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Earliest enamel deposits of the rat incisor examined by electron microscopy electron diffraction and electron probe microanalysis.

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THE ANATOMICAL RECORD 220:233-238 (1988)
Earliest Enamel Deposits of the Rat Incisor
Examined by Electron Microscopy, Electron
Diffraction, and Electron Probe Microanalysis
WILLIAM J. LANDIS, GRACE Y. BURKE, JULIA R. NEURINGER, MARY C. PAINE,
ANTONIO NANCI, PAUL BAI, AND HERSHEY WARSHAWSKY
Laboratory for the Study of Skeletal Disorders and Rehabilitation, Department of Orthopedic
Surgery, Harvard Medical School at the Children’s Hospital, Boston, Massachusetts 02115
(w.J. L., G.Y B . , J. R.N., M. C.P); Departement de Stomatologie, FacultC de MCdecine Dentaire,
Universitt de MontrCal, Montreal, QuCbec, Canada H3C 3T9 (A.N.); Department of Anatomy,
McGill University, Montreal, Quebec, Canada H3A 2B2 (PB., H. W )
ABSTRACT
In order to describe initial events in enamel mineralization and to
help characterize inorganic-organic interactions in this tissue, the earliest rod and
interrod enamel in mandibular incisors from normal young adult (100 gm) rats,
perfused with 100% ethylene glycol, has been studied by transmission electron
microscopy, selected area electron diffraction, and high-spatial-resolution electron
probe microanalysis. Diffraction and probe data were correlated precisely from the
same extracellular regions of the tissue. Sites were examined progressively as a
function of location a) from the most recently deposited enamel adjacent to ameloblasts toward the dentin-enamel junction and b) from the apical portion of the tooth
longitudinally toward its incisal end. Electron diffraction patterns consistent with
that of a poorly crystalline hydroxyapatite were generated at all locations. Diffraction characteristics changed only slightly toward that of more crystalline hydroxyapatite at different locations. Earliest apical enamel generated molar Ca/P ratios in
a range of 0.99-1.46 (average 1.24 0.15). Molar Ca/P ratios of the first enamel
interrod elements increased from 1.24 a t ameloblast-enamel boundaries to 1.40
at the dentin-enamel junction, small changes corresponding to those observed in
electron diffraction characteristics.
-
In the biomineralization of the variety of species comprising both invertebrates and vertebrates, a general
concept of mechanism holds that the deposition of a
mineral phase is ultimately controlled by a specific organic matrix serving as the framework for crystal nucleation and growth. Supporting this idea in a
circumstantial way are observations in bone (Glimcher
and Krane, 19681, dentin (Katchburian, 19731, and calcifying tendon (Landis, 1985, 1986) that hydroxyapatite
crystals are highly oriented such that their crystallographic c-axes lie parallel to the long axes of collagen
fibrils in which they are found. Furthermore, the crystals are deposited initially in the collagen hole zones
(Hodge and Petruska, 1963). In the mollusk, there is
additional evidence indicating a critical interaction between the organic matrix and composite inorganic crystals of aragonite (Weiner et al., 1983; Weiner and Traub,
1984).
While such circumstantial data provide certain evidence for a n intimate inorganic-organic relationship in
biological mineralization, a n explicit description would
be more compelling. For this purpose, both the mineral
and the matrix in a given species must be definitively
known from a molecular perspective. In no case has this
yet been accomplished, but, as a step toward this goal,
this article examines the earliest deposits of a mineral
phase in enamel from the continuously erupting incisors
0 1988 ALAN R.LISS, INC.
-
of young adult rats. This model maintains biologically a
relatively homogeneous population of its mineral phase
particles (Leblond and Warshawsky, 1979), and the preparative methods employed adequately preserve the
chemical and physical integrity of the inorganic matrices (Landis and Glimcher, 1978; Landis et al., 1977). In
this instance the initial deposits of rod and interrod
enamel from animals perfused with anhydrous ethylene
glycol have been systematically examined by transmission electron microscopy, selected area electron diffraction, and electron probe microanalysis to localize and
identify the extracellular mineral phase and to determine changes in its chemical and physical nature with
tissue age and maturation. The data help characterize
the extracellular matrices of dental tissues and some of
the basic events of enamel mineralization as a first
approach to describing molecular interactions between
inorganic and organic tissue components.
