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The Architecture of Life

A universal set of building rules seems to guide
the design of organic structures—from simple
carbon compounds to complex cells and tissues
by Donald E. Ingber

L ife is the ultimate example of complexity at work. An
organism, whether it is a bacterium or a baboon, de-
velops through an incredibly complex series of in-
teractions involving a vast number of different components.
These components, or subsystems, are themselves made up
of smaller molecular components, which independently ex-
hibit their own dynamic behavior, such as the ability to cat-
alyze chemical reactions. Yet when they are combined into
some larger functioning unit—such as a cell or tissue—utterly
new and unpredictable properties emerge, including the abil-
ity to move, to change shape and to grow.
Although researchers have recognized this intriguing fact
for some time, most discount it in their quest to explain life’s
fundamentals. For the past several decades, biologists have
attempted to advance our understanding of how the human
body works by defining the properties of life’s critical materi-
als and molecules, such as DNA, the stuff of genes. Indeed,
biologists are now striving to identify every gene in the com-
plete set, known as the genome, that every human being car-
ries. Because genes are the “blueprints” for the key molecules
of life, such as proteins, this Holy Grail of molecular biology
will lead in the near future to a catalogue of essentially all the
molecules from which a human is created. Understanding
what the parts of a complex machine are made of, however,
does little to explain how the whole system works, regardless
of whether the complex system is a combustion engine or a organelles, which self-assem-
cell. In other words, identifying and describing the molecular ble into cells, which self-assemble
puzzle pieces will do little if we do not understand the rules into tissues, which self-assemble into
for their assembly. organs. The result is a body organized hierar-
That nature applies common assembly rules is implied by chically as tiers of systems within systems. Thus, if
the recurrence—at scales from the molecular to the macro- we are to understand fully the way living creatures form
scopic—of certain patterns, such as spirals, pentagons and and function, we need to uncover these basic principles
triangulated forms. These patterns appear in structures rang- that guide biological organization.
ing from highly regular crystals to relatively irregular proteins Despite centuries of study, researchers still know relatively
and in organisms as diverse as viruses, plankton and hu- little about the forces that guide atoms to self-assemble into
mans. After all, both organic and inorganic matter are made molecules. They know even less about how groups of mole-
of the same building blocks: atoms of carbon, hydrogen, oxy- cules join together to create living cells and tissues. Over the
gen, nitrogen and phosphorus. The only difference is how past two decades, however, I have discovered and explored
the atoms are arranged in three-dimensional space. an intriguing and seemingly fundamental aspect of self-as-
This phenomenon, in which components join together to sembly. An astoundingly wide variety of natural systems, in-
form larger, stable structures having new properties that could cluding carbon atoms, water molecules, proteins, viruses,
not have been predicted from the characteristics of their indi- cells, tissues and even humans and other living creatures, are
vidual parts, is known as self-assembly. It is observed at constructed using a common form of architecture known as
many scales in nature. In the human body, for example, large tensegrity. The term refers to a system that stabilizes itself
molecules self-assemble into cellular components known as mechanically because of the way in which tensional and

