Although the Piscataqua River forms a natural boundary between Maine and New Hampshire, these two states have disputed the exact location of their border for the last 260 years. Maine contends that the state line runs through the middle of the Piscataqua River. New Hampshire maintains that the boundary lies on the river’s north shore.
This border dispute recently came to a head when the New Hampshire attorney general’s office filed a petition with the U.S. Supreme Court.1 This petition was precipitated by 15 years of research conducted by Victor Bourre, a former shipyard worker. Bourre, who retired from the Portsmouth Naval Shipyard, challenged the placement of the border to avoid paying back income taxes to the state of Maine. If the border falls on the river’s north shore, the Portsmouth Naval Shipyard resides in New Hampshire—a state without income taxes. If the border runs through the middle of the river, then the shipyard belongs to Maine and the 1,300 workers who live in New Hampshire must pay Maine state income tax—totaling six million dollars a year in revenue.
Borders are important. These boundaries not only affect economics, they also define and characterize cities, counties, states, and nations. Similar to the way borders demarcate states, cell membranes define life’s boundaries.2 The cell’s membrane separates its contents—its structures and their chemical processes—from the exterior environment. The chemistry inside the cell constitutes life; outside the cell the same chemical processes are abiotic (without life).
Cellular membranes play a critical role in cell survival. The cell membrane, like a well-guarded border, keeps harmful materials from entering the cell and sequesters beneficial compounds in its interior. Like border patrol checkpoints, proteins embedded in the cell’s membrane regulate the traffic of materials into and out of the cell. These transport proteins ensure that the cell imports necessary nutrients and efficiently deports waste products.
Complex (eukaryotic) cells also possess an internal network of membranes that segregates the cell’s activities. The membranes of organelles (structures inside the cell that carry out specific functions) serve as a key site for photosynthesis and energy production. In both cases, the movement of chemicals through membranes generates chemical energy to drive cellular processes—much as shipyard workers crossing Maine’s border fuel the economy through tax revenue.
Sometimes a natural boundary, such as a river, forms a state’s border; at other times a border is determined by the careful, deliberate intent of a sovereign authority for specific purposes. Did cell membranes originate through natural processes, or did they come about through the deliberate activity of an Intelligent Designer?
Because cell membranes play such a critical and defining role for life, evolutionary models must account for their occurrence relatively early in the origin-of-life pathway.3 In fact, the origin of cell membranes represents the initial step in the emergence of protocells (precursors to the first cells). In spite of their importance, origin-of-life researchers have focused limited attention on the problem of membrane origins. Instead, most investigators expend significant effort trying to explain the emergence of self-replicating systems (RNA, DNA, and proteins) and metabolism.
These researchers assume, for the most part, that once membrane components appeared on early Earth, they self-assembled to form the first cell membranes.4 However, data produced over the last 15 years by biochemists studying the physicochemical properties of membranes and their components challenge evolutionary explanations for membrane formation. Moreover, these advances, unaccounted for in naturalistic models, provide evidence for design as an integral feature of cell membranes and, thus, for a supernatural origin of life.
To explain the origin of cell membranes and the emergence of the first protocell, origin-of-life investigators seek to identify compounds likely to be present on the early Earth with the potential to spontaneously assemble into bilayer structures. These scientists also look for mechanisms by which bilayer structures can encapsulate self-replicating molecules and acquire capacities that resemble those of contemporary cell membranes, such as transport and energy transduction.
In the quest to identify bilayer-forming molecules, scientists have discovered several chemical routes that produce both simple amphiphilic compounds (consisting of a single long hydrocarbon chain) and more complex phospholipids (see “Cell Membrane Essentials” sidebar).5 Despite this seemingly favorable discovery, the origin-of-life community hotly debates the likelihood that these chemical routes occurred on early Earth.6
Some researchers appeal to the infall of extraterrestrial materials to explain the source of bilayer-forming compounds.7 Analysis of carbon-containing meteorites (carbonaceous chondrites), such as the Murchison meteorite, initially indicated the presence of compounds consisting of long hydrocarbon chains. However, subsequent analysis demonstrated that these compounds came from contact with Earth (terrestrial contamination).8
Recent laboratory experiments rejuvenate support for an extraterrestrial source of amphiphilic materials on Earth.9 Scientists from NASA Ames, the SETI Institute, and the University of California, Santa Cruz, demonstrated that simulated cometary and interstellar ice irradiated with UV light produces a complex mixture of compounds that includes bilayer-forming materials. Presumably, delivery of these materials to Earth provided the compounds needed to form life’s boundaries, the first cell membranes. Even though phospholipids are the dominant lipid species of contemporary cell membranes, origin-of-life researchers think that simpler lipids may have assembled to form the first bilayers.
