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20
Hierarchical Structures in Biology as a Guide for New Laterals Technology
material that accommodates reversible extensions of more than 150
percent (see "Controlled Orientations. And in bone (surrey, 1979,
1984), oriented collagen fibrils increase the elastic modulus, the work
of fracture, and the breaking strain of the associated hydroxyapatite
mineral. Although it is clear that composition (e.g., the presence of
water or minerals) is critical in determining the properties of these
collagenous materials, the range of behavior achieved on the basis of
this single versatile family of macromolecules, because of their
architecture is astonishing. The lesson for materials design is that
architecture and not composition alone must be considered in the
creation and optimization of new materials systems for use in high-
performance applications. Tendon provides an instructive example.
CASE STUDY - TENDON
Tendons connect muscle to bone around a joint,
thereby transmitting the force and displacement of muscle
into joint motion (Kastelic and Baer, 1980~. Tendons are
subjected almost exclusively to uniaxial tensile loading
directed along their length. Tendons must be elastic yet
sufficiently stiff to transmit muscular force and capable
of absorbing large amounts of energy without fracturing.
For example, tendons absorb the shock to the knee joint
in landing from a jump. This combination of mechanical
properties is accomplished through the unique
hierarchical structure of the tendon and the resulting
incremental response to mechanical loads that provides
initial elasticity, followed by high tensile stiffness and
distributed plastic deformation to avoid catastrophic
failure modes.
In the tendon, collagen fibrils are organized into
ultrastructural fibrils that interact to form microscopic
fibers that are packaged into larger fibers that are aligned
parallel to one another and oriented longitudinally
between the muscle and bone (Figure 2-2~. The linkage
among units at each level differs, giving an overall
complex set of properties to the tendon. When these
fibers are observed between crossed polarizers in the
optical microscope, they have an undulating appearance.
Further examination reveals the waveform to be a planar
OCR for page 21
Natural Hierarchical Alatenals
zigzag or crimp rather than a helix (i.e., the microscopic
structure does not reflect the helical conformation of the
constituent collagen macromolecules). The crimp is
ubiquitous in all mammalian tendons and other connective
tissue types.
i Ten~don
Collagen molecule ~~ ~,~9 ~
Subfibril ~Fibril ~_%
Microlibril ~ I lid /1,1~, ,~`,3
-~51 ~ ~]
3.5nm staining sites
1
1.5 nm 3.5 nm 1~20 nm
~1
64-nm periodicity~
Fibroblasts
F~scicle
Crimp structure \
l
Fascicular membrane
1
50 500 nm 5~300 `~m 10~500 Em
SCALE
FIGURE 2-2 Hierarchical structure of the tendon. Source: Baer et al., 1992.
The response of the various elements of the
hierarchical structure of the tendon is reflected in the
shape of the stress-strain curve (Figure 2-3~. At small
tensile deformations, the curve is nonlinear, which is the
case for all connective tissues. With further stretch, the
curve becomes steeper and linear as a result of progressive
straightening of the crimp. All normal physiological loads
are confined to the nonlinear toe region of the curve.
When all the fibers are straight, the modulus is high and
constant. In the linear region, the fully straightened
collagen fibers are further pulled elastically. If the load
is released, the tendon will immediately and entirely
recover its initial crimped morphology. At high strains,
the tendon shows yielding and irreversible damage as
the collagen fibers begin to disassociate into subfibers,
fibrils, and microfibrils. Localized slippage and voiding
between hierarchical levels account for the yielding
observed at the macroscopic level. The hierarchical
21
-
Reticular membrane
OCR for page 22
22
Hierarchical Structures in Biology as ~ Guide for New Aiatenals Technology
8
7
6
~ 5
.E
~ 4
X
-
~n
to
~ 3
4 -
~n
1
o
l
/37 months
/ 24 months
l 0 I // 12 months
- ~!//
°1
I a) 1
.
o
._
cat
a)1
a)
-1
3 months
I ~1.7 months _
to 17%
1 1 , , ,
-
0 2
4 6 8 10 12
Strain (%)
FIGURE 2-S Strese-strain behavior of rat tail tendon as a function of age. Source:
Kastelic and Baer, 1980.
design distributes stresses throughout the levels of
structure, thereby minimizing dangerous stress
concentrations that could precipitate failure and fracture.