MATERIALS AND METHODS
Normal male Sherman rats, approximately 100 gm in
weight, were treated according to the general procedure
of Bishop and Warshawsky (1982). Animals were anesthetized with sodium pentabarbitone by intraperitoneal
Received April 8, 1987; accepted July 23, 1987.
234
W.J. LANDIS ET AL.
injection and then perfused through the left ventricle of
the heart with lactated Ringer’s solution for 1-2 min
and with 100% ethylene glycol for a n additional 10-15
min. Incisors were dissected from mandibular bone and
the apical third of each was sliced with a clean razorblade transversely to the long axis of the tooth. Specimens (<1 mm3) were then placed in 100% ethylene
glycol in scintillation vials, and the anhydrous treat-
ment of Landis et al. (1977) was continued through ?ample embedment in Epon. Silver sections (-800 A ) of
tissue, containing initial and inner enamel secretion
regions as determined from 1-pm-thick sections stained
with toluidine blue, were obtained with diamond knives,
floated on 100% ethylene glycol, and collected on 75mesh carbon-reinforced Parlodion-coated copper grids
(Landis et al., 1977). Grids were dried with filter paper
4
?
h
40
C.
60 9&3 100 120 1 4 0 160 160 200 228 2 4 0
CHRNNEL N O -
235
ELECTRON OPTICS OF RAT INCISOR ENAMEL
Fig. 7. Selected area electron diffraction (80 keV) of the same region
of initial enamel in the zone of secretion from which probe data were
obtained (Figs. 2 and 5). The pattern has a small number of poorly
resolved, low-intensity reflections. The major reflection appearing is a
relatively wide, bright ring at d = 2.78 A (the unresolved triplet d =
2.81, 2.78, and 2.72 A corresponding to hkl = 211 + 112 + 300,
respectively). This and a very weak reflection at d = 3.44 A (hkl =
002, not labeled) are consistent with that of a poorly crystalline hy-
droxyapatite (see Fig. 12 of Landis and Glimcher, 1978). Magnification
of transmission image was x 15,000.
Fig. 8. Selected area electron diffraction of the region of inner enamel
corresponding to Figures 3 and 6. The pattern is slightly different from
that shown in Figure 7 but only in that the weak reflections a t d =
3.44 A and 2.78 A are somewhat better resolved. Magnification of
transmission image was ~15,000.
and then placed under vacuum for several hours to remove residual glycol. Sections were left completely unstained for electron optical examination.
Methods for electron microscopy, electron diffraction, and high-spatial-resolution (electron beam diameter < l o 0 A ) electron probe X-ray microanalysis were
followed as described in detail elsewhere (Landis and
, .
Glimcher, 1982). As before (Landis and Glimcher, 1978,
Fig. 2. Enlargement of Figure 1showing the first observable initial
a JEoL loo' Or
EM 300 was
for
enamel deposits (E), evident as small irregularly shaped masses of 1982)3
thin. ribbon-like crvstals (inset) adiacent to a laver of dentin (D). The m~CrOscOPYand diffraction, and a modified JEoL JSM
proximal portions 6f secretory amefoblasts form 6lunt and wide Tomes' 50A opeiated in scanning transmission mode for probe
processes WP) without interdigitations with enamel. Dentin is consid- microanalysis. Areas having a 4-pm diameter were deerably more electron-dense than enamel in such unstained sections.
fined at the specimen for selected area electron diffrac~7,000;inset, ~35,000.
tion. Evaporated aluminum and thallous chloride were
Fig. 3. Enlargement of Figure 1 illustrating the first interrod ele- used as electron diffraction calibration standards. Dements (IR)and short, interdigitating portions of Tomes' processes bP).