Formation of Bilayers
Amphiphilic compounds form aggregates when added to water. These aggregates take on a variety of forms depending on the amphiphile’s molecular structure.10 Phospholipids with two long hydrocarbon chains can form bilayers. Amphiphilic compounds with a single long hydrocarbon chain generally form spherical structures, referred to as micelles (figure 5). Just as lakes don’t carry the same value as rivers in forming borders, origin-of-life researchers don’t regard micelles as having importance in forming the first protocells.
In spite of their tendency to form micelles, some single-chain amphiphilic compounds form bilayers under highly specific temperatures and solution conditions (pH, for example) when mixed with the right materials.11 Researchers regard these results as key to explaining the first appearance of cell membranes.
The significance of these results increases in light of the observation that lipid-like materials extracted from the Murchison meteorite form bilayer structures under specific solution conditions.12 Similar bilayer structures also form from extracts of simulated cometary and interstellar ice irradiated with UV light.13 Evolutionary researchers point to these compounds as possibly the first cell-membrane components and as evidence that the materials necessary to form the first protocells’ boundary structures were present on the early Earth. They also argue that these results indicate the ease with which bilayers can spontaneously form once the right components appear. Researchers presume that, once formed, primitive membranes transitioned to bilayers composed of phospholipids.
These few studies seem to reinforce the view that Earth’s first cell membranes readily self-assembled. However, other research designed to characterize the structure of lipid aggregates and to determine the principles governing cell membrane biophysics suggests that evolutionary models for the origin of biological membranes are oversimplified. The emerging tenets of membrane biophysics demand a more convoluted and intricate pathway than that conceived by the evolutionary community.
Challenges to Natural Start
Researchers think that the primitive membranes of the first protocells were composed of aromatic hydrocarbons mixed with octanoic and nonanoic acid. (Octanoic acid consists of a linear carbon chain eight carbon atoms in length, and nonanoic acid consists of a linear carbon chain nine carbon atoms long.) Extracts from the Murchison meteorite formed bilayer structures containing these compounds.
These results, however, can be misleading. Neither octanoic nor nonanoic acid would have occurred at significant levels in any given origin-of-life scenario. Furthermore, the level of amphiphilic compounds in the Murchison meteorite decreases dramatically with increasing chain length.14 Researchers have recovered extremely low levels of octanoic and nonanoic acids from the Murchison meteorite.15 While extraterrestrial infall could conceivably deliver these two compounds to Earth, the levels would be far too low to form primitive membrane structures. Octanoic and nonanoic acids can form bilayer structures only at relatively high concentrations.16 Under laboratory conditions, researchers easily achieved artificially high concentrations of octanoic and nonanoic acids by extraction and concentration procedures. However, these concentrations are not expected to occur readily, spontaneously, on early Earth.
In addition to this concentration problem, octanoic and nonanoic acids need exacting environmental conditions to form bilayers. Both compounds form bilayers only at very specific pH levels.17 Octanoic and nonanoic bilayers become unstable if the solution pH deviates from nearly neutral values. The solution temperature is critical for bilayer stability as well.18
Octanoic and nonanoic bilayer stability also requires “just right” molecular companions. For example, inclusion of nonanol (a nine carbon alcohol) at specific levels stabilizes nonanoic acid bilayers.19
The strict requirements needed for bilayer formation make it unlikely that the amphiphilic compounds in meteorites or comets delivered to Earth could have contributed to the formation of the first protocell membranes. Formation of nonanoic acid bilayers (or bilayers comprised of any amphiphile with a single hydrocarbon chain) is as improbable as a river flowing up a mountain, since several “just right” conditions need to be met simultaneously. If a bilayer structure forms, minor environmental fluctuations or compositional changes would cause them to destabilize and revert to micelles––structures with no biological significance.
