|
Volume 271, Number 36,
Issue of September 6, 1996
pp. 21695-21698
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
COMMUNICATION:
Sequence Determination of an Extremely Acidic Rat Dentin
Phosphoprotein*
(Received for publication, May 17, 1996, and in revised form, July 9, 1996)
Helena H.
Ritchie
§ and
Lee-Ho
Wang
¶
From the Department of Pediatrics, the University of
Iowa, Iowa City, Iowa 52242 and the ¶ Division of Hematology, the
Department of Internal Medicine, the University of Texas Medical
School, Houston, Texas 77030
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
FOOTNOTES
Acknowledgment
REFERENCES
ABSTRACT
The mineralization process associated with the
conversion of predentin to dentin is believed to be initiated and
controlled by a set of acidic regulatory noncollagenous proteins (NCPs)
which include phosphophoryn, the major NCP in dentin. Phosphophoryn
binds tightly to collagen and is believed to initiate the formation of
apatite crystals which play a central role in the mineralization
process. During the process of analyzing the 3 end of an
odontoblast-specific cDNA which codes for dentin sialoprotein
(Ritchie, H. H., Hou, H., Veis, A., and Butler, W. T. (1994)
J. Biol. Chem. 269, 3698-3702), we discovered a
801-base pair open reading frame. This downstream open reading frame
encodes a putative leader sequence and a very acidic mature protein
sequence having a deduced amino acid composition containing high
percentages of both Ser (43%) and Asp (31%) residues which closely
coincides with the amino acid composition of phosphophoryns from human,
bovine, rat, and rabbit (i.e. Asp (30-40%) and Ser
(38-50%)). This newly identified cDNA therefore encodes a protein
with characteristics similar to phosphophoryn. Here we present the
cDNA sequence, the deduced amino acid sequence, and the prospective
Ser residue-specific casein kinase I and II phosphorylation sites for
this putative phosphophoryn.
INTRODUCTION
The calcification process that accompanies the transition of
predentin to dentin is poorly understood, due in part to the
difficulties in isolating and characterizing unique sets of
extracellular matrix molecules that contribute to this complex process
(1, 2, 3, 4). Phosphophoryn, the most abundant noncollagenous protein in
dentin, is secreted by odontoblasts through odontoblastic processes and
appears at the mineralization front within a short time after labeling
with [33P]phosphate (5, 6). Phosphophoryn is known to
bind large amounts of calcium with a relatively high affinity (7) and
to then form an insoluble aggregate in the presence of Mg2+
and Ca2+ (8). Because of its affinity for calcium,
phosphophoryn may concentrate these ions and participate in the
formation of apatite crystals. For example, Linde and co-workers (9)
have demonstrated that when phosphophoryn is immobilized on a stable
support and incubated in physiological solutions of calcium and
phosphate, phosphophoryn induced the formation of hydroxyapatite
(HAP).1 Studies by the same group (10) and
by Boskey et al. (11) also suggested a dual role for
phosphophoryn as both an initiator of HAP formation at low
phosphophoryn concentrations and as an inhibitor of HAP formation at
higher phosphophoryn concentrations.
Phosphophoryn is also believed to have a specific affinity for collagen
(2, 12, 13) which comprises as much as 80% of the protein in dentin.
Furthermore, phosphophoryn was found to be specifically associated with
the ``e'' band of collagen (14). This site-specific protein-protein
interaction, coupled with phosphophoryn's ability to initiate or
inhibit HAP formation when calcium is present, has lead to the
currently accepted view that phosphophoryn plays a central role in the
mineralization process by virtue of its ability to target
mineralization to selected sites as well as to couple mineralization,
temporally, with organ development.
While only several NH2-terminal residues and small
proteolytically obtained segments of internal amino acid sequences of
phosphophoryn are currently known, the complete amino acid sequence of
phosphophoryn has not as yet been reported. During the process of
analyzing the 3 end of dentin sialoprotein (DSP) cDNA, another
recently cloned dentin-specific protein (15), an open reading frame
with a size of 801 bp was revealed. This open reading frame was found
to encode a putative leader sequence and a deduced very acidic mature
protein sequence with an amino acid composition comprised primarily of
Ser (43%) and Asp (31%) residues which coincides with the amino acid
composition of phosphophoryns from human, bovine, rat, and rabbit
(i.e. Asp (~30-40%) and Ser (~38-50%)) (2, 16, 17, 18, 19, 20, 21).