The architecture of tendon provides important
advantages in dynamic performance. For example, in the
running human, the stresses used to launch the body off
the ground at each step stretch the Achilles tendon
elastically by about 4 percent. As the body leaves the
ground, the leap is increased as much as 40 percent by the
elastic recoil of the tendon. The total energy turnover for
one foot-strike of a 70-kg man running at 4.5 m/s is
about 100 I. Of this energy, about 17 ~ is stored as strain
energy by the tendons in the arch of the foot, and 35 J is
stored by the Achilles tendon. This energy storage
amounts to a considerable savings in the cost of
OCR for page 23
Natural Hierarchical Afatenals
locomotion (Ker et al., 1987~. The fatigue resistance of
the tendon is remarkable as well; an athlete who runs 10
miles a day can use each Achilles tendon 6 million times
in a year without suffering permanent damage.
CONTROLLED ORIENTATION
23
Even a cursory examination of tissues such as bone, mesoglea,
or cartilage reveals the important role of orientation in defining the
mechanical response of structural biomaterials. In bone, for example,
the c-axes of the hydroxyapatite crystals are preferentially aligned not
only with the axes of the associated collagen fibers but also with the
directions of pull of the attached muscles. The hierarchical features
of the tissue control the fracture properties of bone, particularly the
toughness (surrey, 1984~. Fracture surfaces show considerable
roughness, because the collagen fibers in neighboring lamellae of the
bone are oriented at right angles to each other. The work of driving
a crack across the interfaces made by the plates, sheets, and Haversian
systems of bone is much greater than it would be if the material were
homogeneous. All types of bone are anisotropic. For example, the
tensile strength of compact bovine Haversian bone is 14S, 49, and 39
MPa in the longitudinal, tangential, and radial directions, respectively.
These differences correlate directly with the orientation of the
Haversian systems in the material.
A second example of subtle orientational control may be found
in the body of the large anemone Metridium (40 cm tall x 10 cm in
diameter). The body is a hollow cylindrical wall consisting of two cell
layers separated by a layer, 2 mm thick, of a collagenous connective
tissue called mesoglea (Gosline, 1971 ). Mesoglea is a fibrous
composite that consists of ~ percent microscopic collagen fibers
(diameter of 1-5 ~m) embedded in I percent of a "rubbery" matrix of
an amorphous polymer with high molecular weight in 91 percent
seawater. The matrix surrounding the collagen fibers is probably a
protein-polysaccharide complex that forms a dilute gel linked into a
permanent network. The matrix accounts for both the extensibility
and the elasticity of the mesoglea; the collagen acts as a reinforcing
filler that provides rigidity to the soft matrix on short time scales. In
the outer layer of mesoglea, collagen fibers lie in a crossed helical
array and account for the ability of the animal to bend with tidal
flows without kinking. But in the inner layer, the microscopic
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24
Hierarchical Structures in Biology as a Guide for New Afatenals Technology
collagen fibers are circumferentially oriented, reinforcing the body
wall to the tenfold increases in body diameter (and one hundredfold
increases in body volume) that the animal undergoes in its normal
behavior.
A third striking example of the role of orientation in controlling
the mechanical performance of hierarchical biomaterials is provided
by wood, in the second case study.
CASE STUDY - WOOD
Wood is a hydrated composite with a high specific
strength and stiffness, especially in the direction of
preferred reinforcement orientation (parallel to the trunk)
(Vincent, 1990; Wainwright et al., 1982~. The fracture
toughness of wood is outstanding, largely due to the
hierarchical structural arrangement and the resulting
failure-containment mechanisms.