Critical Factors Weigh In
At some point in naturalistic origin-of-life scenarios, cell membranes composed of phospholipids must emerge. This fact applies whether the pathway leading to the first contemporary cell membranes began with primitive membranes comprised of simple amphiphiles, or whether the initial cell membranes appeared as phospholipid bilayers.
Once the first phospholipids appear, the spontaneous assembly of cell membrane systems does not necessarily occur. Bilayer-forming phospholipids display complex behavior aggregating into a wide range of bilayer structures (figure 6). Many phospholipids spontaneously form bilayers that stack into sheets (multilamellar bilayers) that are either linear or spherical in shape.20 (Spherical multibilayer structures resemble an onion.) These aggregates only superficially resemble the cell membrane’s structure, which consists of a single bilayer, not bilayer stacks.
Some phospholipids do form structures composed of a single bilayer under laboratory conditions but only when researcher intervention and manipulation take place. When coaxed to form, these single bilayer aggregates arrange into hollow spherical structures called liposomes or unilamellar vesicles.Liposomes exist for a limited lifetime. Their stability is only temporary. Liposomes fuse over time, reverting to multilamellar sheets or vesicles.21
How is it that cell membranes consist of a single bilayer when phospholipids form multiple-bilayer sheets or relatively unstable single-bilayer vesicles? During the 1980s and early 1990s National Institutes of Health (NIH) researcher Norman Gershfeld successfully addressed this question. He discovered that single bilayers, similar to those that constitute cell membranes, form and are stable, but only under a unique set of conditions.22 Chemists refer to phenomena that occur under a specialized set of conditions as critical phenomena. In other words, single bilayers are a critical phenomenon.
Formation of single-bilayer vesicles occurs only at a specific temperature called the critical temperature. Pure phospholipids spontaneously transform from either multiple-bilayer sheets or unstable liposomes into stable single bilayers at the critical temperature.23 The critical temperature is unique for each phospholipid and depends on the bilayer’s phospholipid composition.24
Gershfeld and his team discovered that the critical temperature carries important biological implications. For example, they noted that phospholipids extracted from rat and squid nervous system tissue only assemble into single-bilayer structures at critical temperatures that correspond to the physiological temperatures of these two respective organisms.25 Gershfeld’s group also observed that for the cold-blooded sea urchin, L. pictus, the cell membrane composition of its earliest embryonic cells varies in response to the environment’s temperature. This response works to maintain a single-bilayer phase with a critical temperature that matches the environmental conditions.26 The team noted that the bacterium E. coli also adjusted its cell membrane phospholipid composition in response to changes in the growth temperature to maintain a single-bilayer phase.27
These studies highlight the biological importance of the critical bilayer phenomena. So do other studies that describe the devastation life experiences when cell membranes deviate from critical conditions. For example, human red blood cells rupture (undergo hemolysis) when incubated above 37 ˚C (the normal human body temperature). Gershfeld’s team noted that when this happens, red blood cell membranes transform from a single bilayer to multibilayer stacks, losing the cell membrane’s critical state28—much as a natural boundary might disappear when a river dries up. Gershfeld and his collaborators have even provided some evidence that cell membrane defects at sites of neurodegeneration may play a role in Alzheimer’s disease.29 Again they noted that a collapse of the cell membrane’s single-bilayer state into multiple bilayers occurred in diseased tissue extracts as a result of an altered membrane phospholipid composition.
Gershfeld’s work indicates that cell membranes are highly fine-tuned molecular structures that depend on an exacting set of physical and chemical conditions. It seems unlikely that chemical and physical processes operating on early Earth could produce the precise phospholipid composition to form the stable single-bilayer phase that is universal for all cell membranes. Even if chance events arrived at this “just-right” phospholipid composition, any fluctuations in temperature or membrane composition would have destroyed the single-bilayer structure. With the loss of this structure, the first protocells would have been lost.