Here we present the first reported cDNA sequence, the deduced amino
acid sequence, and the postulated Ser residue-specific casein kinase I
and II phosphorylation sites for this putative phosphophoryn.
EXPERIMENTAL PROCEDURES
RNA Preparation and Reverse Transcription-PCR
The total RNA
was extracted from adult rat incisors using RNAzolTM
(Biotecx Laboratories, Inc., Houston, TX). A cDNA pool was
synthesized from total RNA using an oligo(dT) primer and reverse
transcriptase. This cDNA pool was then denatured at 95 °C for 5 min and amplified with the primer set comprising an oligoprimer
corresponding to rat DSP cDNA nucleotide sequence 1054-1069 (15)
and a poly(dT) primer. PCR was then performed as follows: denaturation
(1 min at 94 °C), reannealing (1 min at 56 °C), and amplification
(3 min at 65 °C), for 40 cycles.
DNA Sequencing
The PCR products recognized by the 3 end
rat DSP probe were subcloned into TA vectors using standard techniques
(22). Following company procedures, Erase-A-Base Kit (Promega, WI) was
used to generate unidirectional deletions of the 2-kb insert for DNA
sequencing. DNA was sequenced according to Sanger et al.
(23).
Northern Blot Analysis
The total RNA from rat incisor was
electrophoresed using a 1.2% agarose gel containing 2.2 M
formaldehyde (22). RNA was transferred onto a nitrocellulose paper and
hybridized overnight with a 32P-labeled putative rat
phosphophoryn probe at 42 °C in 50% formamide and 6 × SSC.
The filter was washed with 2 × SSC and 0.1% SDS at
room temperature twice and 1 × SSC and 0.1% SDS at 65 °C for
15 min prior to autoradiography.
RESULTS
The Deduced Phosphophoryn cDNA Sequence and the Deduced Amino
Acid Sequence
Using an oligoprimer corresponding to DSP cDNA
nucleotide sequence 1054-1069 (15) and a poly(dT) primer to amplify
the cDNA pool from rat incisors, a 2-kb PCR fragment recognized by
32P-labeled 3 end rat DSP probe was obtained and subcloned
into a TA vector for DNA sequencing by the Erase-A-Base technique. An
open reading frame, located immediately downstream from the 3 end
coding region of DSP (i.e. identical to the reported DSP
sequence) (15) was identified in this 2-kb insert. This open reading
frame contained 801 nucleotides, representing 267 amino acids,
including the 27-amino acid putative leader sequence and a 240-amino
acid mature protein sequence (Fig. 1). The deduced
27-residue leader sequence is
Met-Gly-His-Ser-Arg-Ile-Gly-Ser-Ser-Ser-Asn-Ser-Asp-Gly-His-Asp-Ser-Tyr-Asp-Phe-Asp-Asp-Glu-Ser-Met-Gln-Gly.
Fig. 1.
The DNA sequence of the open reading frame
for putative phosphophoryn and its deduced amino acid sequence.
The arrow shows the translation start site (ATG; code for
putative intiation codon Met) located at nucleotide position 43. Brackets enclose the 27-amino acid signal peptide sequence.
Underlined 4-amino acid sequence is identical with the
protein microsequence data for rat (25). Parentheses enclose
potential (i.e. Asn-X-Ser)
N-glycosylation sites.
[View Larger Version of this Image (47K GIF file)]
The completed DNA sequence for this clone was found to contain a
translation start site (ATG) for the secreted protein at nucleotide
position 43 (Fig. 1). At position 3 from the translation ATG start
site, there exists an adenine nucleotide representative of a Kozak
initiation sequence and a purine residue at position +4 (24). The four
NH2-terminal amino acids (i.e. Asp-Asp-Pro-Asn)
deduced from the cloned DNA sequence (Fig. 1) were identical to those
previously reported for mature rat dentin phosphophoryns (25).
