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The two sides of a lipid-protein story

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Abstract

Protein–membrane interactions play essential roles in a variety of cell functions such as signaling, membrane trafficking, and transport. Membrane-recruited cytosolic proteins that interact transiently and interfacially with lipid bilayers perform several of those functions. Experimental techniques capable of probing changes on the structural dynamics of this weak association are surprisingly limited. Among such techniques, electron spin resonance (ESR) has the enormous advantage of providing valuable local information from both membrane and protein perspectives by using intrinsic paramagnetic probes in metalloproteins or by attaching nitroxide spin labels to proteins and lipids. In this review, we discuss the power of ESR to unravel relevant structural and functional details of lipid–peripheral membrane protein interactions with special emphasis on local changes of specific regions of the protein and/or the lipids. First, we show how ESR can be used to investigate the direct interaction between a protein and a particular lipid, illustrating the case of lipid binding into a hydrophobic pocket of chlorocatechol 1,2-dioxygenase, a non-heme iron enzyme responsible for catabolism of aromatic compounds that are industrially released in the environment. In the second case, we show the effects of GPI-anchored tissue-nonspecific alkaline phosphatase, a protein that plays a crucial role in skeletal mineralization, and on the ordering and dynamics of lipid acyl chains. Then, switching to the protein perspective, we analyze the interaction with model membranes of the brain fatty acid binding protein, the major actor in the reversible binding and transport of hydrophobic ligands such as long-chain, saturated, or unsaturated fatty acids. Finally, we conclude by discussing how both lipid and protein views can be associated to address a common question regarding the molecular mechanism by which dihydroorotate dehydrogenase, an essential enzyme for the de novo synthesis of pyrimidine nucleotides, and how it fishes out membrane-embedded quinones to perform its function.

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Acknowledgments

The authors acknowledge the University of São Paulo, Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Grants No 2010/17662-8 and 2012/20367-3) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support. LGMB and LFSM hold FAPESP scholarships (2014/00206-0 and 2012/13309-7).

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    1. Laboratório de Biofísica Molecular, Departamento de Física, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil

      Luis G. Mansor Basso, Luis F. Santos Mendes & Antonio J. Costa-Filho

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    Luis G. Mansor Basso and Luis F. Santos Mendes contributed equally to this work.

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    Basso, L.G.M., Mendes, L.F.S. & Costa-Filho, A.J. The two sides of a lipid-protein story. Biophys Rev 8, 179–191 (2016). https://doi.org/10.1007/s12551-016-0199-5

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