Wood is composed of the high-modulus, high-
strength, crystalline polysaccharide, cellulose, in an
amorphous matrix of hemicellulose, lignin, and other
compounds. The architecture is that of an aggregate of
microscopic cylindrical cell walls of the composite, with
the cylinders lying parallel to the long axis of the stem,
root, or leaf. The cellulose in the cell walls has a
preferred orientation that varies according to its position
along the radius of the cell and hence its age in the wall.
The wood of many tree species occurs in concentric
growth layers of cells that have large lumens (early wood)
alternating with layers of cell walls that have small lumens
(late wood). Figure 2-4 shows the hierarchical scale and
complexity of wood.
Wood is anisotropic and viscoelastic. Most studies
on the physical properties of wood are done on oven dried
timber (12 percent water saturation), but wood evolved to
function in trees in its saturated (wet) state. The low
density (600 kg me) of timber makes it an appropriate
material for many manmade contrivances. Wood and mild
steel show comparable stiffness per unit weight, but the
specific strength of wood is four times that of mild steel.
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Natural Hierarchical Afatenals
. - Tree
m
25
-S3
Secondary
Cell Wall ~ ~ S2
-S1
Primary
Cell Wall 7=
A' /~
Macrofibrils in
amorphous matnx
glycopro~eins Bundles of
\~˘ it/ ~In amorphous
/ hemicelluloseJ - | mains
Plant Cell Walls Macrolibril Mlcrotibril
1 ~1- - 1 -- 1 -- --
amorpl70us domain
| crystalline domain
parallel
polymer chains
i1~4 1inked
glucose
cm/mm ~ m rim
SCALED
FIGURE 2-4 Structural hierarchy of cellulose in wood. (Courtesy of D. Kaplan, U.S.
Army Natick Research, Development, and Engineering Center)
The most remarkable property of wood is fracture
toughness that is 10 times greater than would be predicted
considering volume fractions of fibers and matrix in
fibrous composites. These predictions assume that the
creation of new surface area by fiber pu11-out is the
major mechanism responsible for fracture toughness. The
mechanism accounting for the high fracture toughness for
wood is helical column buckling of the cellulose fiber-
wound cell wall (leronimidis, 1976~. Interfibrillar cracks
due to shearing will open and propagate longitudinally
while the cylindrical wall collapses inward, which allows
each cell wall to be pulled apart without being broken in
two.
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Ilierarch~cal Structures in Biology as a Guide for New Laterals Technology
DURABLE INTERFACES BETWEEN HARD
AND SOFT MATERIALS
The performance of hierarchical materials systems depends
critically on the formation of appropriate interfaces between structural
elements of disparate scale and composition. Particularly
intriguing and challenging from the point of view of system
design are interfaces between materials of widely different stiffness
(i.e., between hard and soft materials).
Nature uses a variety of strategies to make such interfaces. In
bone, for example, it has been proposed that the interface between
collagen and the hundredfold stiffer hydroxyapatite is formed via
epitaxial crystallization of the mineral on a phosphorylated collagen
template (Glimcher, 1984~. In articular cartilage, collagen orientation
changes from parallel to the surface in the outer zone, to a
perpendicular orientation at the interface, with fibers extending into
the bone (see Case Study-Articular Cartilage). And in mollusk shell
nacre, the next case study, a protein-chitin "sandwich" serves to
interconnect much stiffer inorganic crystals, absorbing much of the
work of fracture via ductile deformation and the formation of new
surface.
CASE STUDY - MOLLUSK SHELL NACRE
(MOTHER OF PEARL)
The inner nacreous layer of mollusk shells is a
layered composite that has outstanding strength and
hardness white maintaining remarkable fracture toughness
(Jackson et al., 1988; Sarikaya et al., 1990~. The high
volume fraction of the reinforcing (hard) phase,
compared with processible synthetic composites, allows
strength and hardness to approach that of the monolithic
material. The reinforcing phase is bound with a very thin
layer of soft but tenacious matrix that imparts fracture
toughness to the composite.