Hydropathy distribution analysis (not shown) revealed that the protein
is extremely hydrophilic. The net charge of the secreted protein
(before phosphorylation) was calculated to be 78 with an isoelectric
point of 2.95.
Amino Acid Composition
Table I compares the
deduced rat amino acid percentages obtained from our cDNA to the
actual amino acid percentages (%) for phosphophoryns purified from
rat, rabbit, bovine, and human (2, 16, 17, 18, 19, 20). This putative phosphophoryn
contains high percentages of Ser (43%) and Asp (31%) residues which
yield a highly acidic molecule and closely coincide with the amino acid
composition of authentic phosphophoryns from rat, rabbit, bovine, and
human (i.e. Asp (30-40%) and Ser (38-50%)).
Table I.
Amino acid composition of deduced rat phosphophoryn versus native rat,
rabbit, bovine, and human
phosphophoryns
| Amino
acid |
Rata |
Rata |
Ratb,c
|
Rabbitb,d |
Bovineb
|
Humanb,g |
 |
 |
fetale |
2
yearf |
|
|
residues/ molecule |
% |
% |
% |
% |
% |
% |
% |
| Aspartic
acid |
74 |
31 |
36 |
36 |
27.6 |
3.8 |
40 |
36 |
| Serine |
103 |
43 |
49 |
45 |
50 |
43 |
48 |
38 |
| Glutamic
acid |
10 |
4 |
3.6 |
6.5 |
5.6 |
3 |
1.2 |
5 |
| Glycine |
12 |
5 |
4 |
7 |
4.9 |
4 |
2.4 |
5 |
| Lysine |
5 |
2 |
1 |
0.8 |
4.3 |
5 |
4 |
1.3 |
| Histidine |
4 |
1.7 |
1 |
1 |
0.44 |
0.7 |
0.5 |
1.4 |
| Asparagine |
16 |
6.7 |
|
|
|
|
|
|
| Tyrosine |
1 |
0.4 |
0.35 |
0.47 |
0.28 |
0.2 |
0.2 |
0.44 |
| Threonine |
9 |
3.7 |
1.5 |
1.9 |
2 |
0.6 |
0.7 |
2 |
| Proline |
1 |
0.4 |
0.8 |
2 |
0.9 |
0.8 |
0.5 |
5 |
| Alanine |
4 |
1.7 |
1.4 |
2.9 |
1.3 |
1.4 |
0.6 |
0.68 |
| Isoleucine |
1 |
0.42 |
0.25 |
0.44 |
0.4 |
0.6 |
0.3 |
0.36 |
|
|
a
Amino acid composition derived from deduced protein
sequence; %, amino acid composition represented in percent.
|
|
b
Amino acid composition derived from native protein.
|
|
c
DiMuzio and Veis (17).
|
|
d
Richardson et al. (16).
|
|
e
Termine et al. (18).
|
|
f
Stetler-Stevenson and Veis (19).
|
|
g
Takagi and Veis (20).
|
|
Phosphorylation Sites
The core protein of our putative
phosphophoryn is acidic in nature (i.e. 31% Asp and 4%
Glu) and contains a high content of Ser residues (i.e. 43%
Ser; see Table I). Phosphophoryn protein is secreted by odontoblasts in
a highly phosphorylated form (2, 6, 26, 27). In vitro
studies have demonstrated that membrane-bound forms of casein kinases I
and II isolated from osteoblast-like cells can catalyze phosphorylation
of nascent dentin phosphophoryns (28). Because Ser residues are the
predominate amino acids in our putative phosphophoryn sequence, we
examined the potential casein kinase I and II sites since these
ubiquitous enzymes are known to phosphorylate serine and/or
threonine residues in a variety of proteins involved in different
cellular functions (29, 30).
Casein Kinase I Sites
As a conservative estimate for the
number of casein kinase I phosphorylation sites, we have used the
concensus sequence (Asp/Glu)-X-X-Ser (29).
Phosphophoryn contains 29 putative primary casein kinase I sites (Fig.