48 Scientific American January 1998 Copyright 1997 Scientific American, Inc.

individual members but because of the way the entire struc- This fundamental finding could one day have practical ap. engineering—of the rapidly accumulating data we have about The other category of tensegrity structures encompasses molecules. all the structural mem- bers are already in tension or compression—that is. Copyright 1997 Scientific American. bers throughout the structure—even ones on the opposite TENSEGRITY—an architectural system in which KATE NOBES AND ALAN HALL (background ) structures stabilize themselves by balancing the counteracting forces of compression and tension— gives shape and strength to both natural and artifi- KENNETH SNELSON (foreground). which tensegrity at the cellular level has allowed us to comprehend includes the geodesic domes of Buckminster Fuller. new understanding of tures fall into two categories. An expla. At the same time. Inc. the flexible. The struts that make up the frame- the activities of genes. it is the maintenance of feature.compressive forces are distributed and balanced within the tures are mechanically stable not because of the strength of structure. all structural members. The mol. those that stabilize themselves through a phenomenon known nation of why tensegrity is so ubiquitous in nature may also as prestress. which equilibrate throughout the with chemical composition than with architecture. There my studies of cell biology and also of sculpture led me to realize prestressed. or tense. cial forms. Within the structure. tension-bearing members. structural members that can bear only tension are distinct from those that bear compression. ecules and cells that form our tissues are continually removed Tensegrity structures of both categories share one critical and replaced. the compression-bearing rigid struts stretch. an increase in tension soned. pentagons or hexagons. The struc- plications in many areas. which is that tension is continuously transmitted across pattern and architecture. thereby assuring the stability of the whole structure. The cytoskeleton of a living cell (back- ground) is a framework composed of interconnect- ed microtubules and filaments. while those tension-bearing members compress the rigid struts. in which long struts are joined with cables. In other words. they are M y interest in tensegrity dates back to my undergraduate years in the mid-1970s at Yale University. that we call life. This type of structure was first constructed by provide new insight into the very forces that drive biological the sculptor Kenneth Snelson. Structures in one category. structure. cells and other biological components. are what enable it to stabilize itself. I rea. Even before one of these struc- What Is Tensegrity? tures is subjected to an external force. In Snelson’s elegant sculptures. work are connected into triangles. The dynamic re- lation of these structural elements is reminiscent of a sculpture (at center) by Kenneth Snelson. organization—and perhaps into evolution itself. each of which can bear pressure in blood vessels or compression in bone—influence tension or compression. and ing of natural rules of self-assembly will allow us to make each strut is oriented so as to constrain each joint to a fixed better use—in applications ranging from drug design to tissue position. deeper understand. that the question of how living things form has less to do These counteracting forces. ture distributes and balances mechanical stresses. Scientific American January 1998 49 . are basical- better how cellular shape and mechanical forces—such as ly frameworks made up of rigid struts. For example. in one of the members results in increased tension in mem- Tensegrity struc.

and string. side. biologists generally viewed the cell as a viscous fluid or gel surrounded by a membrane. 50 Scientific American January 1998 Copyright 1997 Scientific American. . as such a structure. three-di- mensional form. In contrast. roughly spherical shape. Each pair was perpendicular to tioned to best withstand stress. structure could easily explain such behavior. and none of the wood struts actually touched structures offer a maximum amount of strength for a given one another. however. Inc. But their role in controlling cell shape was poorly understood. My own interest substrate of glass or plastic by stretching a piece of cloth taut lies in between these two extremes. behave when placed on a surface. the underlying rubber. at the cellular level. and muscles. bones are the com. representing the nucleus. pulling them into a stable. HARRIS. I affixed the As a graduate student working with James D. the structure stabilizes itself through a rigid glass or plastic culture dish. For this reason. known as mi- crofilaments. Then. in the complex I built forces it into what appears to be a flattened pile of sticks tensegrity structure inside every one of us. the energy pression struts. It had been long in compression within certain members spaced throughout the known that cells spread out and flatten when they attach to a structure. and pinning it firmly to a piece of wood below. I also placed a smaller. mechanism that Fuller described as continuous tension and lo. Tensional forces naturally trans. Cells were known to contain an internal framework. In 1980. tendons and ligaments are the stored in the tensed filaments causes the model to spring back tension-bearing members. within the larger one that represented the rest of the cell. In other words. I stretched elastic strings from the surface of the large tensegrity structure to the smaller one inside [see illustration at top right 206 bones that constitute our skeleton are pulled up against on opposite page]. the force of gravity and stabilized in a vertical form by the pull To understand how my experiment worked. elastic string. I arranged the dowels—which bore the com- so the members of a tensegrity structure are precisely posi. in the late 1970s. At the macroscopic level. showed that when affixed to a flexible rubber substrate. I modeled a cell tion. ends of all the dowels. to mimic cytoskeletal W hat does tensegrity have to do with the human body? The principles of tensegrity apply at essentially every detectable size scale in the body. I mimicked a solid culture selves through the principles of tensegrity. I focused on how the components of biological sys- ALBERT K. At this time. Another mystery in those days concerned the way isolated LIVING CELLS crinkle a thin rubber substrate be- cause they exert tractional forces where they adhere. it consisted of six wood dowels and some mit themselves over the shortest distance between two points. cells ty from continuous compression because of the force of gravity. tensegrity the other two. intermediate filaments and microtubules. contract and become more spherical. tendons and ligaments (similar to the ca. Jamieson at Yale. PATRICIA WILD AND DAVID STOPAK tems—especially of cells—interacted mechanically. or puckers. pressive stress—in three pairs. pro. to its original. To simulate how cells teins and other key molecules in the body also stabilize them. by defini. or cytoskeleton. to know that pushing down on a tensegrity model of the kind bles in Snelson’s sculptures). most buildings derive their stabili. arranged geodesically). it is necessary of tensile muscles. composed of three different types of molecular protein polymers. As soon as the pressure is removed. In this way. This global increase in tension is balanced by an increase cells behave when placed on different surfaces. Fuller’s domes or Snelson’s sculptures—map out the shortest It occurred to me that a view of the cell as a tensegrity paths between adjacent members (and are therefore. the connections between the nucleus and the rest of the cell. At the other end of the scale. much like a balloon filled with molasses. Santa Barbara amount of building materials. Albert K.GEODESIC DOME carries a given load with a minimum ©ALLEGRA FULLER SNYDER Buckminster Fuller Institute. This contraction bunch- The tension-bearing members in these structures—whether es up. A tension-bearing elastic string connected to the amount of building material. spherical tensegrity From Skeleton to Cytoskeleton model. Harris of the University of North Carolina at Chapel Hill cal compression.