Interrod growth regions (IGR) exist at the tips of the interrod elements. spite maintenance of high vacuum in the electron probe,
While the first row of rod profiles is not yet elaborated at this location, the regions of enamel investigated were susceptible to
a few of the earliest rods (R) are being formed in the spaces occupied some contamination during data acquisition; X-ray
by the processes. D, dentin. x 3,000.
counts were accumulated over 360-sec integrated detectFig. 4. Energy-dispersive X-ray spectrum generated from a region of ing time periods with a static spot probe. Quantitative
immature enamel (Point 1 in Figure 5). All spectra were obtained at determination of molar Ca/P ratios from X-ray intensity
25 keV with a stationary beam spot, beam current of 1 x lO-"A, and counts of calcium and phosphorus obtained by probe
360 sec integrated detecting time. The abscissa is calibrated relative microanalysis was made by interpolation from a stanto X-ray energy (20 eV/channel). Characteristic lines are phosphorus,
chlorine, calcium, and silicon. Chlorine originates from the Epon dard calibration curve (Landis, 1980; Landis and
Glimcher, 1982). For calculation of Ca/P intensity ratios
embedment, and silicon from electron-beam-inducedcontamination.
(Landis and Glimcher, 1982),X-ray spectra from off-peak
Fig. 5. Scanning transmission image (25 keV) of Figure 2 following regions of the tissues were taken over organic matrices
electron probe microanalysis. The center of the contamination spots
that arise during data acquisition indicates the spatial location of the adjacent to enamel. Such spectra were generally unreelectron beam. X-ray intensities for Ca and P generated from the markable and were considered negligible for computaindividual points noted on the micrograph are presented in Table 1. tional purposes.
Fig. 1. Conventional transmission image (60 keV) of an unstained
incisor thin section of immature enamel in the zone of secretion from
a normal male Sherman rat, perfused with 100%ethylene glycol. The
exact regions of the tooth from which electron diffraction and electron
probe microanalysis data were obtained are enclosed and shown at
higher magnifications in other figures. The ultrastructural features
illustrated are secretory ameloblasts (A), Tomes' processes WP), enamel
( E l dentin (D). and Dredentin (PD). x2.100.
The sites examined were selected to sample enamel deposits near the
ameloblast-enamel junction, the dentin-enamel junction, and the area
between those two regions. ~7,000.
Fig. 6. The region of developing interrod enamel elements corresponding to Figure 3 following electron probe microanalysis. The scan-
ning transmission image shows the sites examined along individual
interrods from interrod growth regions to the dentin-enamel junction.
Selected corresponding data are given in Table 2. ~3,400.
RESULTS
The portion of the rat incisor examined was that along
the labial tooth surface within the zone of secretion,
where immature enamel is formed (Leblond and Warshawsky, 1979; Smith, 1979; Warshawsky et al., 1981).
Figure 1 illustrates this area at relatively low magnifi-
236
W.J. LANDIS ET AL.
indicate a specific trend with respect to changes in calcium or phosphorus. Nor was there an apparent pattern
of change measured with respect to distance (Fig. 6)
along individual interrod or forming rod elements in
inner enamel secretion regions (Table 2), although a
suggestion of slightly increasing Ca/P may be inferred
1
Initial enamel
1.23
1.04
from the average of points such as A, B, and C.
1.56
1.28
2
Selected area electron diffraction of the same regions
1.63
1.34
3
from
which electron probe data were generated yielded
1.49
1.23
4
diffraction
patterns with few reflections (Figs. 7, 81, but
1.78
1.46
5
among those evident yere lattice spacings identified as
1.69
1.39
6
d = 3.44 and -2.78 A , corresponding to the two major
1.63
1.34
7
1.38
1.15
reflections of hydroxyapatite. The absence of other
8
1.44
1.19
9
prominent reflections and the indistinct resFlution of
1.15
0.98
10
the triplet of lines d = 2.81, 2.78, and 2.72 A indicate
Average 1.24 + 0.15 that enamel is a poorly crystalline hydroxyapatite at
Analytical conditions are as described for Figure 4 and in Materials this stage of its development. There were only minor
and Methods. Each site was examined once. Sites correspond to those differences in the intensity of most of the observed renumbered in Figure 5. The exact progression of site number with flections over the entire zone of enamel examined, and
probe location, either transversely or longitudinally along the enamel,
no changes in either the number or sharpness of those
must be followed in Figure 5 .
reflections were apparent.