2). Interestingly, in some cases, the phosphorylation of
the serine residue in this consensus sequence enables casein kinase I
to then phosphorylate the serine residue located two amino acids
downstream from this newly phosphorylated serine
(Ser(P)-X-X-Ser). When this secondary target site
is phosphorylated, it then determines the tertiary Ser site for casein
kinase I and so forth. For example, Ser103 is a primary
target for casein kinase I. Based on this phosphorylation mechanism,
once Ser103 is phosphorylated, it can trigger
phosphorylation of the following 17 target Ser sites ending at
Ser154 (1a through 1r) (see Fig. 2).
When all those subsequent secondary, tertiary ... etc. sites are
included, a total of 66 potential phosphorylation sites may be
available for casein kinase I.
Fig. 2.
A, the potential casein kinase I
(*1) and II (*2) phosphorylation sites for the
putative phosphophoryn. *1a, primary target site
(i.e. (Asp/Glu)-X-X-Ser) for casein
kinase I (29, 36), *1b-*1r, secondary, tertiary (and so
forth) sites (i.e. Ser(P)-X-X-Ser) for
casein kinase I (35); *2a, primary target site
(i.e. (Ser/Thr)-X-X-(Asp/Glu)) for
casein kinase II (29, 39, 40, 41); *2b-2r, secondary, tertiary
(and so forth) sites for casein kinase II (i.e.
(Ser/Thr)-X-X-Ser(P)). B, the acidic
residues and potential acidic regions generated by casein kinases I and
II are depicted in boxes. Many of these acidic regions
consist of (DD)n, (pSpS)n, (pSD)n units (where
n = 1, 2, or 3). Several significant acidic domains
containing for example 21 residues (96-116), immediately followed by a
series of 2 residue (i.e. mainly pSD) repeats (118-155) and
24 residues (176-199) are particularly evident.
[View Larger Version of this Image (55K GIF file)]
Casein Kinase II Sites
This rat phosphophoryn contains 23 potential primary casein kinase II sites
((Ser/Thr)-X-X-(Glu/Asp)). Many of these sites
overlap with the sites for casein kinase I, and 13 sites are specific
for casein kinase II. It is plausible that the overlapping sites ensure
the phosphorylaion of specific phosphophoryn domains that may be
crucial to collagen and/or calcium binding activities during
dentinogenesis (2, 4, 7, 9, 11, 12, 13) (see Fig. 2). For example,
Ser154, once phosphorylated, becomes the primary target
site of casein kinase II and enables the phosphorylation of
Ser151. Following this mechanism, the casein kinase II
could then phosphorylate the following 17 serines (spaced every two
amino acids upstream from Ser151) ending at
Ser103 (2a-2r in Fig. 2). Overlapping kinase I
and II activities within this Ser-rich domain (103-154) could
therefore provide a ``safeguard'' mechanism to ensure the
phosphorylation of this particular domain. There are, in total, 55 potential casein kinase II sites of which 37 sites overlap with casein
kinase I.
Overall, 78% of the Ser residues (81 out of 103) could potentially
become phosphorylated by casein kinases I and/or II. This number is
consistent with the reported 85-87% of phosphorylated Ser residues in
native phosphophoryn (2, 21). With this number of phosphoserines,
phosphophoryn would carry an additional charge of 130 from phosphate
groups alone (i.e. 1.6/Ser(P) or Thr(P)). Furthermore, if
3 of the 9 Thr residues are phosphorylated by casein kinase II, the
charge from the combined phosphoserine and phosphothreonine residues
would be 134. Therefore, phosphophoryn would carry an overall net
charge of 213 at physiological pH. Such a molecule would have a
very high capacity for binding divalent cations such as calcium
and magnesium, as reported for phosphophoryn (2, 7, 8, 21).
Potential N-Glycosylation Site
Seven potential
N-glycosylation sites (Asn-Xaa-(Ser/Thr)) (31, 32) are
present in this novel dentin protein at amino acid positions 31, 37, 69, 170, 202, and 261 (Fig. 1). Because of the overlap of potential
casein kinase sites and N-glycosylation sites, only
positions 31 and 37 are likely to be glycosylated. The other sites
would more likely be subjected to phosphorylation of Ser residues.