The criticality of cell membrane structure not only challenges natural process explanations for the cell membrane and, hence, natural process explanations for life’s beginnings, but also provides startling evidence that cell membranes are the result of an Intelligent Designer’s work. The problem of membrane formation for origin-of-life researchers now becomes similar to the problem these scientists face when trying to account for the development of information-containing molecules such as proteins and DNA. Though amino acids can assemble to form protein chains, only very specific amino acid sequences form functional protein molecules. Likewise, although phospholipids readily aggregate to form bilayer structures, only very precise phospholipid compositions and exacting environmental temperatures lead to the single-bilayer structures needed for cell membranes.
The emergence of cell membrane systems represents a necessary stage in life’s origin and the initial step towards forming the first protocells. Like a country or a state border, the cell membrane establishes a boundary—it delineates life from nonlife processes.
Within the evolutionary framework, most origin-of-life researchers suggest that the first protocell membranes readily assembled under the conditions of early Earth. These researchers assume the cell’s boundary formed through natural processes—just as the Piscataqua river formed, providing a natural border between Maine and New Hampshire.
Advances in membrane biophysics, however, challenge natural-process explanations for cell membrane origins. While a wide range of amphiphilic compounds that could serve as lipid components for primitive biological membranes self-assemble into bilayers, this self-assembly process requires “just right” conditions and “just right” molecular components. It is unlikely that such conditions would exist or persist for long time frames on early Earth.
In addition, the self-assembly of phospholipids, the dominant lipid component of contemporary cell membranes, requires specific concentrations, temperatures, and compositions. Deviation from these conditions leads to a loss of the cell membrane’s structural and functional integrity and has been implicated in disease processes.
The exacting conditions needed to self-assemble and maintain biological membranes make the conclusion that these structures could emerge by natural processes improbable. At the same time, the fine-tuning and singularity of conditions needed for cell membrane structure and function stand as hallmark characteristics of Intelligent Design—reasonable expectations if God is responsible for life.
The Fluid Mosaic Model
Since the early 1970s, the fluid mosaic model has provided the framework to understand membrane structure and function.1 This model views the phospholipid bilayer as a two-dimensional fluid that serves as both a cellular barrier and as a solvent for integral membrane proteins. The fluid mosaic model allows the membrane proteins and lipids to freely diffuse laterally throughout the cell membrane. Beyond the bilayer structure and asymmetry, the fluid mosaic model attributes no structural and functional organization to cell membranes.
In recent years, scientists have revised the fluid mosaic model.2 Instead of diffusing freely in the phospholipid bilayers, most proteins find themselves confined to domains within the membrane. Other proteins diffuse throughout the membrane, but instead of moving randomly, these proteins move in a directed fashion. Phospholipids, too, organize into domains with certain phospholipid classes laterally segregated in the bilayer. Bilayer fluidity also varies from region to region in the cell membrane.
- S. J. Singer and G. L. Nicolson, “The Fluid Mosaic Model of the Structure of Cell Membranes,” Science 175 (1972): 720-31.
- Ken Jacobson et al., “Revisiting the Fluid Mosaic Model of Membranes,” Science 268 (1995): 1441-42.
Cell Membrane Essentials1
Cell membranes are only 3.5 to 4 nanometers thick. (A nanometer is one-billionth of a meter.) In electron micrographs, cell membranes have a sandwich-like appearance (figure 1). Inner and outer membrane surfaces appear dark, whereas the membrane’s interior appears light.
Two classes of biomolecules interact to form cell membranes: lipids and proteins. Lipids, a structurally heterogeneous group of compounds, share water insolubility as a defining property. Additionally, lipids readily dissolve in organic solvents. Cholesterol, triglycerides, saturated and unsaturated fats, oils, and lecithin are examples of familiar lipids.
Phospholipids are the cell membrane’s major lipid component.2 Their molecular shape roughly resembles a distorted balloon with two ropes tied to it (figure 2). Biochemists divide phospholipids into two regions that possess markedly different physical properties. The head region, corresponding to the “balloon,” is soluble in water, or hydrophilic (“water-loving”). The phospholipid tails, corresponding to the “ropes” tied to the balloon, are insoluble in water, or hydrophobic (“water-hating”).
Chemists refer to molecules, such as phospholipids, that possess distinctly different solubility domains within them, as amphiphilic (“ambivalent in its likes”). The amphiphilicity of soap and detergents gives these compounds great economic importance.
