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BONE
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There are a number of different organisms
on earth today which incorporate inorganic ions (such as calcium, silicon,
and iron) into hard protective structures.
This process is known as biomineralization. The earliest animal known to perform biomineralization
was the Precambrian worm Cloudina. |
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The modern marine bloodworm
Glycera dibranchiata is unusual in that
it synthesizes a copper based biomineral in its jaws (Lichtenegger, 2002). Bone and cartilage are connective tissues
and, as such, they are composed of specialized cells, extracellular protein
fibers, and a ground substance. The
ground substance of vertebrate cartilage is composed of the gel-like chondroitin
sulfate. Cartilage-like tissue
is actually known from a variety of organisms including vertebrates, jellyfish,
annelids (sabellid worms), snails, cephalopods, horseshoe crabs, and the
imagos of locusts. Cartilage and neural tissue share a number of
characteristics. Chondromucoid,
in the matrix of cartilage, is similar to molecules found in certain sensory
receptors. The cartilage proteins
type II collagen and aggregan are also found in the nervous system. Molecules once thought to be specific to cartilage
(such as the chondroitin sulfate proteoglycan) have been found in the
nervous system and proteins thought to be specific to the nervous system
(such as S-100 acidic protein) have been found in cartilage. (Hall, 1999). Originally, jawless fishes were thought to
possess true cartilage and certain invertebrate tissues were either classified
as chondroid if they were similar to cartilage or chordoid if they were
similar to the tissue of the notochord.
Given that lamprey and hagfish cartilages are now known not to
possess collagen as a major component, any definition which includes the
skeletal tissues of jawless fish as true cartilage also includes a number
of invertebrate cartilages. Cartilage/cartilage-like tissue is known in
cnidarians, annelids, arthropods, and mollusks (Robson, 1999). The cartilage of squid does possess collagen
and resembles the hyaline cartilage of vertebrates, although it is not
the collagen II found in vertebrate hyaline cartilage. A variety of collagenous and non-collagenous
proteins are known from invertebrate cartilages (excluding type II collagen)
which seem to have evolved separately in different lineages (Robson, 1999).
Both nonsulfated chondroitin and polysulfated
chondroitin are known in invertebrates (such as squid and crabs).
Acorn worms possess a cartilage-like skeletal rod ventral to the
stomachord in the head region (Benito, form Harrison 1997, p. 16).
Enteropneusts possess gill bars and a proboscis “skeleton” which
has been described as being similar to cartilage. (Benito, form Harrison
1997, p. 34). The pharynx of Amphioxus stretches for half the length of the body and contain 100-200
gill slits (depending on the species).
Each gill bar contains a skeletal rod for support composed of collagen
and glycosaminoglycans. (Ruppert, from Harrison, 1997, p. 434). There is disagreement over whether the material
which composes the gill bars of hemichordates (acorn worms and enteropneusts)
and lancelets should be classified as cartilage or simply as a tissue
similar to cartilage. The mucopolysaccharides
of the Amphioxus skin and notochord,
although different from craniates (including lamprey and hagfish), are
more similar to vertebrates than to those of invertebrates (Anno, 1975). Cartilaginous fish are the most primitive
animals which produce cartilage with collagen type II (and type I). Hyaline
cartilage in most vertebrates possesses collagen II as its major protein
with lesser amounts of collagen types VI, IX, XI, and XII. Lampreys possess
cartilaginous arches above the notochord.
Although type II collagen exists in the notochord of lampreys and
hagfish, it is not a major component of agnathan cartilage. The major protein in lamprey cartilage is named
lamprin, that of hagfish cartilage is named myxinin. Lamprin is homologous to vertebrate elastin,
insect chorion proteins, and spider silk proteins (Robson, 1999). Hagfish possess two types of cartilage, one
of which is not like any other known vertebrate cartilage (and is similar
to cartilage-like tissues found in invertebrates) and the second of which
possesses a unique protein myxinin. The
alveolar cartilage of hagfish is different from that of lampreys in the
amount of intercellular matrix and characteristics of the perichondrium
(Tsuneki, 1993). Lampreys possess
a similar protein similar to myxinin (called lamprin) in their cartilage
which can compose up to half the dry weight of the cartilage (Wright,
1984). In lampreys, there are dense cartilages in the
region of the brain and the neural arches around the spinal cord. A different type of cartilage, alveolar cartilage.
is found in the branchial and nasal regions. The earliest craniate fossils from the Cambrian possess no skeletal material other than the cartilage of the pharyngeal arches (Shimeld, 2000). Cartilage from the gill
bar of a fish is depicted below. |
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Collagen is the most abundant protein in
the human body. It composes about
a quarter of bone and can compose a similar or greater percentage of cartilage
(depending on the type of cartilage). It is not unique to humans or vertebrates
with skeletal systems, however. Collagen
is the major extracellular protein of all animals and is even found in
the simplest animals. A number of invertebrates have collagen fibrils
very similar to the type of collagen found in vertebrates; collagen fibrils
are even known from cnidarians and sponges.