Northern Blot Analysis
We examined newborn rat tooth germs
for putative phosphophoryn mRNA expression. To eliminate the DSP
DNA sequence, we constructed a cDNA probe for 32P
random primer labeling containing only the phosphophoryn DNA sequence
(i.e. from nucleotide position 208). Northern blot analysis
indicated that multiple 4.6-kb transcripts were detected in the newborn
tooth germs (Fig. 3). Therefore, transcripts for the
putative phosphophoryn are expressed in the rat tooth germs.
Fig. 3.
Northern blot analysis. Total RNA
isolated from newborn rat tooth germs was subjected to Northern blot
analysis (see ``Experimental Procedures'') and then probed using a
32P-cDNA probe containing only the phosphophoryn DNA
sequence (i.e. from nucleotide position 208). Multiple
transcripts for putative phosphophoryn were detected near 4.6 kb in the
newborn rat tooth germs.
[View Larger Version of this Image (67K GIF file)]
DISCUSSION
During the process of analyzing the 3 end of an
odontoblast-specific cDNA which codes for dentin sialoprotein (15),
we discovered an open reading frame with a size of 801 bp. Our newly
discovered cDNA was found to encode a novel rat dentin protein
whose characteristics are in solid agreement with the following
reported features for phosphophoryn: (i) the predicted
NH2-terminal amino acid sequence (i.e.
Asp-Asp-Pro-Asn) is identical to that derived from protein
microsequencing for one form of rat phosphophoryn (25), (ii) the six
NH2-terminal amino acid sequence (i.e.
Asp-Asp-Pro-Asn-Ser-Ser) obtained from our putative phosphophoryn (Fig.
1) agrees with that reported by Reynolds and co-workers (33)
(i.e. Asp-Ser(P)-Pro-Asn-Ser(P)-Ser(P)) for bovine
phosphophoryn, (iii) amino acid sequences of Asp-Ser and Asp-Ser-Ser
were found interspersed in our putative rat phosphophoryn.
Additionally, a sequence of Asp-Ser-Ser-Ser-Ser was identified in our
putative protein. These sequence combinations of Asp-Ser, Asp-Ser-Ser,
and Asp-Ser-Ser-Ser were also observed in the NH2-terminal
50 residues of bovine phosphophoryn (33), and (iv) its deduced amino
acid composition contained high percentages of Ser (43%) and Asp
(31%) residues which coincided with the amino acid composition of
phosphophoryns from human, bovine, rat, and rabbit (i.e. Asp
(~30-40%) and Ser (~38-50%)) (2, 16, 17, 18, 19, 20, 21).
Phosphophoryn is the most acidic protein so far discovered. The
interspersed arrangement of Ser and Asp residues enables phosphophoryn
to be an excellent substrate for casein kinases I and II
phosphorylation action. The 78% of Ser residues in this protein which
can potentially be phosphorylated coincide with the reported 85-87%
of Ser(P) in authentic phosphophoryn (21). As discussed previously (see
``Results''), many of these phosphorylation reactions occur at
secondary and tertiary Ser sites and therefore result from a
phosphorylation cascade-type mechanism involving casein kinases I and
II operating over similar domains but in opposite directions to ensure
complete phosphorylation within these specific Ser-rich domains.
Roach and co-workers (34, 35, 36) have reported that threonine can also
serve as a substrate for casein kinase I. Based on this information,
all 9 threonine residues and an additional 10 serine residues could
also be phosphorylated. This mechanism could enable the sequential
phosphorylation of a 47-residue acidic patch extending from
Ser96 to Ser142. In this case, 88% of the Ser
residues (91 out of 103) could potentially become phosphorylated by
casein kinases I and/or II.
The full phosphorylation of the presumed phosphorylatable serines in
phosphophoryn therefore leads to the generation of many acidic patches
consisting of (DD)n, (pSpS)n, (pSD)n repeat
units. Furthermore, it was reported that bovine phosphophoryn can
undergo a conformational folding in the presence of Cd(II) and a
pH-dependent conformational folding (37, 38). These folding
experiments, suggesting that bovine phosphophoryn was comprised of
(DD)n, (pSpS)n, and (pSD)n structures arranged
into polyelectrolytic cluster regions (37), are in agreement with the
predicted (DD)n, potential (pSpS)n, and (pSD)n
acidic patches shown for our putative phosphophoryn (Fig. 2). Taken
together, our deduced acidic protein likely represents one form of rat
phosphophoryn.
