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Membrane proteins can mediate uptake and release from mesoporous spheres

Transmembrane proteins that function as gateways to the cell interior can successfully transport ions against a chemical concentration gradient.
17 December 2012, SPIE Newsroom. DOI: 10.1117/2.1201212.004545

Transport across membranes is mediated by membrane proteins and underpins basic functions of living cells such as sensory perception and cell recognition. The uptake of specific ions, sometimes available only at very low concentrations, is also an integral part of biomineralization processes in living organisms. Membrane proteins are situated in the cell membrane, which consists of a bilayer of lipid molecules. Any attempt to study and use the function of membrane proteins requires synthetic model systems that mimic the natural environment. Limitations posed, for example, by the stability and size of commonly used hollow lipid bilayer spheres, called vesicles, have prompted the search for other, more cell-like systems. Recent work1, 2 has shown that porous silica spheres are particularly attractive due to their cytoskeleton pore-like inner structure and ease of depositing defect-free, ion-tight (i.e., not allowing the passage of molecules such as sodium and potassium) lipid bilayers onto the other surface. The use of a rigid porous particulate substrate is of interest in systems where mechanical stresses may otherwise destroy softer protein-containing colloidosomes or proteoliposomes. Such stresses may occur in ‘cell’ sorting operations, during mechanical agitation and stirring, and in high shear flows typical in microfluidic devices.

We have designed robust and versatile systems for selective uptake and release of ions from nanoporous particles sealed with ion-tight lipid bilayers of various compositions that also contain fully functional membrane proteins or peptides (protein components).2, 3 We produced porous silica spheres by two different techniques to yield particles characterized by a well-defined and connected porosity where specific target molecules4 can be contained in the aqueous network, and a very smooth outer surface that is essential for the formation of defect-free cell membranes around the particles. Indeed, the high specific surface area of the internal nanoporous space—which is also biomimetic with respect to organellar and other intracellular surfaces—allows for systems where internal reactive sites are made readily available, for example, in ion-induced biomineralization studies. We previously demonstrated how a multisubunit, trans-membrane complex ‘molecular machine,’ cytochrome c oxidase (CytcO), can be incorporated in a fully functional, reconstituted form into a lipid membrane supported on mesoporous silica colloids and used to transport protons across the cell membrane.2 The enzyme CytcO is a proton pump that is driven by electron transfer from cytochrome c to oxygen, which is reduced to water.

In our recent work,3 we showed that it is possible to introduce a passive ion-channel-type peptide (gramicidin A) and a more complex primary sodium-ion-transporter membrane protein—ATP (adenosine triphosphate) synthase—that operates in response to a chemical potential gradient or by the addition of ATP, the energy source used in cellular processes. Using a sodium-complexing dye, we demonstrated and quantified chemical potential- and ATP-driven transport of sodium ions across the supported lipid bilayer in real time by confocal scanning laser microscopy. Observation of passive and active sodium pumping detected via fluorescent dyes on a per-particle, time-resolved imaging basis, rather than as an integrated signal, is clearly advantageous for statistical analysis and may be useful in the construction of devices such as arrays and other deployments of this technology at a single-particle level. Specifically, we show that the ATP synthase-containing system can pump ions through an otherwise ion-tight membrane into the internal compartment of the particles against a concentration gradient.

Figure 1. Lipid-bilayer-coated mesoporous spheres are an excellent and versatile platform for designing systems for model studies of the function and response of membrane proteins, biomimetic microreactors, and protein-specific biosensing and drug delivery. A, B, and C represent different membrane proteins.

Designing robust and versatile lipid-bilayer-coated particle-based systems with fully functional membrane proteins is an important step for future studies of single or cascading membrane protein systems (see Figure 1). We plan to explore new possibilities for highly selective delivery vehicles and the design of microreactors that concentrate reactants at low concentrations and perform biomimetic reactions at specific locations in the porous network.

We thank Christoph von Ballmoos, Peter Brzezinski, Gustav Nordlund, and Vitaliy Oliynyk for fruitful collaboration. This work is supported by the Swedish Science Council and the Institute Excellence Centre CODIRECT. CODIRECT is hosted by YKI, Institute for Surface Chemistry, and is funded by Vinnova (the Swedish Governmental Agency for Innovation Systems), KK-stiftelsen (the Knowledge Foundation), the Swedish Foundation for Strategic Research, and industry.

Lennart Bergström, Jovice Boon Sing Ng
Department of Materials and Environmental Chemistry
Stockholm University
Stockholm, Sweden

Lennart Bergström, professor of materials chemistry, is the author of more than 140 papers and numerous book chapters, and has received many awards, including the Humboldt Research Award. His research is focused on colloidal processing and self-assembly of materials, often in nanostructural form.

Christian Mille
Department of Materials and Environmental Chemistry
Stockholm University
YKI, Institute for Surface Chemistry
Stockholm, Sweden
Robert Corkery
YKI, Institute for Surface Chemistry
Stockholm, Sweden

1. R. W. Davis, A. Flores, T. A. Barrick, J. M. Cox, S. M. Brozik, G. P. Lopez, J. A. Brozik, Nanoporous microbead supported bilayers: stability, physical characterization, and incorporation of functional transmembrane proteins, Langmuir 23, p. 3864-3872, 2007.
2. G. Nordlund, J. Boon Sing Ng, L. Bergström, P. Brzezinski, A membrane-reconstituted multisubunit functional proton pump on mesoporous silica particles, ACS Nano 3, p. 2639-2646, 2009.
3. V. Oliynyk, C. Mille, J. B. S. Ng, C. von Ballmoos, R. W. Corkery, L. Bergström, Selective and ATP-driven transport of ions across supported membranes into nanoporous carriers using gramicidin A and ATP synthase, (unpublished).
4. J. Boon Sing Ng, P. Kamali-Zare, H. Brismar, L. Bergström, Release and molecular transport of cationic and anionic fluorescent molecules in mesoporous silica spheres, Langmuir 24, p. 11096-11102, 2008.