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News Physiol Sci 13: 137-142, 1998;
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News in Physiological Sciences, Vol. 13, No. 3, 137-142, June 1998
© 1998 Int. Union Physiol. Sci./Am. Physiol. Soc.

The Dichotomy of MIP Family Suggests Two Separate Origins of Water Channels

Kenichi Ishibashi and Sei Sasaki

K. Ishibashi and S. Sasaki are in the Second Department of Internal Medicine of the Tokyo Medical and Dental University, Tokyo 113, Japan.

   Abstract
 
MIP family proteins can be divided into two groups according to their primary sequences. The CHIP group is predominant in the plant and animal kingdoms and functions primarily as water channels. The GLP group is a minor group with limited prevalence and functions primarily as glycerol transporters. Both prototypes are present in bacteria and may have evolved separately.


   Introduction
Top
 Introduction
Separation of MIP family...
 The distribution of two...
 Functional characteristics of...
 Origin and development of...
 NOTE ADDED IN PROOF
 References
 
The flow of small molecules into and out of cells is mediated by various classes of membrane proteins, i.e., pumps, transporters, and channels. Among such proteins, water-permeable pores of biological membranes have been studied for decades. They are referred to as "water channels." As water is vital for every living thing on earth, water channels and other water transport mechanisms are an important field of study. However, the molecular identity of water channels remained unknown until the discovery of a 28-kDa protein from human red blood cells. The identification of this protein, so-called "CHIP28," as a water channel has led to the discovery of a large family of water channels and related proteins (reviewed in Ref. 7). This family was first named the MIP family (MIP proteins) as an acronym for the first cloned protein of this family, the major intrinsic protein of lens fiber cells in the eye (12, 14). The members that were shown to function as water channels have been called aquaporins (AQP) to distinguish them from other uncharacterized or water-impermeable MIP proteins (7).

Now that the signature sequence has been identified (14), the number of identified MIP/AQP proteins is increasing. The signature sequences consist of two repetitions of NPA boxes (asparagine-proline-alanine), which may have been caused by ancient gene duplication (Fig. 1Go). They are widely distributed in bacteria, plants, and animals. In mammals, eight members have been cloned and shown to be aquaporins (see references cited in Refs. 5 and 7). Aquaporin 0 (AQP0) is MIP itself, a protein whose expression is limited in the fiber cell membranes of eye lens. AQP1 is CHIP28, a water channel whose expression is widely distributed in the body. AQP2 is a vasopressin-regulated water channel that is expressed selectively at the collecting duct of kidney. AQP3 and AQP4 are basolateral-type water channels that are expressed in several tissues such as kidney, colon, and trachea. AQP5 is an apical-type water channel that is expressed in the secretory glands. AQP6 is expressed in the kidney. AQP7 is expressed in testes and is present in sperm. In plants, many MIP proteins are identified (see references cited in Ref. 12). Arabidopsis thaliana has more than 23 different MIP proteins, and at least 9 are aquaporins. Some are present at the plasma membrane and some are present at the tonoplast or vacuolar membrane of plant cells. A nomenclature has not yet been worked out for plant aquaporins. In the bacteria Escherichia coli, one aquaporin has been identified that is named AQP-Z (1, 3).



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  		FIGURE 1. Schematic drawing of the transmembrane structures of 2 groups of MIP family proteins. There are 6 transmembrane segments. Both the amino (N) and carboxy (C) termini are located in the cytosol. B: 2 superfluous amino acid residues at extracellular domains in GLP group are shown with dotted lines.