In addition. puckering that surface (right). the cytoskeleton. the model re- mained flat. the tensegrity model popped up into its more spherical form. Opposing this inward pull are two main types of I n the years since my modeling experiment. I showed that tensegrity structures mimic the known behavior of living cells. and nuclei spread and polarize in a similar manner when they adhere to a substrate. one of which is outside the cell and the other inside. biologists have learned a great deal about the mechanical aspects of cells. The third component of ton’s three major types of filaments but also from the extra. INGBER DONALD E. it pulls the cell’s Hard-Wiring in Cells membrane and all its internal constituents toward the nucleus at the core. thereby mak- ing the cell’s anchoring surface flexible. filaments within the cytoskeleton. just as a real cell does on a hard substrate. puckering the cloth TENSEGRITY MODEL of a cell underneath. With the dowel ends sewed to the tightly pinned cloth. now known as integrins or adhesion re- ceptors. stiff- CYTOSKELETON of a cell consists of microfilaments CELL SURFACE (bottom left). exerting tension. Soon thereafter. INGBER These attachments were analogous to the cell-surface molecules. just as the models predict. Thus. with my highly simplified construction. however. the cell and Like a living cell. Furthermore. a gossamer network of contractile micro. INGBER ROBERT D. they act as guy wires. Inc. The molecular structure of each CYTOSKELETON component is shown above the corresponding photo- graph and is color coded to the top left illustration. it flattens itself and its nu- nucleus inside it extended in a coordinated manner. INGBER three components interconnect to create the cytoskele- tal lattice. The nu. the compressive “girders” inside the cell can be ei- their shape from tensegrity. Further. NUCLEUS tensegrity model to the substrate by flattening it and sewing the ends of some of the dowels to the cloth. the intermediate filaments. microtubules (bottom center) and inter- mediate filaments (bottom right). The component outside the cell is the extracellu- lar matrix. SLIM FILMS. all of which are RYOTA MATSUURA. . filaments to one another as well as to the surface membrane Inside the cell. connecting microtubules and contractile micro- naturally secured in the body. GOLDMAN Northwestern University Medical School Copyright 1997 Scientific American. The AND DONALD E. filaments—a key element of the cytoskeleton—extends through- out the cell. cleus when it attaches to a rigid surface (left) and cleus model also moved toward the bottom of the simulated retracts into a more spherical shape on a flexible sub- cell. ther microtubules or large bundles of cross-linked micro- most cells derive their structure not only from the cytoskele. are the great in- cellular matrix—the anchoring scaffolding to which cells are tegrators. SOURCE: DONALD E. I showed experimentally that living cells strate. and the cell’s nucleus. which stretches from the cell surface to the nucleus (top left). I noticed that when I stretched the was built with dowels and elastic cords. and their findings seem to confirm that cells do indeed get compressive elements. ROBERT EZZELL NUCLEUS nanometers wide. The rounded shape near the center in each of these photographs is the cell nucleus. In other words. When I lifted the pins to free the cloth from the wood. that physically connect a cell to its anchoring substrate. MICROFILAMENTS MICROTUBULES INTERMEDIATE FILAMENTS LAURIE GRACE DONALD E. model flat by connecting it to the cloth substrate.

