aquaporins have been poorly investigated to date. level of aquaporin expression is considerably lowered (8) The Nod proteins of plant origin (nodulins, in CAM plants. This property seems to have an adap- Nlm family) are glycerol permeable similarly to aqua- tive significance [84]. glyceroporins [73]. Both clusters are characterized by The expression of SunTIP7 aquaporin in stomatal the maximal rate of evolution, which is presumably due guard cells of sunflower leaves exhibits a circadian to the release of structural restrictions required for periodicity. Gene activation occurs by noon, and the specificity to water [62]. Mathematical analysis protein mediates water efflux from the guard cells dur- revealed the relationship of nodulins to bacterial water- ing stomata closing. The expression of SunTIP7 was specific aquaporins. According to current views, these also observed upon drought [85]. proteins were transferred from prokaryotes to plants Protein phosphorylation, glycosylation, ligand through horizontal gene transfer. This transfer could be binding, and proteolytic cleavage are posttranslational necessitated by the lack of intrinsic glycerol carriers in events that affect functional activity, folding, sorting, plants [74]. The Nod26 protein participates in the and degradation of aquaporins [86Ð89]. The vaso- metabolite transfer between the plant cell cytoplasm pressin-induced export of vesicles containing Aqp-2 and symbiotic bacteria in soybean root nodules; it rep- aquaporin towards the surface of epithelial cells in resents the main protein component of the perib- mammalian kidneys is a bright example of posttransla- acteroid membranes [28]. Since Arabidopsis and some tional regulation. The vasopressin reception leads to the other plants containing such proteins are devoid of activation of protein kinase A and phosphorylation of nitrogen-fixing symbionts, it is obvious that the func- C-terminal region in Aqp2. Thereafter, the cytoplasmic

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132 SHAPIGUZOV aquaporin domain binds to the proteins of vesicle coat, could be unspecific and some aquaporins are resistant and Aqp2 is exported together with the vesicles to the to such treatments [115, 116]. plasma membrane [90]. This mechanism ensures a very Inactivation of individual aquaporin genes often rapid manyfold increase in water permeability of the results in mobilization of various compensatory mech- membrane [91]. A regulatory mechanism of such kind anisms. The transformation of A. thaliana with an anti- has not been revealed in plants so far, although there is sense construct to the PIP1b aquaporin gene, which led some evidence of its existence [92]. to about threefold decrease in water permeability of the Aquaporin activity can be modulated by proteinÐ protoplast plasma membrane, was accompanied by a protein interactions with various partners, including the fivefold expansion of the root system [117]. The over- cytoskeletal components [93], calmodulin, and other expression of the same gene accelerated growth and proteins [94Ð96]. photosynthesis, elevated the density of stomata on a The ability of some aquaporins to bind Ca2+ and leaf surface, and stimulated transpiration in plants cyclic nucleotides is particularly important for regula- grown under favorable conditions. However, the viabil- tion in vivo. The Ca2+-binding activity of Aqp1 was ity of mutant plants under salt or drought stresses inferred from the structural similarity between its C- became impaired [118]. terminal domain and the EF-domains of calcium-bind- The aquaporin activity was discovered in stomatal ing proteins [97]. The binding of cGMP to Aqp1 aqua- guard cells [85, 119], in cells of the root extension zone porin also occurs in its C-terminal domain [39]. [120], and in some other cases. For example, aquapor- It was recently shown that the enlarged N-terminal ins play an important role in swelling and germination domain of several PIP1 aquaporins is capable of binding of pollen grains, thus providing self-incompatibility of flavin derivatives, including riboflavin. The complex pollination [121, 122]. formed upon this binding might be a photoreceptor [98]. The understanding of aquaporin role in root functions are currently expanding [109, 123, 124]. Appar- Phosphorylation was observed in cytoplasmic loops ently, the proteins of this family are directly responsible or terminal domains of many aquaporins. Phosphoryla- for rapid changes in root conductivity [125]. For exam- tion of aquaporins in Xenopus oocytes, triggered by ple, circadian periodicity of hydraulic conductivity in protein kinase A, often increases aquaporin activity Lotus japonicus was found to correspond to aquaporin [99, 100]. expression in the cells of the endodermis or vascular It remains unclear if this activation is due to the cylinder [126]. Aquaporins are also involved in the increased abundance of “conducting” aquaporin mole- adaptive decrease of root hydraulic conductivity upon cules or by a higher activity of individual molecules. In deprivation of mineral nutrition [127, 128]. The signif- plants, in vivo phosphorylation of aquaporins is often icance of aquaporins is indirectly confirmed by the correlated with the increase in the apoplast water poten- sensitivity of root conductivity to mercurial inhibitors tial. Thus, the aquaporin pool becomes less phosphory- [125, 128]. lated under water deficit, which reduces water perme- The increasing attention to the study of aquaporins ability of membranes and can be important for plant is fascinating even for the reason that proteins of this adaptation to drought [75]. broad family, many of which are predominant constitu- Phosphorylation of aquaporins in vivo was demon- ents in the membrane protein fraction, were discovered strated for several higher plant aquaporins, including so late and with so much effort. At present, the study of Nod26 from soybean, α-TIP from beans, and PM28A these proteins and their role in cell and organism phys- from spinach [86, 101Ð103]. The phosphorylation iology undergoes rapid development and will certainly occurs on serine residues. The conserved sequences lead to new unexpected discoveries. containing serine or threonine and presumably repre- senting phosphorylation sites were found in many aquaporins. 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