 

   Separation of MIP family proteins into two groups
Top
 Introduction
 Separation of MIP family...
The distribution of two...
 Functional characteristics of...
 Origin and development of...
 NOTE ADDED IN PROOF
 References
 
The primary structures of these proteins are similar in size (250–290 amino acids). Following the variable length of the NH2 terminus is a hydrophobic stretch of six putative transmembrane helices. The COOH terminus is also variable in length and is hydrophilic. Both the NH2 terminus and the COOH terminus are in the cytosol (Fig. 1Go). There are two highly conserved amino acid residues, named NPA boxes. To find new aquaporins, we made polymerase chain reaction (PCR) primers of NPA boxes and amplified DNA sequences between these NPA boxes from the cDNA of several tissues. Two bands of 350 and 400 base pairs (bp) were detected in some tissues. When the PCR products were aligned, we realized that they were divided into two groups based on the presence or absence of extra amino acid residues at the second extracellular loop. Figure 2Go shows the hydropathy profiles of eight MIP proteins. The top four proteins [AQP3 (2, 6); AQP7 (5), C01G1.6, MIP protein of Caenorhabditis elegans (12); and GlpF, glycerol transporter of E. coli (12)] have longer amino acid sequences at the second extracellular loop (between helices 3 and 4, by 13–21 amino acids) as described in the PCR products. They also have longer amino acid sequences at the third extracellular loop (between helices 5 and 6, by 11–13 amino acids). Both are indicated by the horizontal bars in the AQP3 hydropathy profile in Fig. 2Go and by dotted lines in Fig. 1BGo. On the other hand, the bottom four proteins [AQP-Z (1, 3); SmpX, MIP protein of Synechococcus (cyanobacterium) (12); NOD (nodulin 26), a nodule-specific symbiosome membrane protein from soybean (12); and AQP1] have shorter amino acid sequences in these places. Interestingly, both of the extra amino acid residues always coexist, and no MIP proteins have been identified that have only one of these extra amino acid residues.



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  		FIGURE 2. Hydropathy analysis of 8 representative members of MIP family. Y-axis shows hydrophobicity index; X-axis shows number of amino acids. The 2 horizontal bars in AQP3 hydropathy profile represent the extra sequences that distinguish GLP group from CHIP group.

 
We named the latter group the CHIP group, as represented by CHIP28 (AQP1), and the former group the GLP group, as represented by GlpF (Table 1Go). Previously, based on the fact that only a single MIP gene (GlpF) had been found in bacteria, Reizer et al. (14) postulated that a single MIP gene was vertically transmitted from prokaryotes to a different eukaryotic kingdom. However, Agre's group (1) and later our own group (3) also found another MIP family protein (AQP-Z) in E. coli that belongs to the CHIP group. Therefore, bacteria (E. coli) already have a prototype of each group, AQP-Z and GlpF, indicating that the duplication of the ancestor gene to two prototypes occurred in the very early phase of its evolution.


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  		TABLE 1. MIP family divided into two groups
 
Four MIP proteins that belong to the GLP family have been reported from the C. elegans genome project (12). In addition to several AQPs that belong to the CHIP group, we and others found a GLP group protein (AQP3 and AQP7) in rat (2, 5–7), indicating that mammals also have both CHIP and GLP proteins. Therefore, the two bacterial MIP proteins may have evolved separately up to mammals. Recently, Park and Saier (12) have divided MIP proteins into two groups according to their homology of protein sequences. Their division agrees with our above-described division based on the presence or absence of two extra amino acid residues. We think our division is more practical because MIP proteins are now easily classified by the comparison of the length of sequences between NPA boxes. Moreover, these extra amino acid residues may shed light on the functional relevance as is discussed below.

The genomic structure also suggests the division of MIP proteins into two subgroups in mammals. AQP0–2 and AQP4–6, both belonging to the CHIP group, have similar exon-intron boundaries. However, the exon-intron boundaries of AQP3 are quite different from those of the above MIP proteins (4). This suggests that both proteins originated from separate ancestors before the introduction of the intron. Furthermore, the chromosomal localization of human aquaporins revealed that AQP0, AQP2, AQP5, and AQP6 are colocalized at chromosome 12q13, suggesting that they derived from gene duplication.