TABLE 1. CalP measurements by high-spatial-resolution
electron probe microanalysis of initial enamel deposits in
the rat incisor (Fig. 5)
Ca/P X-ray
Ca/P
Site
Location
intensity ratio
molar ratio
cation in an undecalcified, unstained thin tissue section
treated anhydrously. The precise regions studied by
probe microanalysis and electron diffraction were those
between initial and inner enamel secretion (Leblond and
Warshawsky, 1979; Warshawsky et al., 1981), in which
flattened, wide proximal portions of ameloblast Tomes’
processes become apparent and the first enamel deposits
are evident as small, irregularly shaped masses. The
enamel is much less electron-dense than the adjacent
layer of relatively mature dentin (Fig. 2). Within the
initial enamel masses are narrow, Cibbon-like crystals
whose thickness varies up to 400 A (inset, Fig. 2). As
they are elaborated, the first interrod enamel elements
alternate with the short Tomes’ processes in this portion
of the rat incisor, and enamel rods are formed between
interrod partitions as development of an enamel matrix
proceeds (Figs. 2, 3).
The results of electron probe X-ray microanalysis of
immature enamel are given in Tables 1and 2. A typical
X-ray spectrum is presented in Figure 4. After 360-sec
counting times, the predominant peaks are those of calcium and phosphorus, silicon, and chlorine. The sites
examined are identified in Figures 5 and 6, scanning
transmission images corresponding to Figures 2 and 3,
but illustrating the enamel regions of interest following
microanalysis. The small, dense spots in Figures 5 and
6 are the result of electron beam-induced contamination
in this dose-sensitive tissue region; the centers of tbese
spots serve to mark the exact areas probed (- 100 A in
diameter). The underlying sources of such contamination or the causes of the observed sensitivity are unknown. At points analyzed from initial enamel, the data
(Table 11, corrected for background, show a highly variable calcium and phosphorus content and Ca/P molar
ratios between 0.98 and 1.46. Nearly all enamel values
were lower than those of adjacent dentin (Ca/P = 1.50
k 0.05 to 1.55 0.04; manuscript in preparation). The
presence of other elements, such as magnesium and
sodium, was not detected in these spectra. Comparison
of results obtained from regions of initial enamel adjacent t o ameloblasts, regions adjacent t o the dentinenamel junction, and regions between the two did not
-
+
DISCUSSION
On the basis of electron probe measurements, Glick
(1979) and Halse and Selvig (1974)have demonstrated a
gradient in the content of calcium and phosphorus with
respect to location in rat incisor teeth. Their work
showed an increase in calcium and phosphorus concentration transversely from the ameloblast-enamel junction to the dentin-enamel junction in the zone of
secretion as well as longitudinally from the apical to the
incisal region of the incisor. Thus, the most recently
deposited enamel in these teeth exists at the apical
ameloblast-enamel junction (zone of secretion). In the
present study, within this particular region of initial
and inner enamel secretion of the incisor, the progressive increases in calcium and phosphorus reported by
Glick (1979) and Halse and Selvig (1974) over the whole
incisor were also suggested by increasing Ca/P ratios
along some individual forming rod and interrod elements extending both transversely and longitudinally
as defined above. It appears, then, that small calcium
and phosphorus gradients occur even over relatively
limited portions of the rat tooth, here restricted to 15 pm in thickness and -40 pm in length in the zone of
secretion and representing a very short transit time for
the ameloblasts, calculated as about 80 min (based on
the data of Leblond and Warshawsky, 1979, Fig. 1, p.
951).