themselves in a tissue-specific searchers discovered that microtubule assembly (elongation)— manner: capillary cells formed and. By simply modifying the shape of the cell. compressing them neurite extends (bottom). however. it is this hard-wired network of molecular ical forces transmitted across the cell surface. Andrew Matus of the Friedrich Miescher In. and so on. demonstrated this directly. BEAT LUDIN AND ANDREW MATUS crotubules and transmit electrical signals in the nervous sys. with their cytoskeletons of the cell’s skeleton. working with Harish Joshi and Robert E. In other words. important because many of the enzymes and other substances If the cell and nucleus are physically connected by tensile that control protein synthesis. Rahul Singhvi and pipettes to adhesion receptors on the surface of living cells and Christopher S. This finding is struts and cables that stabilizes cell shape. GROWING MICROTUBULE buck- mechanics and biochemistry at the molecular level. as my early experiments suggested. ical School. they could switch T ensegrity can be invoked to explain more than the stabi- lization of cellular and nuclear form. Recently Andrew Maniotis. they Heidemann’s group found that microtubules are com. Thus. cells were neither too extend- tem. cells between different genetic programs. By mak. adhesive “islands” composed of extra- cellular matrix. This growth is required for repair of nerve damage. Although The tensegrity model suggests that the structure of the cell’s the cytoskeleton is surrounded by membranes and penetrated cytoskeleton can be changed by altering the balance of phys- by viscous fluid. Steven R. hence. points where the cell anchors to its underlying substrate (center). they enable the microtubules to elongate. They forced living cells to take on of pull. Chen in my group. changing cytoskeletal geometry and mechanics tural changes deep inside the cell. called neurites. adhesions. the existence liver normally supplies to the of a tensegrity force balance provides a means to integrate blood. CELL BODY NEURITE PETIT FORMAT/SCIENCE SOURCE LAURIE GRACE NERVE CELL has long extensions. electrically with neighboring nerve cells (above left and top are connected to other ones (orange) that extend forward to the right). and the filaments (red) surround the microtubules. Thus. The same microfilaments. By binding micro. the re. could affect biochemical reactions and even alter the genes who was in my group at Children’s Hospital of Harvard Med. for exam. . To investigate this possibility further. cells secreted proteins that the ments to its extracellular matrix. neurite extension—is promoted by shifting com. developed a method to engineer structures in the nucleus to realign immediately in the direction cell shape and function. For example. by elongating internal molec. Matus actually cell what to do. hollow capillary tubes. For this reason. ed nor too retracted. 52 Scientific American January 1998 The Architecture of Life Copyright 1997 Scientific American. Heidemann.les under compression in these time- Very recently. Cells that spread flat became more likely to divide. different shapes—spherical or flattened. neither divided nor died. When STEFANIE KAECH. that connect and restricting their growth. liver pressive loads off the microtubule and onto the cell’s attach. cells and nu. also at Harvard. then pulling on in the cell are physically immobilized on the cytoskeleton. Inc. during the repair of an injury. Contractile micro. ple. turing of the cell and cyto. ening the central nucleus and securing it in place. placing them on tiny. Very flat cells. skeleton apparently tells the curs when the microtubule elongates ing cells that produce fluorescent microtubules. prevented from spreading found that tensegrity can explain how nerve cells extend activated a death program long. Neurites extend from the cell (views at right). thin projections called neurites. mechanical restruc. known as apoptosis. Maniotis caused cytoskeletal filaments and Whitesides. that are activated and thus the proteins that are made. which are filled with mi. pulling outward. and pushes against other components viewed those microtubules buckling under compression. working with George M. energy conversion and growth filaments and not solely by a fluid cytoplasm. receptors at the cell surface should produce immediate struc.lapse video images. The buckling oc- stitute in Basel added a vivid footnote to this story. More important. When the microfilaments pull themselves forward against these ular fibers known as microtubules (purple). whereas round cells that were Buxbaum of Michigan State University in the mid-1980s. Each adhesive island was surrounded by a How Mechanics Controls Biochemistry Teflon-like surface to which cells could not adhere. round or square—by clei do not behave like viscous water balloons. In- pressed at their ends by the pull of surrounding contractile stead they differentiated microfilaments inside the neurites.