   The distribution of two groups of MIP family proteins in living organisms
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 Introduction
 Separation of MIP family...
 The distribution of two...
Functional characteristics of...
 Origin and development of...
 NOTE ADDED IN PROOF
 References
 
As stated above, both groups of MIP proteins are present in bacteria (Table 1Go; references cited in Ref. 12). In E. coli, two MIP proteins, i.e., AQP-Z and GlpF, are present and represent each group. Haemophilus influenzae also has two MIP proteins that represent each group. As the complete genome sequence is known in both bacteria, it is unlikely that another MIP protein is present in these bacteria. On the other hand, the complete genome sequences of some mycoplasma and synechococcus bacterium revealed the presence of a single MIP protein in these organisms. These all belong to the CHIP group. Whether the MIP protein of the GLP group has been lost in these bacteria or whether E. coli and H. influenzae have acquired the GLP group is unknown. Interestingly, the complete genome sequence of one of the archeon, Methanococcus jannaschii, revealed the absence of MIP proteins. In eukaryotes, MIP proteins are also widely distributed. The complete genome sequence of one yeast (Saccaromyces cerevisiae) revealed the presence of four MIP proteins, two from the CHIP group and two from the GLP group. It is surprising that a single cell such as yeast has four MIP proteins, although one member of the CHIP group may be a pseudogene.

In plants, all MIP proteins identified so far belong to the CHIP group. The distribution of MIP proteins in plants is diverse and can be divided into three subgroups: plasma membrane type (PIP), tonoplast type (TIP), and symbiosome type (NOD). Most of these PIPs and TIPs are expressed in all organ systems (roots, leaves, fruits, and stems). It is intriguing that no MIP proteins belonging to the GLP group have been found in plants. One of the lower animals, C. elegans, has four MIP proteins belonging to the GLP group and two belonging to the CHIP group, as revealed by the C. elegans genome project currently underway. In insects, only two MIP proteins, both belonging to the CHIP group, have been cloned. One is BIB (big brain of Drosophila), a homologue of mammalian AQP4, and its absence results in a big brain due to the impairment of the ectoderm differentiation. The other is AQP-CIC expressed at the digestive tract. In higher animals, both groups are present. In fish, we identified a member of the GLP group from Petromyzon (Ishibashi, unpublished observation). Two CHIP group proteins are reported from toad bladder. So far, extensive searches for MIP proteins have been performed only in mammals. Of the eight MIP proteins thus far reported, six belong to the CHIP group and two to the GLP group. Although more MIP proteins are expected to be identified in mammals, the current limitation of the GLP group distribution is intriguing.


   Functional characteristics of two MIP groups
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 Introduction
 Separation of MIP family...
 The distribution of two...
 Functional characteristics of...
Origin and development of...
 NOTE ADDED IN PROOF
 References
 
Most of the CHIP group proteins have been shown to stimulate osmotic water permeability of plasma membrane when expressed in Xenopus oocytes, cells that have a very low endogenous water permeability. There has been some controversy over functions other than water transport. MIP26 protein has been reported to be an ion channel in reconstitution studies in liposomes. However, a recent study of its expression in Xenopus oocytes revealed it to have a small water channel function and no capacity for ion permeation. Thus it has been renamed AQP0 (7). The previous ion channel activity may be artifactual for the reconstitution in liposomes. RD28, a protein that is induced by desiccation of Arabidopsis thaliana, was recently shown to be a mercury-insensitive aquaporin. Furthermore, similar MIP proteins (PIPs) from plasma membrane of A. thaliana have been shown to be aquaporins. Tonoplast intrinsic proteins (TIP) are also shown to stimulate water transport. MIP protein from the digestive tract of homopteran insects has been shown to transport water (AQP-CIC). Therefore, the function of the CHIP group can be generalized as a water channel activity.

On the other hand, the GLP group seems to be functionally specialized for the transport of glycerol. GlpF stimulated glycerol uptake but failed to transport water when expressed in Xenopus oocytes (11). GlpF exists within operons encoding other known glycerol metabolic enzymes. Because glycerol is used as an organic osmotic solute (osmolyte) as well as an energy source in bacteria and some yeasts, the transport of glycerol by GLP group proteins may be important for osmoregulation in these lower organisms. The glycerol taken up through GlpF is phosphorylated by glycerol kinase, a member of the same operon, and then trapped in the cell. In the case of yeast, glycerol accumulated in the cytosol in the hypertonic environment also acts as an osmolyte. When the yeast is exposed to hypotonic medium, the accumulated glycerol is rapidly lost from the cell to prevent the attraction of water from outside. FPS1, which is inactivated in hypertonic medium, functions as an exit pathway for the glycerol after exposure to hypotonic medium (9). AQP3 and AQP7, proteins that belong to the GLP group and facilitate glycerol transport, are unique in that they also transport water, functioning as aquaporins (2, 5–7).