The structure of nacre is shown in Figure 2-5.
Aragonite "bricks" make up layers 150-500 nm thick that
are interspersed with layers of organic polymeric material
20-250 nm thick. The aragonite bricks are plate-like
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Natural Hierarchical Materials
single crystals with specific orientation relationships
among crystals of the same layer, as well as among
crystals of successive layers. The organic matrix phase is
continuous throughout the material and is composed of
the aminopolysaccharide, chitin, coated with a protein
that promotes adhesion to the aragonite plates.
The mechanical properties of nacre are better than
those of most monolithic ceramics, with fracture strength
of 185 ~ 20 MPa and fracture toughness, K,c = ~ +3
MPa m-% (Sarikaya et al., 1990~. The work of fracture
across layers is 1 kJ me, and between layers is 0.1 kJ ~ ma.
Toughening mechanisms revealed by fractographic
analysis of fracture surfaces and indentation cracks
include (1) crack blunting and branching; (2) microcrack
formation; (3) sliding and pull-out of aragonite plates; (4)
polymeric ligament formation, akin to crazing, which
bridges cracks; and (5) possible strain hardening and
shearing of the organic material.
THE ROLE OF WATER
27
Water is ubiquitous in biological materials, in amounts varying
from a few percent in fibrous proteins to more than 90 percent in
mesoglea. Water forms strong hydrogen bonds with biological
macromolecules and facilitates motion on all length scales, from
molecular to macroscopic. The elasticity and toughness of many
biological materials depend critically on hydration. In nacre, for
example, toughness and ductility double upon hydration without
significant loss of stiffness (Vincent, 1990~.
Swelling pressures resulting from the presence of water in
biological structures help to oppose compressive loads. In articular
cartilage, for example, water constitutes 65-80 percent of the tissue
and is confined in a swollen network of collagen fibers and
proteoglycan aggregates. As described in the fourth ease study, the
resulting hydrostatic pressure accounts for most of the apparent
compressive modulus of the material and provides a source of
lubricating fluid, which maintains the low coefficient of friction in
the joint.
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28
Hierarchical Structures in Biology as a Guide for New Materials Technology
. ~
. ..
FIGURE 2-5 The structure of nacre. Source: Sarikaya et al., 1990.
,,.~
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Natural Hierarchical Afatenals
CASE STUDY - ARTICULAR CARTILAGE
Articular cartilage (Mow et al., 1990; 1992) is a
natural hierarchical material exhibiting high strength and
stiffness; functionally gradient microstructure; and
outstanding friction, lubrication, and wear characteristics.
Compositional and organizational characteristics provide
the appropriate Reformational behavior required for
cartilage to function as the low-friction, wear-resistant
bearing materials at the ends of long bones (hip, knee,
shoulder, etc.) and sides of sesamoid or carpus bones
(patella, wrist bones, etc.) in highly loaded conditions.
Articular cartilage is a porous-permeable, fiber-
reinforced composite filled with fluid. The fibrous
component is primarily type II collagen, and the gel
matrix is made of aggregating proteoglycans. Collagen
and proteoglycan form interpenetrating networks that
create a strong solid matrix. Water, is by far the largest
component (70 to 90 percent) of the tissue by wet weight
as it is with most biologic tissues. Water contains a
physiologic concentration of electrolytes that is required
for osmotic equilibrium.
The collagen network is cohesive, strong, and
permanent, and it provides the required tensile stiffness
and strength for cartilage. These properties derive from
the intrinsic properties of the collagen molecule and the
hydroxypyridinium cross-links that exist between
collagen fibers. The proteoglycan aggregates form a
labile network that provides the compressive stiffness that
results from their bulk compressive stiffness and from the
swelling pressure. The swelling pressure has two
components --Donnan osmotic pressure and charge-to-
charge repulsion amongst fixed negative charges (COO
and SO3-) on the glycosaminoglycan groups of
proteoglycans.