Essentially. in turn. sense that more cells are needed to cover the sur. yet until we examined this phenomenon in the to cell-surface receptors involved with metabolism—rather context of tensegrity. one disparity needed explaining. the lin- ear-stiffening response of tissues. such as DNA. A lthough the tensegrity models predicted many cell behav- iors. tural members reorient ating too much. are transmitted over specific molecular paths in living cells. SOURCE: DONALD E. Furthermore. themselves to lie more in the direction of ap- In between these two extremes. we found that applying stress ear stiffening. that the gist of the response can be discerned from the way ply? Again using an uncomplicated modeling approach. cropipette-pulling experiments. using a stick-and-string tensegrity mod. We found that when we increased of phenomena. for example. Inc. Recent studies In Wang’s magnetic-twisting studies and in Maniotis’s mi- show that even isolated molecules. nal force is met with increasing resistance. such as large bundles or networks of triangles. stretched. SLIM FILMS. the members come to lie in the direction of the applied stress. developed a finding that provided new insight into how cells sense me- device that allowed us to twist individual molecules on the chanical stimuli that regulate tissue development. If you pull on your skin. Working with Dimitrije Stamenovic of Boston Making Cells Do the Twist University. the tension in con- tractile microfilaments. than adhesion—did not effectively convey force to the inside ical explanation for this behavior. contractile microfilaments ening results because as the applied stress increases. you will feel may also be incorporated within computer programs as a the resistance increase as you tug harder. exhibit lin. cell’s membrane and link the extracellular matrix to the inter- nal cytoskeleton). the cells responded by becoming stiffer and Molecular Geodesic Domes stiffer—just as whole tissues do. for the first time. cartilage. It predicts. I in which tensegrity structures respond to stress. sight. In the cytoskeleton of a living cell. that may be useful in such applications as protective clothing blood vessels and skin. from the growth of muscle in response to ten- the stress applied to integrins (molecules that go through the sion to the growth of plant roots in response to gravity. Understanding how this switching in the right-hand view). Rounding indicates that too many cells are structure because struc- competing for space on the matrix and that cells are prolifer. which are created from the joining of cells to one another and to their extracellular matrix. all found that. To explore the SODA-STRAW MODEL (below) with flexible joints shows how contracting microfilament net- works can rearrange into linear bundles (top right) or triangulated geodesic forms. occurs in a tensegrity sion is needed. shortcut to accelerate molecular modeling and drug design. This in- surface membrane of living cells while simultaneously measur. Thus. a Butler of the Harvard School of Public Health. Many different types of tissue. One based on these principles. may help us better understand a wide variety ing the cellular response. for example. If living cells can change from known. INGBER Copyright 1997 Scientific American. vanced materials that have the linear-stiffening property and ly. incredibly. INGBER tissue repair and perhaps even to the creation of artificial-tis- sue replacements. Many cells can spread and flatten without microtubules—the most important Although the exact details of the interaction are not all compression struts in the model. including muscle. normal tissue function is es- plied stress (downward tablished and maintained. LINEAR STIFFENING rounding substrate—as in wound repair—and that cell divi. exhibit a response known as linear and artificial body parts. living cells could be made stiff or flexible by varying the prestress in the cytoskeleton by changing. spherical to flat without these struts. occurs could lead to new approaches to cancer therapy and DONALD E. Linear stiff. some must die to prevent tumor formation. such as the octa- hedron (bottom right). we showed. We hope to use this model to help design ad- emergent property of tissues is how they behave mechanical. living cells and even molecules. the microfilament network itself is a the interconnected structural elements of a tensegrity model tensegrity structure. working with James P. . there was no mechanical or mathemat. The same mathematical approach stiffening. of the cell. rearrange themselves in response to a local stress. how can tensegrity ap- el. we developed a mathematical model T he next level up in the hierarchy of self-assembly is the formation of tissues. more of form a lattice that reorganizes locally into different forms. these studies confirmed that mechanical forces In 1993 my co-worker Ning Wang. An increasing exter.