How is the specificity of water channels determined? Previous studies showed that AQP1 was highly specific to water permeation but excluded urea and glycerol, suggesting that the channel formed by AQP1 is too narrow to allow molecules other than water to pass through (see references cited in Ref. 7). However, GlpF of E. coli has been shown to exclude water when expressed in oocytes (11). The transport kinetics of glycerol transport through GlpF is nonsaturable and has a low temperature dependency (Arrhenius activation energy: 4.5 kcal/mol), suggesting that the channel mechanism of transport is most likely. Therefore, the size of the pore may not be the sole determinant of the water permeation capacity. GlpF may have glycerol binding sites to facilitate glycerol transport and/or a hydrophobic barrier to exclude water. The two sites of extra amino acid sequences (dotted lines in Fig. 1Go) that distinguish the CHIP group and the GLP group are mostly polar and located at extracellular loops. It is tempting to speculate that these extra amino acids are necessary for the binding to glycerol. We reported that the water and glycerol transport of AQP3 showed similar kinetics, i.e., a low temperature dependency (3.7 and 6.0 kcal/mol, respectively) and inhibition by mercury and phloretin (6). On the basis of these observations, we speculated that water and glycerol are transported through the same channel in AQP3.

However, a recent report by Echevarria et al. (2) on the kinetics of glycerol transport through AQP3 conflicts with our view. The water permeability of AQP3 was inhibited by mercury, but the glycerol permeability of AQP3 was not. Their estimation of the activation energy of AQP3 for glycerol transport was high (12.2 kcal/mol). They speculated that a glycerol pathway separate from the water channel was present and concluded that AQP3 forms a water-selective channel and glycerol was transported through the separate pathway. The transport kinetics of glycerol transport of AQP3 in their study (2) is completely different from those of GlpF. The transport of glycerol through GlpF has a low temperature dependence (4.5 kcal/mol) and is inhibited by mercury and phloretin (11). The reason for the discrepancies in the AQP3 transport characteristics reported by different researchers (2, 6) remains unclear. Cloned AQP7 (5) also transports water and glycerol with low activation energy (2.1 and 5.3 kcal/mol, respectively). The similar kinetics of water and glycerol transports does not mean that they share the same pathway. If glycerol affects (decreases) water permeability induced by AQP3 expression, water and glycerol are most likely transported through a common pore. The idea of the separate pathway for water and glycerol is interesting, and further site-directed mutagenesis as well as swapping studies may identify the mechanism of the selectivity differences.


   Origin and development of water channels
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 Introduction
 Separation of MIP family...
 The distribution of two...
 Functional characteristics of...
 Origin and development of...
NOTE ADDED IN PROOF
 References
 
It is worthwhile here to speculate on how water channels have come about and evolved in living organisms. In unicellular organisms, water transport at the cytoplasmic membrane should be minimized to keep the cell volume constant. Unicellular organisms adapt to changes in extracellular osmolarity not by transporting water but by transporting or producing osmolytes. Thus the emergence of water channels at the plasma membrane may be suppressed. In fact, no MIP proteins have been found in the methanogenic archeon that grows at temperatures in the range of 48–94°C. Although the localization of AQP-Z, a bacterial aquaporin, has not been reported, we speculate that CHIP group proteins in eubacteria may not be localized at the plasma membrane. On the other hand, some intracellular organelles such as endosomes may need the facilitated water transport to minimize the generation of an osmotic gradient between intracellular compartments. Alternatively, water channels in the endosomes may permit the use of the vacuolar space for rapid osmoregulation of the cytoplasm. For example, plants have four aquaporins in their tonoplast (an intracellular organelle). When challenged with a hypotonic environment, the accumulated water in the cytosol may be rapidly transported to the vacuoles to prevent the cell lysis. Evolutionarily, the aquaporins of intracellular organelles may then have had access to the plasma membrane by way of membrane fusion via exocytosis.