In addition, with respect t o characterization of the
initial development of enamel, the present data indicate
a solid mineral phase having a variable but consistently
low Ca/P molar ratio that does not correspond to the
known stoichiometry of a single specific calcium phosphate species. The enamel Ca/p values are generally
higher than ratios obtained from the lowest-density fractions of embryonic chick bone [molar Ca/P = 0.90-1.04
(Roufosse et al., 1979)],brushite and monetite standards
[Ca/p = 1.03 and 1.00, respectively (Roufosse et al.,
197911, and earliest deposits of an extracellular solid
mineral phase measured in situ in epiphyseal growth
plate cartilage from rat tibiae [Ca/P = 0.88-1.21 (Landis
and Glimcher, 198211. On the other hand, some Ca/P
ratios of the early enamel are similar to the values
determined from thin tissue sections of the mineral deposits in osteoid regions of embryonic chick bone [Ca/P
-
237
ELECTRON OPTICS OF RAT INCISOR ENAMEL
TABLE 2. CalP measurements by high-spatial-resolution electron probe microanalysis of
sites of earliest rod and interrod enamel in the rat incisor (Fig. 6)
C a P X-ray
C a P molar
intensity ratio
ratio
Site
Location
(range)
(average f SD)
A
B
C
D
E
F
G
H
I
1- 27
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
Interrod 1(growth region)
Interrod 1(midzone)
Interrod 1(near dentin-enamel junction)
Newly forming rod
Interrod-rod transition
Interrod (near dentin-enamel junction)
Interrod 2 (growth region)
Interrod 2 (midzone)
Interrod 2 (near dentin-enamel junction)
Interrod progressively analyzed
Adjacent to ameloblast
Adjacent to dentin - enamel junction
1.23 - 1.82
1.31 - 1.79
1.26 - 1.84
1.24 - 1.87
1.37 - 2.01
1.64 - 1.95
1.44 - 1.84
1.42 - 1.83
1.25 - 1.73
1.96
1.61
1.79
1.31
1.50
1.65
1.31
1.61
1.58
1.57
1.55
1.60
1.69
1.54
1.34
1.48
1.67
1.73
1.85
1.88
1.94
1.66
1.57
1.82
1.45
1.64
1.99
n
n
n
n
n
n
n
n
n
=
=
=
=
=
=
=
=
=
10*
10
10
10
10
10
10
10
10
1.24 f 0.12
1.29 & 0.13
1.34 0.14
1.26 f 0.14
1.38 f 0.14
1.40 f 0.07
1.31 f 0.08
1.33 f 0.10
1.28 f 0.12
1.58
1.33
1.45
1.10
1.25
1.37
1.14
1.33
1.31
1.30
1.28
1.34
1.39
1.27
1.16
1.24
1.38
1.43
1.52
1.55
1.58
1.37
1.30
1.48
1.21
1.35
1.59
*n = the number of individual sites microanalyzed at the particular location described.
Analytical conditions are as described for Figure 4 and in Materials and Methods. Each site was
examined once. Sites correspond to those numbered in Figure 6. The exact progression of site number
with probe location, either transversely or longitudinally along the enamel, must be followed in Figure 6.
- 1.2-1.3 (Landis and Glimcher, 1978)], a n octacalcium
phosphate standard [CaR 1.34 (Landis and Glimcher,
1978)], and a calcium phosphate containing poorly crystalline hydroxyapatite [CaJP = 1.45 (Roufosse et al.,
1979). Most of the rat enamel CaJP ratios are lower
than density fractions of embryonic bovine enamel [ C d
P = 1.48-1.82 (Landis and Navarro, 1983; Landis et al.,
1984)l and a well-crystallized synthetic hydroxyapatite
[ C a = 1.62 (Roufosse et al., 197911.
In terms of electron diffraction, the reflections of initial and inner enamel are characteristic of those of a
very poorly crystalline hydroxyapatite. Similar electron
diffraction patterns have also been identified under comparable conditions in all embryonic bovine enamel density fractions (Landis et al., 1984), intermediate and
higher-density fractions of embryonic chick bone (Roufosse et al., 1979), whole unfractionated embryonic and
postnatal (14 week) chicken bone (Roufosse et al., 19791,
-
and thin tissue sections of early extracellular mineral
deposits in rat growth plate cartilage (Landis and
Glimcher, 1982) and embryonic chick tibiae (Landis and
Glimcher, 1978). The present enamel diffraction patterns may resemble as well that generated from young
rat incisor enamel prepared elsewhere by anhydrous
means (Bishop and Warshawsky, 1982); but because exact lattice spacings were not published (Bishop and Warshawsky, 1982), direct comparison is not possible.
