Cited by 169Origins and Evolution of LifeATP Synthase and ATPases ResearchLipid Membrane Structure and Behavior

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Co-evolution of primordial membranes and membrane proteins

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Mulkidjanian, Armen Y., Galperin, Michael Y., Koonin, Eugene V.·2009·Trends in Biochemical Sciences

DOI 10.1016/j.tibs.2009.01.005PMC PMC2752816

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Abstract

Studies of the past several decades have provided major insights into the structural organization of biological membranes and mechanisms of many membrane molecular machines. However, the origin(s) of the membrane(s) and membrane proteins remains enigmatic. We discuss different concepts of the origin and early evolution of membranes with a focus on the evolution of the (im)permeability to charged molecules such as proteins, nucleic acids and small ions. Reconstruction of the evolution of F-type and A/V-type membrane ATPases (ATP synthases), which are either proton- or sodium-dependent, might help us to understand not only the origin of membrane bioenergetics but also of membranes themselves. We argue that evolution of biological membranes occurred as a process of co-evolution of lipid bilayers, membrane proteins and membrane bioenergetics.

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VMD: visual molecular dynamics
Humphrey, W., Dalke, A., & Schulten, K. (1996) · Journal of Molecular Graphics · doi:10.1016/0263-7855(96)00018-5 · Cited by 66,952
CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION
Mitchell, P. D. (1966) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1966.tb01501.x · Cited by 3,674
THE ATP SYNTHASE—A SPLENDID MOLECULAR MACHINE
Boyer, P. D. (1997) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.66.1.717 · Cited by 2,014
Synthesizing life
Szostak, J. W., Bartel, D. P., & Luisi, P. L. (2001) · Nature · doi:10.1038/35053176 · Cited by 1,681
Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology
Forgac, M. D. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2272 · Cited by 1,626
Intracellular protein topogenesis
Blobel, G. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.3.1496 · Cited by 1,393
The biological chemistry of the elements: the inorganic chemistry of life
(1992) · Choice Reviews Online · doi:10.5860/choice.30-0286 · Cited by 1,326
Biomembranes: molecular structure and function
(1989) · Choice Reviews Online · doi:10.5860/choice.27-0304 · Cited by 1,232
The universal ancestor
Woese, C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.6854 · Cited by 1,053
Data growth and its impact on the SCOP database: new developments
Andreeva, A. E., Howorth, D., Chandonia, J., Brenner, S. E., Hubbard, T., Chothia, C., & Murzin, A. G. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm993 · Cited by 933

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Authors: Mulkidjanian, A. Y., Galperin, M. Y., & Koonin, E. V.
Affiliations: Osnabrück University (DE)
National Institutes of Health (US)
Corresponding author: Mulkidjanian, Armen Y.
Koonin, Eugene V.
ORCID: Mulkidjanian, Armen Y.
Galperin, Michael Y.
Koonin, Eugene V.
Venue: Trends in Biochemical Sciences
Publisher: Elsevier BV
Published: 2009-04
Volume: 34
Issue: 4
Pages: 206-215
ISSN: 0968-0004 (ISSN-L)
DOI: 10.1016/j.tibs.2009.01.005
PMC: PMC2752816
OpenAlex: W2153085358
Cited by: 169
References: 105
Citations by year: 2026: 6 · 2025: 7 · 2024: 14 · 2023: 7 · 2022: 9 · 2021: 12 · 2020: 8 · 2019: 9 · 2018: 4 · 2017: 5 · 2016: 9 · 2015: 13 · 2014: 11 · 2013: 14 · 2012: 12
FWCI: 0.96
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Biochemical Sciences (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
U.S. National Library of Medicine (Z01LM000073)
Topics: Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Keywords: membrane protein evolution, lipid bilayers, membrane permeability, membrane ATPase, F-type ATP synthase, membrane bioenergetics, coevolution
MeSH terms: Adenosine Triphosphatases, Cell Membrane, Biological Evolution, Membrane Proteins, Evolution, Molecular

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Co-evolution of primordial membranes and membrane proteins

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