The aquaporins at the cytoplasmic membrane may provide an efficient pathway for water to minimize the osmotic gradient between cell and interstitium. This is particularly important in places where the interstitial osmolarity differs from that of the cytoplasm. The examples are kidney medulla and colon, tissues where the interstitial hypertonic osmolarity is maintained to concentrate urine and feces, respectively. Two aquaporins are present at such membranes: AQP3 from the GLP group and AQP4 from the CHIP group colocalize at the basolateral membrane of kidney collecting duct cells and colonic surface epithelia (see references cited in Ref. 7). Because both AQP3 and AQP4 are water channels, it is intriguing to find both aquaporins at the same membrane. Speculatively, AQP3 stemmed from GlpF and has always been localized at the plasma membrane, whereas AQP4 stemmed from AQP-Z and may have found its way to the plasma membrane from the endosomes through exocytosis. This mechanism of delivering aquaporins from endosomes to plasma membranes seems to be conserved in other CHIP members. For example, AQP2 is present at endosomes in a hydrated state. When dehydrated, AQP2 is exocytosed to the apical membrane with the stimulation of vasopressin (see references cited in Ref. 7). Similarly, AQP1 has also been shown to translocate to plasma membrane from vesicle when stimulated by secretin in cholangiocytes (10).

In multicellular organisms, the role of water channels extends from cell volume regulation to transepithelial water transport. The epithelial cells transport water vectorially through aquaporins at plasma membranes, driven by an osmotic gradient that facilitates water absorption or secretion. Compared with paracellular transport, this transcellular transport has the advantage of ease in regulation. In tight epithelia such as kidney collecting ducts, transcellular water transport is predominant. The transcellular water transport can be facilitated by opening aquaporins through phosphorylation as documented in AQP1 (15), AQP2 (4), and AQP-{alpha}TIP or by increasing their number at the plasma membrane through exocytosis as shown in AQP1, AQP2, and possibly AQP5. As the regulation of water transport is tissue specific, it is not surprising that a variety of aquaporins may be produced by gene duplication in various tissues in multicellular organisms. On the other hand, the paracellular transport of water is important in leaky epithelia. For example, no aquaporins have been identified so far in the epithelia of the small intestine. However, even such leaky epithelia have at least one aquaporin, i.e., AQP1 in kidney proximal tubular cells, in gallbladder epithelia, and in choroid plexus epithelia (see references cited in Ref. 8). As people with nonfunctional mutation of AQP1 show no obvious abnormality (13), the role of aquaporins in such leaky epithelia remains to be clarified.

In summary, the evolution of MIP family proteins should be reevaluated now that new members have been discovered in mammals (AQP3 and AQP7) and bacteria (AQP-Z). MIP proteins can be classified into two groups, depending on their primary sequences. This separation may have functional relevance: relatively selective transport of water or glycerol. The separate evolution of each group should be considered in the evaluation of the distribution of MIP proteins. The recognition of the two groups in the MIP family may facilitate the research of this ancient protein family.


   NOTE ADDED IN PROOF
Top
 Introduction
 Separation of MIP family...
 The distribution of two...
 Functional characteristics of...
 Origin and development of...
 NOTE ADDED IN PROOF
References
 
Recent survey of the C. elegans genome revealed two more MIP proteins (CHIP group: CEH09F14, Z95391; and GLP group: C35A5.1, Z71185). We have also cloned two more aquaporins from mammals (CHIP group AQP8: AB005547, and GLP group AQP9: AB008775).