Amphiphilicity also has great biological importance. Phospholipids’ “schizophrenic” solubility properties play the key role in cell membrane structure. When added to water, phospholipids spontaneously organize into sheets two molecules thick, called bilayers. The phospholipid “heads” align adjacent to one another, and the phospholipid “tails” pack together closely. These monolayers, in turn, come together so that the phospholipid tails of one monolayer contact the phospholipid tails of another monolayer. This tail-to-tail arrangement ensures that the water-soluble head groups make contact with water and the water-insoluble tails avoid water (figure 3).
Phospholipids possess a wide range of chemical variability (figure 2). Phospholipid head groups typically consist of a phosphate group bound to a glycerol (glycerin) backbone. The phosphate group, in turn, binds one of a number of possible compounds that vary in their chemical and physical properties. Phospholipids are identified by their head group substituents. For example, when choline binds to the phosphate group, biochemists refer to it as a phosphatidylcholine.
Phospholipids vary in tail length and structure. Phospholipid tails—typically long, linear hydrocarbon chains—also link to the glycerol backbone. The phospholipid hydrocarbon chains are commonly 16 to 18 carbon atoms long. Sometimes a permanent kink exists at some point along one or both hydrocarbon chains.
The precise mixture of the cell membrane’s phospholipids affects its physical, chemical, and consequently, biological properties. For example, cell membranes in which the phospholipids’ headgroups contain high levels of glycerol or serine are sensitive to calcium ions (Ca2+). Those composed of phospholipids with short hydrocarbon chains or kinked hydrocarbon chains possess a liquid-like interior. On the other hand, cell membranes formed from phospholipids having longer hydrocarbon chains without kinks have solid-like interiors.
Role of Proteins
Proteins comprise the other major class of biomolecules that play a role in cell membrane structure and function. The cellular machinery builds proteins by joining smaller subunit molecules, amino acids, in a head-to-tail manner.3 Cells use 20 different amino acids with variegated chemical and physical properties to form proteins. The amino acid chains that make up proteins adopt complex and precise three-dimensional structures. A protein’s three-dimensional structure determines its functional and/or structural role in the cell.
Proteins associate with the cell membrane in a variety of ways. Some, called peripheral proteins, bind to the inner or outer membrane surfaces. Others, called integral proteins, embed into the cell membrane. Some integral proteins embed only partially into the membrane interior, others penetrate nearly halfway into the membrane’s core, and still others span the entire membrane (see figure 4).
Membrane proteins operate in many different ways. Some proteins function as receptors, binding compounds that allow the cell to communicate with its external environment. Some catalyze chemical reactions at the cell’s interior and exterior surfaces. Some proteins shuttle molecules across the cell membrane. Others form pores and channels through the membrane. Some membrane proteins impart structural integrity to the cell membrane.
The cell membrane’s inner and outer monolayers differ in composition, structure, and function. For this reason, biochemists refer to cell membranes as asymmetric. The phospholipid classes on the inner and outer membrane surfaces differ; membrane proteins, likewise, are specific to either the inner or outer membrane surfaces. Proteins that span the cell membrane possess a specific orientation. Because of protein asymmetry, the functional characteristics of the inner and outer surfaces vary.
Cell membranes are highly complex, dynamically intricate biosystems, not just inert barriers. Their life-critical remarkable structural and functional organization suggests divine design. Any viable explanation for the cell membrane’s origin must account for these characteristics.
- Robert C. Bohinski, Modern Concepts in Biochemistry, 4th ed. (Boston: Allyn and Bacon, 1983), 243-53; Lubert Stryer, Biochemistry, 3d ed. (New York: W. H. Freeman, 1988), 283-312; Gary R. Jacobson and Milton H. Saier, Jr., “Biological Membranes: Structure and Assembly” in Biochemistry, ed. Geoffrey Zubay (Reading, MA: Addison-Wesley, 1983), 573-619.
- Some biological membranes also contain cholesterol and another class of lipids known as glycolipids. Glycolipids possess a sugar headgroup (that sometimes can be quite large) instead of a phosphate headgroup.
- Stryer, 15-42.
- Abiotic: non-living.
- Aggregate: a group of atoms or molecules held together in some way, for example, a micelle.