at many different size scales. GEODESIC FORMS appear in many dif- filament lattice as a polyhedral framework of soda straws ferent natural structures. the existence of a these focal-adhesion sites where integrin receptors anchor the geodesic dome within the cytoskeleton at the molecular level cell to the matrix. observed these very ual contractile microfilaments that formed the squares in the transformations in the region of the cytoplasm above the nu- model to self-assemble into linear bundles stretching between cleus in spreading cells. the internal elastic thread in the model would then framework of squares and triangles converts mimic the continuous tension in the whole structure that re. the cytoskeleton of a mammalian cell tration on preceding page]. organelles. unattached (suspended) cell. thereby transforming it as focal adhesions. an adenovirus (top middle) a single elastic string that I threaded through all the straws and (clockwise from bottom right) a pollen and tied to itself. SPL Photo Researchers. Contractile microfilaments respond to an. chorage by shortening and increasing isometric tension within Elias Lazarides. Inc. into fully tri- I assumed that this soda-straw model represented one mod. into a highly triangulated dome—specifically. In fact. in other words. rather they are “spot welded” in localized sites known work down over the spherical nucleus. Cells attach by binding to surface-bound molecules in the a cell. Inc KATE NOBES AND ALAN HALL mechanism behind this reorganization. Germany. I modeled the micro. demonstrates conclusively that cells can and do use the archi- individual contractile microfilaments align in a nearly identi. when living cells spread on a surface. But cells are not evenly “glued” to the that interconnect with the cell base would bend this frame- matrix. Inc. along with he called a “jitterbug” transformation: the highly flexible viruses. I found that the individual mod- The question I was trying to answer was. cells and even small organisms. including part of that contained six triangles and four squares [see bottom illus. straw models. multicellular organism known as a volvox. a buckyball surrounding a potassi- um ion. Planck Institute in Göttingen. Fuller showed many years ago that inward pulling and twist- T he geodesic structure found within the cytoskeleton is a classic example of a pattern that is found everywhere in nature. ular cytoskeletal unit that interconnected in all directions with When I interconnected many similar soda- other similar modules in a round. 54 Scientific American January 1998 The Architecture of Life Copyright 1997 Scientific American. a geodesic dome. dral forms—or. In KEN EWARD BioGrafx/Science Source/Photo Researchers. tecture of tensegrity to shape their cytoskeleton. It is known that contractile microfilaments get stiffer when they shorten. A Universal Pattern strate to resist the pull of the shortening microfilaments. angulated tensegrity structures. FRANCIS LEROY Biocosmos/ . In contrast. then at Cold Spring Harbor Laboratory in the lattice. The soda-straw models suggested that the increas. cal manner to form bundles called stress fibers. What would happen ules progressively contracted. erate mechanical tension by shortening itself. at the top of the cell. a protein enzyme complex and a represented a single contractile microfilament that could gen. contraction of surrounding microfilament networks extracellular matrix. there is no adhesive sub. The straws were held together by (above left). Spherical groups of carbon ing causes this type of polyhedral structure to undergo what atoms called buckminsterfullerenes or buckyballs. resulting in the forma- to this framework if the cell it supported were to attach to a tion of a geodesic framework composed of alternat- rigid surface? ing octahedral and tetrahedral forms. enzymes. Thus. . into fully triangulated octahedral or tetrahe- sults from the shortening of all these stiffened filaments. In these regions the contraction of each microfilament can be re- sisted only by the pull and stiffness of its neighboring filaments. closely packed. Significantly. and Mary Osborn and Klaus Weber of the Max ing tension produced by attachment would cause the individ. I assumed that each soda straw in the model grain. New York.

Strangely. that do not exhibit geodesic forms. ABBEY Photo Researchers. Inc. involves binding interactions between many similar balls. 60 carbon atoms form a geodesic sphere covered by 20 CHRIS HERIC. soccer ball. linear extensions of the pro. Protein organization also involves hierarchical assembly. these helical regions stabilize themselves through tensegrity—as does any heli- cal molecule. proteins that come together to form a geodesic viral coat that hexagons interspersed with 12 pentagons: the pattern on a encloses the genetic materi. Each tern is visual evidence of the existence of common rules for joint in this framework self-stabilizes as a result of a balance SOURCE: Journal of Biological Chemistry (below) self-assembly. through tensegrity. all exhibit geodesic forms. The small re- gions of a protein that are helically stiffened are separated from one an- other by parts of the same amino acid DAVID SCHARF Copyright 1997 Scientific American. In effect. catalysis and many other functions. or compression. Proteins. In bucky- earth. In other words. except The assembly of viruses. In particular. My view is that this recurrent pat. gulated geodesic framework on the nanometer scale. few researchers seem to tails that extend from neighboring proteins to form a trian- have asked why this is so. are long strings of amino acids. such as DNA. Inc. Small regions of the protein’s amino acid backbone fold into helical forms that stabilize them- selves through a balance between the attractive force of hydrogen bonds (pulling together different regions of the molecule) and the ability of the protein coil to resist shortening. between the pull of intermolecular attractive forces (hydro- selves in three dimensions in a similar way: by arranging gen bonds) and the ability of the individual protein tails to re- their parts to minimize energy and mass through continuous sist compression and buckling. tension and local compression—that is. the smallest form of life on the that the building blocks are atoms instead of proteins. ball are the struts in a tensegrity sphere. however. M. . During virus formation. It is more difficult. The same basic scheme is apparent in buckyballs. including many bio- logical molecules. all these entities stabilize them. to see that the same building teins overlap with similar rules also apply to irregular structures. on which cells depend for structure. the 90 carbon-carbon bonds in a bucky- al.