Figure 2-6 illustrates the collagen microstructural
organization of articular cartilage. Collagen content and
collagen fiber orientation vary with depth from the
articular surface. In the tissue, collagen content decreases
and proteoglycan content increases from the surface zone
to the inner zone next to the bone. Collagen fiber
29
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30
Hierarchical Structures in Biology as a Guide for New Afatenals Technology
orientation can be characterized in three zones: the outer
surface zone has a preferred orientation parallel to the
surface; the middle zone has orientation at nearly 45° to
the surface; the deep zone has orientation perpendicular
to the bony interface, with the fibers extending into the
bone for effective anchorage. This is an excellent example
of a junction between materials of high and low modulus.
Normal articular surface is textured with ripples and
dimples, with characteristic dimensions ranging from 0.1
to 10.0 ,um. These features function to trap pockets of
synovial fluid that enhances fluid-film lubrication
between the two bearing surfaces of the joint. In
addition, the formation of the fluid lubricant film in
joints is augmented by a circulation of water from
cartilage. The high water content in the surface zone is
particularly important for this self-lubrication process to
develop.
Zones
Superficial tangential (10-20%)
Middle (40-60%) ~ I,
Deep (30%)
_ Articular surface
Calcified cartilage / ',~V'~.@c8~7~=,~~cV~ e~t5~_-,~O_ -"v~.v''"~' "v''=
~ A._
~ Cancellous bone
FIGURE 2-6 Ultrastructural organization of collagen fibers throughout the depth of
articular cartilage. Source: Mow et al., 1992. By permission of the publishers,
Butterworth-Heinemann, Ltd.
The hierarchical architecture of diarthroclial joints
and articular cartilage is illustrated in Figure 2-7. The
charged nature of proteoglycans and electrolytes at the
nanometer scale is responsible for tissue swelling,
hydration, and pre-stress in the collagen network. The
molecular and ultrastructural organizations of the
OCR for page 31
Natural Hierarchical Afawnals
collagen-proteoglycan solid matrix are responsible for the
fiber-reinforced composite nature of the tissue. The pre-
stress (or residual stress) in the collagen network that
results from proteoglycan swelling is believed to have an
important physiologic function similar to pre-stressed
reinforcement bars in concrete beams. The degree of
hydration in the cartilage depends on the balance of
swelling pressure and the elastic pre-stress developed in
the solid matrix and is the most important factor
governing cartilage mechanical properties and function.
The cells in each zone of the tissue are structural
features at the microlevel, and they are responsible for
the phenotypic expression of the protein and
carbohydrate products that are required to make collagen
and proteoglycan and to maintain the specific structural
organization in each zone of cartilage throughout life.
This self-repair process is essential for maintaining the
structural integrity of the tissue. When the biologic
maintenance and repair processes fail, the cohesive
collagen-proteoglycan solid matrix weakens, cartilage
gains excessive hydration, and it fails to function as a
bearing material in the joint. In this case, diseases such as
arthritis develop. Normal cartilage has a coefficient of
friction ranging from 0.005 to 0.02. Diseased cartilage
has higher coefficients of friction. To put these figures
in perspective, the value of ice on ice is 0.01~.1, and for
graphite on steel, about 0.1.
The complex architecture of articular cartilage
results in a joint that can endure millions of cycles, under
heavy loads (up to 18 MPa), without failure. The tensile
modulus varies from zone to zone, from 41 MPa near the
surface to 1.0 MPa near the bone. The equilibrium
compressive modulus (1.5 MPa) does not appear to vary
with zone and is provided equally by the bulk
compressive stiffness and the swelling pressure. Under
dynamic loading, very high compressive moduli have
been reported (50 MPa). This apparent stiffness is
provided largely by the pressure developed in the
incompressible water component of the tissue. Thus,
water has a major role in the ability of normal cartilage to
oppose compressive loads in physiologic conditions.