- Amphiphile: a molecule with a polar head attached to a long hydrophobic tail.
- Liposome: a vesicle composed of one or more concentric phospholipid bilayers and used medically.
- Micelle: a submicroscopic structure consisting of amphiphilic molecules. It occurs at a well-defined concentration known as the critical micelle concentration. The shapes of micelles can vary, but in a colloquial sense, they are generally considered as spherical structures.
- Multilamellar sheet: a sheet formed from layered stacks.
- Octanoic/nonanoic: Octanoic acid consists of a linear carbon chain eight carbon atoms in length, and nonanoic acid a linear carbon chain nine carbon atoms long.
- Phospholipid: any of a class of esters of phosphoric acid containing one or two molecules of fatty acid, an alcohol, and a nitrogenous base.
- Physicochemical: being physical and chemical.
- Soluble: capable of being dissolved. Insoluble: incapable of being dissolved.
- Vesicle: a small, thin-walled cavity, usually filled with fluid.
- Many origin-of-life researchers posit that single-bilayer membranes naturally self-assemble from amphiphiles.
- Advancing studies on cell membranes both challenge this aspect of evolutionary theory and offer evidence for design:
- The strict requirements needed for bilayer formation make it unlikely that compounds in meteorites or comets contributed to the formation of the first protocell membranes.
- Single bilayer formation is a critical phenomenon that requires “just right” conditions and “just right” molecular components. Such conditions would not likely exist or persist for long on early Earth.
- Complexity and fine-tuning of cell membrane structures imply design.
- Warren Richey, “Welcome to Maine. Or Is This Still New Hampshire?” Christian Science Monitor, 16 April 2001; “Supreme Court Settles Border Dispute,” USA Today, 29 May 2001.
- Robert C. Bohinski, Modern Concepts in Biochemistry, 4th ed. (Boston: Allyn and Bacon, 1983), 8-28.
- Geoffrey Zubay, Origins of Life on the Earth and in the Cosmos, 2d ed. (San Diego: Academic Press, 2000), 371.
- Zubay, 371-76.
- Zubay, 347-50; Arthur L. Weber, “Origin of Fatty Acid Synthesis: Thermodynamics and Kinetics of Reaction Pathways,” Journal of Molecular Evolution 32 (1991): 93-100; Ahmed I. Rushdi and Bernd R. T. Simoneit, “Lipid Formation by Aqueous Fischer-Tropsch Type Synthesis over a Temperature Range of 100 to 400 ˚C,” Origin of Life and Evolution of the Biosphere 31 (2001): 103-18; W. R. Hargreaves, S. Mulvihill, and D. W. Deamer, “Synthesis of Phospholipids and Membranes in Prebiotic Conditions,” Nature 266 (1977): 78-80; M. Rao et al., “Synthesis of Phosphatidylcholine Under Possible Primitive Earth Conditions,” Journal of Molecular Evolution 18 (1982): 196-202; M. Rao et al., “Synthesis of Phosphatidyethanolamine Under Possible Primitive Earth Conditions,” Journal of Molecular Evolution 25 (1987): 1-6.
- Stanley L. Miller and Jeffrey I. Bada, “Submarine Hot Springs and the Origin of Life,” Nature 334 (1998): 609-11; Nils G. Holm and Eva M. Andersson, “Hydrothermal Systems,” in The Molecular Origins of Life: Assembling Pieces of the Puzzle, André Brock, ed. (Cambridge: Cambridge University Press, 1998), 86-99; Charles B. Thaxton, Walter L. Bradley, and Roger L. Olsen, The Mystery of Life’s Origin: Reassessing Current Theories (Dallas: Lewis and Stanley, 1984), 56, 177-78.
- David W. Deamer, Elizabeth Harany Mahon, and Giovanni Bosco, “Self-Assembling and Function of Primitive Membrane Structures” in Early Life on Earth: Nobel Symposium No. 84, Stefan Bengtson, ed. (New York: Columbia University Press, 1994), 107-23; D. W. Deamer, “Membrane Compartments in Prebiotic Evolution,” in The Molecular Origins of Life: Assembling the Pieces of the Puzzle, André Brock, ed. (Cambridge: Cambridge University Press, 1998), 189-205.