strength using a minimum of materials. These strut. tensegrity is clearly na.” backbone that act as if they were flexible hinges. enzymes tensegrity structure. The stiffened helices may be extremely compressed locally. At the Johns Hopkins School of and tension. sonous gas. teins and trigger a cascade of molecular an explosive metal. this character- tensegrity. and chlorine. Only three-dimensional space. SCHUTT (right) bones and muscles and tendons of the which a structure shapes itself and human body. It is plain how all these phenomena are so crofilament (above) derive strength from possible that fully triangulated tensegri- perfectly coordinated in a living crea. . Indeed. regardless and the interconnected molecules that of scale or position. given these form the internal framework of the cell constraints. Thus. These conformational changes. The im- Thus.The flexibility exhibited by prestressed ic oscillators. in membrane and into a cell.and molecular model of a cytoskeletal mi. to couple. genes are a product of evolution. For example.eye (background at right). CLARENCE E. PRESTRESSED TENSEGRITY CANTILEVERS filaments. VERTICAL TENSEGRITY sculpture the molecular scale. even though forces are equilibrated across the whole prestressed molecule.the same principle: they stabilize them. Very simply. holds its subcomponents together in ture’s preferred building system. sodium. at the same time. all matter is subject to lular matrix extends. at the macroscopic Remarkably. structures function as coupled harmon. The relevant question is. the attach. for example. Coffey and Ken. Even water their relative positions throughout the molecules are structured geodesically. Donald S. the whole system mechanically as one. geodesic forms similar to those found in viruses. like regions fold back on themselves (because of tensile hy- drogen-bonding forces) in order to stabilize the entire Implications for Evolution and Beyond molecule.scale and at all scales in between. whose emergent property is changes in their environment. terms of how emergent properties arise. or “tune. tensegrity may even ex. not its driving force.JIM AND JULIE BRUTON Photo Researchers. from the molecules to the portant principle here is the manner in KENNETH SNELSON (left). nuclei. ganelles or cells into tissues is not very ceptor. your skin stretches. the same spatial constraints. membrane ion channels and entire living cells and include the muscle-and-bone neck of a giraffe and a tissues exhibit characteristic resonant frequencies of vibra- cable-and-beam sculpture by Kenneth Snelson.tural efficiency—their high mechanical neth J. How did or- when a signal-bearing molecule binds ganic molecules and cells evolve from to a receptor that goes through the inorganic components? After all. that it can be used as table salt. In the surface tissue of a fly’s through evolution because of their struc- Medicine. transmission of tension through a tensegrity array provides a means to distribute forces to all intercon- nected elements and. a poi- restructuring inside that cell. arm. your cells distort. cytoskeletal uous tension and local compression. length of the protein. More broadly. For example. different from the self-assembly of atoms in turn. In Because a local force can change the shape of an entire fact.pose—to provide stability through contin. tion. into compounds. combine to form sodium this is how cells sense and respond to chloride. alter the shape of adjacent pro. your extracel. DNA. Pienta found that tensegrity ranged geodesically for the same pur. stiffened helical regions to rearrange als long before DNA ever came into existence. the binding of a molecule to a protein and cells existed in the inorganic world of crystals and miner- can cause the different. tensegrity is the most eco- feel the pull—all without any breakage nomical and efficient way to build—at or discontinuity. can explain istic is what defines the way the struc- how every time that you move your ture as a whole will behave. Inc. A lthough changes in DNA generate biological diversity. tensegrity structures would be advanta- 56 Scientific American January 1998 The Architecture of Life Copyright 1997 Scientific American. Inc. ment can cause conformational self-assembly of molecules into or- changes at the opposite end of the re. cells are ar.ty structures may have been selected selves through a balance of compression ture.