31
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32
Hierarchical Structures in Biology as a Guide for New Afatenals Technology
Oculars
Carobs ~ ~
5\ Led ||
HICK
(0.5cn~15cm)
67 nm
Collagen Triple Helix
Jolnt Cavig''
Subchondral Cortex
Cancelhus id
and Marrow
Collagen Proteoglycans
1 1
~ ~1
Nano
(10 tin-10~m)
Jesus
(10~10~m)
1
ChondrocyI. Arikular Cartable
~'o'm.O 'm ~ .
15llm~
Ultra
(10~10~m)
Ulkro
(10 7m-10~m)
FIGURE 2-7 Hierarchical architecture of diarthrodial joints and the constituent
articular cartilage. Source: Mow et al., 1992. By permission of the publishers,
Butterworth-Heinemann, Ltd.
Finally, the collagen-proteoglycan solid matrix is
viscoelastic, with a shear modulus that increases
monotonically with frequency from 0.2 MPa at 0.01 Hz to
2.5 MPa at 20 Hz. Thus the shear stiffness of cartilage is
provided by collagen within the collagen-protoglycan
solid matrix.
PROPERTY VARIATION IN RESPONSE TO CHANGING
PERFORMANCE REQUIREMENTS
Perhaps the most fascinating characteristic of many natural
materials is their capacity to respond-via changing properties to
changes in performance requirements. For example, while the spines
of the sea urchin are moving, the attacher! ligaments are soft and
extensible, but when the animal is stimulated,the ligaments become
OCR for page 33
Natural Hierarchical Materials
33
viscous, causing the joints to stiffen (Motokawa, 1984; Trotter and
Koob, 1989~. The effect is so dramatic that the calcite spines will
fracture before the stiffened joints will give way to a sudden blow.
The catch connective tissue of the urchin contains collagen alders In
a tendon-like parallel array. Extending into the array are axons of
nerve cells whose bodies lie in a ganglion outside the tissue. These
ligaments lie parallel to muscles that bend the joint at the base of the
spines, allowing the animal to point its spines at aggressors or to use
its spines as stiff legs for walking. Isolated ligaments deprived of
calcium ions are soft, while those exposed to natural concentrations of
calcium are extremely viscous. Neurotransmitters (to which the
isolated ligaments are sensitive) may be produced by the attendant
nerve cells to control the ionic environment and thus the mechanical
properties of the ligaments.
. . . -
CASE STUDY - SHARK SKIN
The skin of sharks and other fishes operates
mechanically as a two-dimensional membrane that is 2-4
mm thick and formed into a pressurized cylinder
(Wainwright et al., 1978~. Shark skin is more than 80
percent collagen by volume. Its thick inner layer is made
up of collagen fibers in 30 to 90 layers that are each 10
Am thick. Fibers in each layer are parallel, and fibers in
alternating layers wrap around the animal's body in right-
and left-handed helices. This makes the body a fiber-
wound, pressurized cylinder. The fibers lie closely spaced
in a viscous matrix of cells and other extracellular
materials as yet unknown.
When the fish swims, it bends its body in left and
right directions, stretching the skin 10-15 percent on the
outside and compressing it 1-15 percent on the inside of
the bends. Thus the skin normally functions by stretching
10 percent, even though collagen's breaking strain is
about 4 percent. The crossed-helical array of fibers and
the hierarchical structure of the skin permit this range of
motion.
The shark's body is mostly muscle, which is a
cellular viscoelastic solid of constant volume. When
muscle contracts, shortening one side of the fish, it bulges
OCR for page 34
:
34
Hierarchical Structures in Biology as a Guide for Mew Afatenals Technology
and causes an increase in pressure against the skin on that
side. High modulus fibers wound helically around
flexible cylinders reinforce against aneurysms that can be
caused by internal pressure and allow the cylindrical body
to bend without kinking.