Sponge collagen is homologus to that of vertebrates.
Since sponges can contain both fibrillar and non-fibrillar collagens,
the amplification of this gene family had begun in the early animals (Exposito,
1990). Although collagen was once
thought to exist only in animals, it has been found in fungi where it
composed the fimbriae which function in cell to cell communication. Animal cells can interact with fungal collagen
in a way similar to the manner in which they interact with animal collagens
(Celerin, 1996). Collagen sequences
may have functioned long before collagen was an extracellular protein. Collagenous sequences are known from vertebrate
proteins such as acetylcholinesterase, C1q (a complement protein), pulmonary
surfactant apoprotein, several lectins, and type I macrophage scavenger
receptor. The bacteria Streptococcus pyogenes possesses a collagen-like
sequence in enzyme hyaluronidase (Stern, 1992). Bone is not known until jawless fish in the
fossil record, but its ground substance is primarily composed of calcium
and phosphate salts. Calcium and
phosphate are important metabolic molecules in all groups of organisms
and are commonly used in metazoan animals. (Carroll, p. 23). Vertebrates depend on vitamin D and its receptor
in order to absorb the calcium necessary for the synthesis of bone.
The nuclear receptor for vitamin D, VDR, activates gene transcription
after binding to vitamin D. Although its major functions in mammals include
the absorption of calcium for skeletal formation and regulation of the
hair cycle, vitamin D receptors are expressed in lampreys which lack both
bones and hair. Lampreys may use
this gene to induce P450 enzymes (Whitfield, 2003). The proteins of vertebrate enamel are not
expressed in any other parts of the body and their function is unique,
even among other biomineralized tissues.
Amelogenin is the major protein in vertebrate enamel, composing
90% of the organic portion of enamel.
One of its exons (exon 2) is homologous to an exon of proteins
found in protostomes (osteonectin) and deuterosotmes (SC1, hevin, and
QR1). Enamel definitely existed in Ordovician ostracoderms
while its existence in Cambrian euconodonts and fish such as Anatolepis is less certain (Delgado, 2001). The secretory calcium-binding phosphoprotein
family (SCPP) includes three proteins in enamel matrix (amelogenin, enamelin,
and ameloblastin), five proteins involved in the formation of dentin and
bone (dentin, sialophosphoprotein, dentin matrix acidic phosphoprotein
1, integrin-binding sialoprotein, matrix extracelullar phophoglycoprotein,
and secreted phosphoprotein 1, caseins, and several salivary proteins.
Most of these genes are located on a cluster on chromosome 4q13
in humans. This gene family seems to have arisen from the
SPARC gene. SPARC, which is expressed
in fish bone and scales, may have been the first gene expressed in vertebrate
mineralized tissue. SPARC is expressed
where the epithelium meets the connective tissue beneath in invertebrates
and jawless fish ( The most primitive forms of cartilage in lancelets
and jawless fish does not involve collagen. SPARC is only associated with collagenous skeletal
tissues. SPARCL1 gave rise to amelogenin,
enamelin, and ameloblastin early in the history of gnathostomes ( The cells which compose the human skeletal system arise through multiple embryological mechanisms. In vertebrates, the caudal end of the embryo does not develop in the same manner as the cranial portion. The tail develops neural tissue, muscle, bone, and blood vessels from tailbud mesenchyme without ever dividing into three germ layers. In the cranial portion of vertebrate embryos, ectoderm and endoderm are the primary germ layers which induce the two secondary germ layers, mesoderm and neural crest cells. Much of the embryonic skeletal tissue is produced by mesoderm. In the head, neural crest cells (rather than mesoderm) form much of the skull (Halll, 1999). |
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Neural crest cells were a vertebrate innovation.
Amphioxus lacks them and lampreys have them (the situation in hagfish
is not yet clear). While Amphioxus lacks neural crest cells, it
expresses many of the important genes involved in the differentiation of
vertebrate neural crest cells in the region of the junction between the
neural plate and the non-neural ectoderm.
Thus it appears that vertebrate neural crest cells employed genes
which were already present in vertebrate ancestors (Ahlberg, 20-5). |
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THREE COMPONENTS OF THE COMPOSITE VERTEBRATE
SKULL Although the adult skull in higher vertebrates
is one solid structure, it develops from three separate parts: the chondrocranium,
the splanchnocranium, and the dermatocranium. The splanchnocranium is the oldest of the three
structures. The splanchnocranium,
or at least its precursor, exists in protochordates around gills forming
supports for gill arches. Although
the splanchnocranium in vertebrates is a product of neural crest cells,
true neural crest cells do not exist in protochordates.