clay is that geodesic forms. Ingber in Science.Phil. The emergence of DNA and genes gave rise to a new For example. in turn. M. March 1993. KENNETH SNELSON geous because it allows structures to take on different shapes. 1997. and Ph. No. more philosophical questions arise: Are these hedra and tetrahedra are not closely packed. Revised edition. pages 103–138. Donald L. rather than in the primordial sea. 1986. As suggested combination and progressive remodeling of different organs. D’Arcy W. different molecular collectives self-assembled to 1923. Inc. pages sachusetts Institute of Technology. in octahedral and tetrahedral forms. In addi. 1997. itself a porous network of atoms arranged geodesically with. James P. McCABE Cambridge. if a molecule or cell were able to transform into mechanism for generating structural diversity that accelerated a shape that was more stable at a certain temperature or evolution. a Huang. Vol. These cells then tension. Organs developed from the sive forces locally can only lead us to wonder. they retain the building principles universal? Do they apply to structures ability to move and slide relative to one another. Then. similar entities and then to self-assemble bones and muscles is remarkably similar in Tyrannosaurus once again. 32. pages 1124–1127. Cytoskeleton. Thompson. or more efficient metabolically. Vol. Butler and Donald E. Milan Mrksich. Fuller himself went so far as to imagine the solar sys- form the first structures with specialized functions—the fore. No. Finally. The Architecture of Life Scientific American January 1998 57 Copyright 1997 Scientific American. a research associate in the departments of Clay Minerals and the Origin of Life. May 30. Mass. This flexibil. who holds B. Ingber in Journal of Cell Science. 1.D. genesis. tem as a structure composed of multiple nondeformable rings runners of present-day organelles—which then combined with of planetary motion held together by continuous gravitational one another to create the first simple cells. including the discovery of an anti. tal in Boston. Ingber in Annual Review of Physiology. Graham Cairns-Smith and Hyman surgery and pathology at Children’s Hospi. and of clay. Cambridge University Press.. .. advanced materials with biologically in. pages 575–599. Yale University. Ning Wang. however. Caspar in Biophys- pathology at Harvard Medical School and ical Journal. Indeed. predominate in natural systems. October 1980. and isolated black holes that experience immense compres- sembly of multicellular tissues. 104. contributed to the study of tumor angio. Donald E. that animals. such as hexagons. Christopher S. SA The Author Further Reading DONALD E. He is the Geometric Control of Cell Life and Death. scale ones? We do not know. 3.D. who. company that creates 1425–1428. Donald spired properties. D. pages JENNIFER R. 1993. Interestingly. It would have been more likely to changed. Whitesides and Donald E. Tensegrity: The Architectural Basis of Cellular Mechanotransduction. is an associate professor of Movement and Self-Control in Protein Assemblies. So it is no surprise that the basic arrangement of interact with other. Sui founder of Molecular Geodesics. Perhaps there self-assembly of tissues. Thompson. Vol.A.. Ingber in Science. He is also a member of the Cellular Tensegrity: Defining New Rules of Biological Design That Govern the Center for Bioengineering at the Mas. Ingber has Mechanotransduction across the Cell Surface and through the Cytoskeleton. tion to his work on cell structure. 1942 (reprinted 1992). Cambridge University M. the development of an embryo from a sperm and an who quoted Galileo. by early 20th-century Scottish zoologist D’Arcy W. E.A. M. that are molded by very large scale forces as well as small- ity apparently allows clay to catalyze many chemical reactions. 260. But because these octa.. Inc. promoted self-as. and complex organisms arose through is a single underlying theme to nature after all. 59. Hartman. 613–627. On Growth and Form. ture may indeed be written in the characters of geometry. cancer drug now in clinical trials. then its lifetime process of hierarchical self-assembly remained essentially un- would have been extended. George M. 276. too. Yet throughout all this time the rules guiding the pressure. has proposed including ones that may have produced the first molecular an intriguing model of the atom based on tensegrity that takes building blocks of organic life. degrees from Press.. insects and plants all rely Researchers now think biological evolution began in layers on prestress for the mechanical stability of their bodies. in turn. INGBER. pentagons and spirals. cited Plato: the Book of Na- egg recapitulates all these stages of self-assembly. off where the French physicist Louis de Broglie left off in Over time. Chen. rex and Homo sapiens. Snelson. May 21. Vol. Edited by A. Vol. the fact that our expanding (tensing) uni- produced proteins that self-assembled to form extracellular verse contains huge filaments of gravitationally linked galaxies matrix–anchoring scaffolds that.