Stress in the skin of any thin-walled cylinder equals
the pressure multiplied by the ratio of the body radius to
the skin thickness. Skin stress in a fast swimming shark
rises with pressure by as much as 200 percent. Since the
skin is only stretching by 15 percent at most, to bear the
increased stress the apparent stiffness of the skin
increases amazingly, by a factor of 13. Thus, during
normal function, stiffness, a material property normally
thought to be static, is changing according to the demands
of muscle action. The increase in stiffness apparently
allows the skin to act in transmission of force from
muscle in the anterior parts of the fish to manipulate the
tail.
It is likely that the study of biological materials capable of this
kind of environmental response will reveal a rich variety of
mechanisms for coupling of sensory information and the physical and
mechanical properties of materials. Such studies should provide
concepts useful in the design of new classes of advanced ("smart")
materials with the capacity to adapt rapidly and productively to
changing environments.
FATIGUE RESISTANCE AND SELF-REPAIR
Organisms are remarkably durable, especially in view of the
fragility of their molecular constituents. The mechanisms by which
organisms and tissues withstand damage without catastrophic failure
are of interest with respect to the design of damage-tolerant materials
and structures. In some tissues (e.g., in bone), durability results from
a complex process of remodeling and reconstruction (surrey, 1984~.
In others (e.g., in cellular membranes and associated soft tissues),
resistance to wear and fracture emerges from the architectural features
of the structure itself.
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Natural Hierarchical Alatenals
CASE STUDY - CELL MEMBRANES AND SOFT TISSUES
The structure of cell membranes and their assembly
into soft tissue can provide remarkable durability and
wear resistance to biological organisms (Bloom et al.,
1991; Evans, 1985; Evans and Skalak, 1980; Lipowsky,
1991~. The core layer of the membranes of animal and
plant cells is a bilayer in which lipids, surfactants with
short alkyl polymer chains, are organized into a
hydrophobic film sandwiched between hydrophilic
surfaces in which other cosurfactants (e.g., cholesterol,
integrin proteins, ion channels, etc.) are embedded.
Adjacent to the lipid core is a scaffolding of cytoskeletal
proteins (e.g., actin), which supports the bilayer through
specific sites of attachment along the inner surface of the
membrane. Embedded inside the cell and often within a
cytoskeletal mesh, other nonstructural organelles form a
visceral slurry in which many biochemical functions are
carried out, such as protein and lipid fabrication and
chemical energy storage and generation.
The membrane is hyperdeformable and ultrasoft
with low extension modulus, for example, 0.1 to 1 kPa for
the red blood cell (the modulus of soft rubber is 0.1 to 1
MPa). The lipid bilayer chemically isolates and regulates
the cell interior; the cytoskeletal network provides
mechanical support and controls the ability of the cell to
change shape and, in some cells, to move. Large
deformations are made possible by wrinkles and folds in
the membrane. Cholesterol augments the cohesive and
anchoring strength of the bilayer tenfold. Thus, in the
red blood cell, a rigid polymer scaffolding has been
interfaced with a fluid membrane to form a compatible
composite that is two orders of magnitude softer than
existing synthetic elastomers.
At the next higher level of the structural hierarchy,
a soft tissue, such as skin or liver, can be described as an
aggregate of fluid membrane capsules which is supported
by internal networks that are connected to form a
compatible composite that is resistant to wear and
fracture. Cells are bonded together by specific molecular
"welds" between integral proteins in adjacent membrane
35
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Hierarchical Structures in Biology as a Guide for New laterals Technology
bilayers, which provide transmission of cytoskeletal stress
from one cell to the next. The lipid bilayer envelopes are
thus "transparent" to stress, and the mechanical properties
of the tissue arise from the network of cytoskeletons that
penetrate the bilayer capsules. Intercellular connections
easily translate along the fluid bilayer, and the
membranous envelope readily flows to accommodate
network deformation. Friction between cells is
minimized by highly hydrated glycoprotein spacers.