   References
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 Introduction
 Separation of MIP family...
 The distribution of two...
 Functional characteristics of...
 Origin and development of...
 NOTE ADDED IN PROOF
 References
 

  1. Calamita, G., W. R. Bishai, G. M. Preston, W. B. Guggino, and P. Agre. Molecular cloning and characterization of aqpZ, a water channel from Escherichia coli. J. Biol. Chem. 270: 29063–29066, 1995.[Abstract/Free Full Text]
  2. Echevarria, M., E. E. Windhager, and G. Frindt. Selectivity of the renal collecting duct water channel aquaporin-3. J. Biol. Chem. 271: 25079–25082, 1996.[Abstract/Free Full Text]
  3. Fushimi, K., L. Bai, F. Marumo, and S. Sasaki. Isolation of a gene encoding nodulin-like intrinsic protein of Escherichia coli. Biochem. Mol. Biol. Int. 41: 995–1003, 1997.[Medline]
  4. Inase, N., K. Fushimi, K. Ishibashi, S. Uchida, M. Ichioka, S. Sasaki, and F. Marumo. Isolation of human aquaporin3 gene. J. Biol. Chem. 270: 17913–17916, 1995.[Abstract/Free Full Text]
  5. Ishibashi, K., M. Kuwahara, Y. Gu, Y. Kageyama, A. Tohsaka, F. Suzuki, F. Marumo, and S. Sasaki. Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J. Biol. Chem. 272: 20782–20786, 1997.[Abstract/Free Full Text]
  6. Ishibashi, K., S. Sasaki, K. Fushimi, S. Uchida, M. Kuwahara, H. Saito, T. Furukawa, K. Nakajima, Y. Yamaguchi, T. Gojobori, and F. Marumo. Molecular cloning and expression of a new member of the aquaporin family (AQP3) with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc. Natl. Acad. Sci. USA 91: 6269–6273, 1994.[Abstract/Free Full Text]
  7. King, L. S., and P. Agre. Pathophysiology of the aquaporin water channels. Annu. Rev. Physiol. 58, 619–648, 1996.[Medline]
  8. Kuwahara, M., K. Fushimi, Y. Terada, L. Bai, F. Marumo, and S. Sasaki. cAMP-dependent phosphorylation stimulates water permeability of aquaporin-collecting duct water channel protein expressed in Xenopus oocytes. J. Biol. Chem. 270: 10384–10387, 1995.[Abstract/Free Full Text]
  9. Luyten, K., J. Albertyn, W. F. Skibbe, B. A. Prior, J. Ramos, J. M. Thevelein, and S. Hohmann. Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J. 14: 1360–1371, 1995.[Medline]
  10. Marinelli, R. A., L. Pham, P. Agree, and N. F. LaRusso. Secretin promotes osmotic water transport in rat cholangiocytes by increasing aquaporin-1 water channels in plasma membrane: evidence for a secretin-induced vesicular translocation of aquaporin-1. J. Biol. Chem. 272: 12984–12988, 1997.[Abstract/Free Full Text]
  11. Maurel, C., J. Reizer, J. I. Schroeder, M. J. Chrispeels, and M. H. Saier, Jr. Functional characterization of the Escherichia coli glycerol facilitator, GlpF, in Xenopus oocytes. J. Biol. Chem. 269: 11869–11872, 1994.[Abstract/Free Full Text]
  12. Park, J. H., and M. H. Saier, Jr. Phylogenetic characterization of the MIP family of transmembrane channel proteins. J. Membr. Biol. 153: 171–180, 1996.[Medline]
  13. Preston, G. M., B. L. Smith, M. L. Zeidel, J. J. Moulds, and P. Agre. Mutations in aquaporin-1 in phenotypically normal human without functional AQP water channels. Science 265: 1585–1587, 1994.[Abstract/Free Full Text]
  14. Reizer, J., A. Reizer, and M. H. Saier. The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution and proposed functional differentiation of the two repeated halves of the proteins. Crit. Rev. Biochem. Mol. Biol. 28: 235–257, 1993.[Medline]
  15. Yool, A. J., W. D. Stamer, and J. W. Regan. Forskolin stimulation of water and cation permeability in aquapoin 1 water channels. Science 273:1216–1218, 1996.[Abstract]



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