The splanchnocranium supports the roof of the pharynx in jawless
fish (Kardong, 2002). The second portion of the skull to evolve
was the chondrocranium and all craniates possess a chondrocranium under
their brain (Kardong, 2002, p.
233, 239). The chondrochranium and splanchnocranium compose the head skeleton
of jawless fish and cartilaginous fish.
The head of lampreys consists of a number of cartilaginous structures
and includes studs on the dorsal cranium similar to those observed in
some fossil sharks and a pair of plates proceeding caudally from the occipital
region (Dean, 1900). In higher vertebrates, the chondrocranium and
splanchnocranium serve as embryonic scaffolding for the development of
the structures of the head and throat.
Some parts ossify and contribute to the bony adult skull. In the shark skull below, the splanchnocranium
forms the upper jaw (palatoquadrate), lower jaw (Meckel’s cartilage),
and a series of branchial arches (including the hyomandibula of the second
arch). Obviously the gill arches
are lost in adult amniotes, but the embryonic splanchnocranium contributes
to the malleus (Meckel’s cartilage), incus (palatoquadrate), alisphenoid
(palatoquadrate), stapes (hyomandibula of arch II), the hyoid bone (ceratohyal
and basihyal components of arch II and the epibranchial, ceratobranchial,
and hypobranchial portions of arch III), and larynx (derivatives of arches
IV and V). The embryology of the skeletal and muscular
structures of the jaws suggest that jaws developed evolved from a modified
pair of gill arches (arch I) (Kardong, 2002, p. 237) |
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shark skull |
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The
early gnathostomes evolved cartilage to form the orbital region, nasal capsules,
ethmoid region, and an otic capsule around inner ear.
Parachordal cartilage and trabeculae from around notochord contribute
in development of braincase (Romer, p. 192).
In humans, the chondrocranium contributes to the occipital bone (supraoccipital,
exoccipital, and basioccipital regions), ethmoid bone (mesethmoid and turbinals),
sphenoid bone (prespheniod, orbitosphenoid, and basispheniod regions), and
temporal bone (petrosal and mastoid process).
Early jawless and jawed fish developed dermal
bone as head armor, forming the third portion of the skull, the dermatocranium.
Dermal bone in the developing human embryo will form the following
bones in humans: premaxilla, maxilla, nasal, lacrimal, zygomatic, squamosal
(part of temporal), frontal, parietal, vomer, palatine, pterygoid, paraspheniod
(the previous 2 forming parts of the sphenoid), and dentary.
Placental mammals have lost many of the dermal bones present in
more primitive vertebrates such as the prefrontal, postfrontal, postorbital,
intertemporal, supratemporal, tabular, quadratojugal, postparietal, ectopterygoid,
splenials, angular, surangular, and a number of bones present in fish
(such as the opercular series). Fossil jawless fish (such as the ostracoderms)
and the primitive gnathostomes (placoderms) possess a dermatocranium composed
of large plates of bone. In the most primitive bony fish (acanthodians,
pictured below) the dermatocranium is composed of many smaller bones whose
patterns resembles that of higher fish although establishing precise homology
is difficult (Carroll, p. 86). |
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After acanthodians the
dermatocranium is more ossified and a pattern of dermal bones of the skull
evolved which provided the basis of the dermatocrania of actinopterygians,
sarcopterygians, and all tetrapods. These
higher vertebrates possess skulls composed of homologous bones (as indicated
in the following images of a primitive actinopterygian, Cheirolepis, and a primitive sarcopterygian,
Eusthenopteron ). |
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In fossil jawless fish such as ostracoderms
(such as that pictured below), bone existed in the skull while the rest
of the skeleton was cartilaginous. |
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Most vertebrates converted this postcranial cartilaginous
skeleton (and cartilage in the skull as well) to bone. The same pattern
is observed in higher vertebrate embryos, including those of humans. In human embryos, bone is first laid down in
the skull while the rest of the skeleton is cartilaginous. Gradually this cartilage of the postcranial
skeleton (and some in the skull as well) is converted to bone. The human skeleton can
be divided into two divisions: the axial division composed of the skull,
vertebral column, and the thorax. |
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THE CRANIUM The
Skull has two major regions: the cranium (which surrounds the brain) and
the face. (There are additional
minor elements of the skull composed of the hyoid and the auditory ossicles). The human cranium is composed of the frontal,
parietal, occipital, temporal, sphenoid, and ethmoid bones. The human face
is composed of maxillary, zygomatic, palatine, nasal, lacrimal, vomer,
turbinate, and dentary bones. |
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