SHAPE CONTROL
The beautiful and intricate shapes of biological structures are
apparent to even the most naive observer (Figure 2-~. But perhaps
even more remarkable are the mechanisms by which structural shapes
are controlled in biology. The shapes of a few simple biological
structures (e.g., simple viruses), are entirely determined by the
interactive properties and shapes of their macromolecular components,
as these govern the self-assembly of the structures. However, complex
shapes emerge from small scales to large, through intricate processes
of molecular and supra-molecular assembly. Molecular information
in biology is translated into structural features that are orders of
magnitude larger in scale, and into performance properties that serve
the survival needs of the organism. An understanding of these
processes offers the prospect of significant new approaches to the
fabrication of complex synthetic structures.
Large biological structures consist of cells and matrices. The
overall shape of such a structure is governed by the disposition of the
component cells and of the matrices that some of them manufacture.
The matrix-producing cells are closely apposed to existing matrix and
may eventually become enveloped in matrix that they form. At any
time during manufacture, the evolving shape of a biological structure
is the product of multiple, successive hen-and-egg events: the cells
that are currently making matrix are at specific sites because of earlier
events in the development of the organism, and they, in turn,
influence the sites where future cells will produce additional matrix.
The number of synthetically active cells at a given site depends on
earlier replication of cells by cell division; on migration of cells over
preexisting structures; and on numerous genetic programs that control
cell division, specialization of cells, and synthetic acitivity. In
OCR for page 37
Natural Hierarchical Aiatenals
37
addition, there are a variety of control feedback loops, many of which
are poorly understood. Cells can mutually influence each other
through diffusible factors, such as hormones and cytokines; cells
repond to signals from adjacent matrix; and the biosynthetic activity
of matrix-producing cells may even respond to local, repeated
mechanical stress.
From the above, it follows that the intimate relationships
between the local manufacturer of matrix components, for example,
a fibroblast cell, and the matrix to which it adheres, which may be
part of a tendon or bone, influence both the local composition and the
orientation of new matrix and, eventually, the shape of the completed
tendon or bone. The local composition readily acquires a layered, or
even interwoven, structure due to repeated cycles of deposition by sets
of cells.
Shape is not only influenced by geographically different rates
of formation but also by selective removal of existing matrix or of
complex combinations of cells and matrix. Tadpoles initially make a
tail but then lose it when they turn into frogs. The whole head of a
newborn infant could fit into the skull cavity of the adult head that it
later develops into. This is partly because of selective removal of bone
from the inner surface of the skull even while more bone is added to
the outer surface during growth. The removal of existing matrix
cluring growth can be highly selective not only at the macroscale of
sculpting a previous shape but also at the microstructural level. For
example, the walls and ends of a tubular long bone are not
continuously solid but consist of trabeculae of bone that run along
lines of mechanical stress during average, common use. These
trabeculae are not permanently fixed but can change during abnormal
use of limbs, as with a lopsided gait after injury to the one leg. Thus
normal and pathological bone removal change the shape and structure
of an earlier biological form.
In summary, biological shape is the outcome of repeated
deposition and selective removal. A critical feature during biological
manufacture is that the microfactory, the cell, is intimately and locally
associated with the evolving matrix. Importantly, many cells function
at any one time, and the successive actions of cells are influenced by
the history of manufacture. In general, shape and size are not fixed
but change with the development and age of the organism.
OCR for page 38
Hierarchical Structures in Biology as a Guide for New Afatenals Technology
FIGURE 2-8 Scanning electron micrographe of the rasping tongue of the mollusk
Urosalpir~x cinereaSol~yensis. The mineralized structure contains crystalline magnetite in
an ordered matrix of organic fibrile. Magnification: (a) 200x, (b) 575x, (c) 980x, (d)
980x. Source: Carriker et al., 1974.
Representative terms from entire chapter:
natural hierarchical
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