- John R. Cronin, “Clues from the Origin of the Solar System: Meteorites,” in The Molecular Origin of Life: Assembling Pieces of the Puzzle, André Brock, ed. (Cambridge: Cambridge University Press, 1998), 119-46.
- Jason P. Dworkin et al., “Self-Assembling Amphiphilic Molecules: Synthesis in Simulated Interstellar/Precometary Ices,” The Proceedings of the National Academy of Sciences, USA 98 (2001): 815-19; R. Cowen, “Life’s Housing May Come from Space,” Science News 159 (2001), 68.
- J. N. Israelachvili et al., “Physical Principles of Membrane Organization,” Quarterly Review of Biophysics 13 (1980): 121-200.
- William R. Hargreaves and David W. Deamer, “Liposomes from Ionic, Single-Chain Amphiphiles,” Biochemistry 17 (1978): 3759-68.
- Deamer, Mahon, and Bosco, 107-23; D. W. Deamer 189-205; D. W. Deamer and R. M. Pashley, “Amphiphilic Components of the Murchinson Carbonaceous Chondrite: Surface Properties and Membrane Formation,” Origins of Life and Evolution of the Biosphere 19 (1989): 21-38; David W. Deamer, “Boundary Structures Are Formed by Organic Components of the Murchinson Carbonaceous Chondrite,” Nature 317 (1985): 792-94.
- Dworkin, 815-19.
- J. G. Lawless and G. U. Yuen, “Quantitation of Monocarbonoxylic Acids in the Murchinson Carbonaceous Meteorite,” Nature 282 (1979): 396-98.
- Deamer, Mahon, and Bosco, 107-23; Deamer: 189-205.
- Deamer, Mahon, and Bosco, 107-23; Deamer: 189-205.
- Deamer: 792-94.
- Hargreaves and Deamer, 3759-68.
- Charles L. Apel et al., “Self-Assembled Vesicles of Monocarboxylic Acids and Alcohols: Conditions for Stability and for the Encapsulation of Biopolymers,” Biochimica et Biophysica Acta (2001), in press.
- Danilo D. Lasic, “The Mechanism of Vesicle Formation,” Biochemical Journal 256 (1988): 1-11.
- For example, see Barry L. Lentz et al., “Spontaneous Fusion of Phosphatidylcholine Small Unilamellar Vesicles in the Fluid Phase,” Biochemistry 26 (1987): 5389-97.
- N. L. Gershfeld, “The Critical Unilamellar Lipid State: A Perspective for Membrane Bilayer Assembly,” Biochimica et Biophysica Acta 988 (1989): 335-50.
- For example see, Norman L. Gershfeld et al., “Critical Temperature for Unilamellar Vesicle Formation in Dimyristoylphosphatidylcholine Dispersions from Specific Heart Measurements,” Biophysical Journal 65 (1993): 1174-79.
- N. L. Gershfeld, “Spontaneous Assembly of a Phospholipid Bilayer as a Critical Phenomenon: Influence of Temperature, Composition, and Physical State,” Journal of Physical Chemistry 93 (1989): 5256-64.
- Lionel Ginsberg et al., “Membrane Bilayer Assembly in Neural Tissue of Rat and Squid as a Critical Phenomena: Influence of Temperature and Membrane Proteins,” Journal of Membrane Biology 119 (1991): 65-73.
- K. E. Tremper and N. L. Gershfeld, “Temperature Dependence of Membrane Lipid Composition in Early Blastula Embryos of Lytechinus pictus: Selective Sorting of Phospholipids into Nascent Plasma Membranes,” Journal of Membrane Biology 171 (1999): 47-53.
- A. J. Jin et al., “A Singular State of Membrane Lipids at Cell Growth Temperatures,” Biochemistry 38 (1999): 13275-78.
- N. L. Gershfeld and M. Murayama, “Thermal Instability of Red Blood Cell Membrane Bilayers: Temperature Dependence of Hemolysis,” Journal of Membrane Biology 101 (1988): 67-72.
- Lionel Ginsberg et al., “Membrane Instability, Plasmalogen Content and Alzheimer’s Disease,” Journal of Neurochemistry 70 (1998): 2533-38.