Aquaglyceroporins: ancient channels for metalloids

Abstract

A Aq qu ua ag gl ly yc ce er ro op po or ri in ns s: : a an nc ci ie en nt t c ch ha an nn ne el ls s f fo or r m me et ta al ll lo oi id ds s Hiranmoy Bhattacharjee, Rita Mukhopadhyay, Saravanamuthu Thiyagarajan and Barry P Rosen Address: Department of Biochemistry and Molecular Biology, Wayne State University, School of Medicine, Detroit, MI 48201, USA.Correspondence: Barry P Rosen. Email: brosen@med.wayne.edu Arsenic, a metalloid, is widely distributed in the Earth's crust and is toxic to all forms of life. Humans can be exposed to arsenic from drinking water that has flowed through arsenicrich rocks or from crops that have been irrigated with arseniccontaminated water. Arsenic occurs predominantly in the environment as the pentavalent arsenate (As(V)) and trivalent arsenite (As(III)) forms. Arsenite is more toxic than arsenate and is primarily responsible for the biological effects of arsenic. The toxicity of arsenite is due to its affinity for closely spaced cysteine thiolates; it inactivates enzymes and receptors by binding to active site cysteine residues or by preventing formation of disulfide bonds. Arsenite also leads to the production of reactive oxygen species by binding to reduced glutathione. In addition to the severe health effects of arsenic in drinking water, its accumulation in crops such as rice jeopardizes the safety of our food supply [1]. An understanding of the pathways of arsenic uptake, metabolism, and elimination will help in developing strategies to produce plants that take up essential metalloids while excluding toxic ones.A Aq qu ua ag gl ly yc ce er ro op po or ri in ns s a an nd d m me et ta al ll lo oi id d t tr ra an ns sp po or rt t A little over a decade ago, Sanders et al.[2] isolated a mutant of GlpF, the glycerol facilitator of Escherichia coli, that was resistant to antimonite (Sb(III)). Later, Meng et al. [3] determined that this mutant also exhibits a 90% reduction in arsenite uptake. Antimony is another metalloid in the same group of the periodic table as arsenic (Figure 1). GlpF is a member of the major intrinsic protein (MIP) or aquaporin superfamily of channels for water and small solutes that is widely expressed in nearly every organism. Aquaporins fall into two broad groups, aquaporins or water-specific channels, and aquaglyceroporins, which conduct water, glycerol and other small, uncharged solutes.It might seem surprising that a transporter for water and small organic compounds could transport a metalloid. However, analysis of the state of trivalent arsenic in solution shows how this is possible. Although trivalent inorganic arsenic is often referred to as an anion, arsenite, in solution, has a pK a of 9.2, and it is therefore protonated at physiological pH. Extended X-ray absorption fine structure (EXAFS) analysis has shown that in aqueous solution there are three oxygen ligands 1.78 Å from the arsenic atom; the major species in solution is therefore the neutral hydroxide As(OH) 3 , which is an inorganic molecular mimic of glycerol [4]. A Ab bs st tr ra ac ct tTh...

Functional and molecular characteristics of rice and barley NIP aquaporins transporting water, hydrogen peroxide and arsenite

“…In the present study, OsNIP3;2 and OsNIP3;3 were characterized as H 2 O 2 -permeable NIPs. As for arsenite transport, OsNIP3;3 and HvNIP1;2 were identified to show arsenite transport activity in addition to previously reported NIPs from rice, Arabidopsis, or Lotus japonicus (Ali et al 2009;Bhattacharjee et al 2008;Bienert et al 2008;Isayenkov and Maathuis 2008;Kamiya et al 2009;Ma et al 2008). Because OsNIP3;3 was found as an arsenite transporter, the effects of As(OH) 3 on the expression of OsNIP3;3 in rice plants were investigated (supplementary Figure S4).…”

“…Ma et al (2008) demonstrated that arsenite is transported via NIP aquaporins. Previously some rice NIPs (OsNIP1;1, OsNIP2;1= Lsi1, OsNIP2;2= Lsi6, OsNIP3;1, OsNIP3;2) were investigated as silicon (Si(OH) 4 ) or arsenite (As(OH) 3 ) transporters (Ali et al 2009;Bhattacharjee et al 2008;Bienert et al 2008;Ma et al 2008), but their water transport activities are not yet well understood. Novel OsNIP3;3 was characterized in the present study.…”

Boron Toxicity Tolerance in Barley through Reduced Expression of the Multifunctional Aquaporin HvNIP2;1

“…Five major subgroups of aquaporins in plants are now recognized (Danielson and Johanson, 2008;Sade et al, 2009;Shelden et al, 2009). In particular, members of one of these subgroups, the nodulin-26-like intrinsic proteins (NIPs), were recently described as functional equivalents of aquaglyceroporins (Bhattacharjee et al, 2008). These channel pro-teins usually enable water transport but recent studies have demonstrated that they also facilitate transport of other small, uncharged solutes under physiological conditions including glycerol and lactic, boric (B), silicic (Si), arsenious (As), antimonious (Sb), and germanic (Ge) acids (Ma et al, 2006Takano et al, 2006;Choi and Roberts, 2007;Bienert et al, 2008;Chiba et al, 2008;Isayenkov and Maathuis, 2008;Tanaka et al, 2008;Kamiya et al, 2009;Mitani et al, 2009).…”

Aspergillus glaucus Aquaglyceroporin Gene glpF Confers High Osmosis Tolerance in Heterologous Organisms

“…Aquaporins share limited similarity with respect to sequence identity and differ in size, but the reported X-ray structures of aquaporins, such as bovine AQP0, human AQP1, E. coli AqpZ and GlpF, spinach SoPIP2;1, and Plasmodium falciparum PfAQP, show that these proteins share a conserved overall typical hourglass model (43)(44)(45). AQPs are assembled as homotetramers consisting of four independent monomers embedded in the lipid bilayer (46).…”