The electron diffraction data reported here show no
evidence of brushite or octacalcium phosphate, a result
consistent with earlier studies of embryonic bovine
enamel (Landis and Navarro, 1983; Landis et al., 1984).
Magnesium found in the same bovine enamel fractions
(Landis and Navarro, 1983) and in sections of rat incisors (Casciani et al., 1979) does not appear in electron
probe spectra, possibly because its concentration is below instrument sensitivity. Nor could the presence of
238
W.J. LANDIS ET AL.
carbonate, suggested in recent enamel work (Casciani
et al., 1979; Driessens and Verbeeck, 1982; Landis and
Navarro, 1983; Landis et al., 1984), be detected by the
methods employed here. Auger electron and X-ray photoelectron spectroscopies (Landis et al., 1982)are continuing in order to examine more carefully the possibility
of carbonate phases in enamel.
To describe fully the mineralization process in enamel,
it is important to relate present data from electron probe
microanalysis and electron diffraction of the extracellular calcium phosphate in the rat incisor with similar
studies of the organic matrices in this model. With respect to the latter, reports from other laboratories have
already provided some significant results from secretory
and maturation ameloblasts (Boyde and Reith, 1977,
1978; Reith and Boyde, 1978,1979), and most recently a
detailed study of the role of the organic matrix in mineralization of enamel from the rat and other species has
been completed (Jodaikin, 1986). In the latter, the nature of the organic and mineral phases of the tissues of
interest has been elegantly described in large part by Xray crystallography and electron diffraction means. The
mineral was determined to be apatitic, as shown here,
and was found to interact with a protein and lipid moeity of enamel at the molecular structure level (Jodaikin,
1986). Additional studies of inorganic-organic matrix
interrelations in rat incisor enamel treated anhydrously
are in progress in this laboratory to extend current
results.
Glimcher, M.J., and S.M. Krane (1968) The organization and structure
of bone, and the mechanism of calcification. In: A Treatise on
Collagen. B.S. Could and G.N. Ramachandran, eds. Academic Press,
New York, Vol. 2B, pp. 68-251.
Hake, A., and K.A. Selvig (1974) Mineral content of developing rat
incisor enamel. Scand. J. Dent. Res., 8240-46.
Hodge, A.J., and J.A. Petruska (1963) Recent studies with the electron
microscope on ordered aggregates of the tropocollagen macromolecule. In: Aspects of Protein Structure. G.N. Ramachandran, ed.
Academic Press, New York, pp. 289-300.
Jodaikin, A. (1986) The role of the organic matrix in enamel mineralization. Doctoral Thesis, Weizmann Institute of Science, Rehovot,
Israel.
Katchburian, E. (1973) Membrane-bound bodies as initiators of mineralization in dentine. J. Anat., 116:285-302.
Landis, W.J. (1980) X-ray microanalysis of calcium phosphate solids
prepared anhydrously as calibration standards for mineralized tissues. In: Eighth International Congress on X-ray Optics and Microanalysis. D.R. Beaman, R.E. Ogilvie, and D.B. Wittry, eds.
Pendell Publishing Co., Midland, MI., pp. 497-500.
Landis, W.J. (1985) Temporal sequence of mineralization in calcifying
turkey leg tendon. In: The Chemistry and Biology of Mineralized
Tissues. W.T. Butler, ed. EBSCO Media, Birmingham, AL., pp.
360-363.
Landis, W.J. (1986) A study of calcification in the leg tendons from the
domestic turkey. J. Ultrastruct. Res., 94:217-238.
Landis, W.J., and M.J. Glimcher (1978) Electron diffraction and electron probe microanalysis of the mineral phase of bone tissue prepared by anhydrous techniques. J. Ultrastruct. Res., 63:188-223.
Landis, W.J., and M.J. Glimcher (1982) Electron optical and analytical
observations of rat growth plate cartilage prepared by ultracryomicrotomy. J. Ultrastruct. Res., 78:227-268.
Landis, W.J., and M. Navarro (1983) Correlated physicochemical and
age changes in embryonic bovine enamel. Calcif. Tissue Int., 35:4855.
Landis, W.J., M.C. Paine, and M.J. Glimcher (1977) Electron microscopic observations of bone tissue prepared anhydrously in organic
ACKNOWLEDGMENTS
solvents. J. Ultrastruct. Res., 59:l-30.
Landis, W.J., M.D. Grynpas, R.M. Latanision, and J.R. Martin (1982)
This work was supported by research grants from the
Mineralized biological tissues studied by Auger electron and x-ray
National Institute of Dental Research, National Instiphoto-electron spectroscopy. In: Microbeam Analysis. K.F.J. Heinrich, ed. San Francisco Press, San Francisco, CA, pp. 121-127.
tutes of Health (grant DE 05351 to W.J.L.), and from the
W.J., M. Navarro, J.R. Neuringer, and K. Kurz (1984) Single
Medical Research Council of Canada (to H.W. and A.N.). Landis,
enamel particles examined by electron optics. J. Dent. Res., 63:629634.
Leblond, C.P., and H. Warshawsky (1979) Dynamics of enamel formaLITERATURE CITED
tion in the rat incisor tooth. J. Dent. Res., 58@3):950-975.
Bishop, M.A., and H. Warshawsky (1982) Electron microscopic studies Reith, E.J., and A. Boyde (1978) Histochemical and electron probe
analysis of secretory ameloblasts of developing rat molar teeth.
on the potential loss of crystallites from routinely processed secHistochemistry, 55:17-26.
tions of young enamel in the rat incisor. Anat. Rec., 202177-186.
Boyde, A,, and E.J. Reith (1977) Qualitative electron probe analysis of Reith, E.J., and A. Boyde (1979) The enamel organ, a control gate for
calcium influx into the enamel. J. Dent. Res., 580:980.
secretory ameloblasts and odontoblasts in the rat incisor. HistoRoufosse, A.H., W.J. Landis, W.K. Sabine, and M.J. Glimcher (1979)
chemistry, 50:347-354.
Identification of brushite in newly deposited bone mineral from
Boyde, A,, and E.J. Reith (1978) Electron probe analysis of maturation
embryonic chicks. J. Ultrastruct. Res., 68:235-255.
ameloblasts of the rat incisor and calf molar. Histochemistry,55:41Smith, C.E. (1979) Ameloblasts: Secretory and resorptive functions. J.
48.
Dent. Res., 58@):695-706.
Casciani, F.W., E.S. Etz, D.E. Newbury, and S.B. Doty (1979) Raman
microprobe studies of two mineralizing tissues: Enamel of the rat Warshawsky, H., K. Josephsen, A. Thylstrup, and 0. Fejerskov (1981)
The development of enamel structure in rat incisors as compared
incisor and the embryonic chick tibia. In: Scanning Electron Mito the teeth of monkey and man. Anat. Rec., 200:371-399.
croscopy. 0. Johari, ed. SEM, Inc., AMF O’Hare, IL., Vol 2, pp.
Weiner, S., and W. Traub (1984) Macromolecules in mollusk shells and
383-391.
their functions in biomineralization. Phil. Trans. R. SOC.Lond.,
Driessens, F.C.M., and R.M.H. Verbeeck (1982) The probable phase
304(B):421-438.
composition of the mineral in sound enamel and dentine. Bull. SOC.
Weiner, S., Y. Talmon, and W. Traub (1983) Electron diffraction of
Chim. Belg., 91573-596.
mollusk shell organic matrices and their relationship to the minGlick, P.L. (1979) Patterns of enamel maturation. J. Dent. Res.,
eral phase. Int. J. Biol. Macromol., 5:325-328.
58(B):883-892.
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