By using a cDNA probe containing only the phosphophoryn DNA
sequence beginning from position 208, we determined by Northern blot
analysis whether this putative phosphophoryn cDNA was indeed
transcribed in tooth germ. Multiple transcripts, sized around 4.6 kb,
were detected (Fig. 3). The presence of multiple phosphophoryn
transcripts may be due to more than one phosphophoryn gene or due to
alternative splicing. However, it is equally likely that these multiple
transcripts are due to the use of multiple polyadenylation signals,
similar to many other mRNAs encoding extracellular matrix proteins.
Further experiments are needed to determine the origin of these
multiple transcripts. However, our Northern blot strongly suggests that
the putative phosphophoryn mRNA was present in the rat tooth germ
total RNA pool. Therefore, the DNA sequence for this novel protein is
unlikely to be an artifact. Taken together, we strongly feel that rat
tooth germs do actively synthesize the mRNA of this putative
phosphophoryn.
The presence of both DSP and phosphophoryn DNA sequences in the PCR
product could be due to an artifact generated during reverse
transcription-PCR or subsequent cloning processes. However, the
possibility of a bicistronic gene could not be excluded. Further work,
such as the examination of these two genes at the genomic level, is
needed to investigate these possibilities.
FOOTNOTES
*
This work was supported by National Institutes of Health
Grant DE11442-01 (to H. H. R.). The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
``advertisement'' in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) U63111[GenBank].
§
To whom correspondence should be addressed: BB135, Dept. of
Pediatrics, the University of Iowa, Iowa City, IA 52242. Tel.:
319-353-2055; Fax: 319-335-4489; E-mail:
dritchie{at}tic-po.tic.uiowa.edu.
1
The abbreviations used are: HAP, hydroxyapatite;
DSP, dentin sialoprotein; NCP, noncollagenous protein; bp, base
pair(s); kb, kilobase(s); PCR, polymerase chain reaction.
Acknowledgment
We thank Dr. David G. Ritchie for helpful
discussion and contributions during the preparation of this
manuscript.
REFERENCES
-
Veis, A.
(1978)
Ions in Macromolecular and Biological Systems
(Everett, D. H.,
Vincent, B.,
eds)
, p. 259, Scientichnia, Bristol, UK
-
Veis, A.
(1985)
Chemistry and Biology of Mineralized Tissues
(Butler, W. T.,
eds)
, p. 170, EBSCO Media, Birmingham,
AL
-
Linde, A.,
Goldberg, M.
(1993)
Crit. Rev. Oral Biol. Med.
4,
679-728
[Abstract/Free Full Text]
-
Butler, W. T., and Ritchie, H. H. (1995) Int. Dev. Biol.
39, 169-179
-
Weinstock, M.,
Leblond, C. P.
(1973)
J. Cell Biol.
56,
838-845
[Free Full Text]
-
Rahima, M.,
Tsay, T.-G.,
Andujar, M.,
Veis, A.
(1988)
J. Histochem. Cytochem.
36,
153-157
[Abstract]
-
Marsh, M. E.
(1989)
Biochemistry
28,
346-352
[CrossRef][Medline]
[Order article via Infotrieve]
-
Marsh, M. E.
(1989)
Biochemistry
28,
339-345
[CrossRef][Medline]
[Order article via Infotrieve]
-
Linde, A.,
Lussi, A.,
Crenshaw, M. A.
(1989)
Calcif. Tissue Int.
44,
286-295
[Medline]
[Order article via Infotrieve]
-
Lussi, A.,
Crenshaw, A.,
Linde, A.
(1988)
Arch. Oral Biol.
33,
685-691
[CrossRef][Medline]
[Order article via Infotrieve]
-
Boskey, A. L.,
Muresca, S.,
Doty, S.,
Sabsay, B.,
Veis, A.
(1990)
Bone Miner.
11,
55-65
[CrossRef][Medline]
[Order article via Infotrieve]
-
Stetler-Stevenson, W.,
Veis, A.
(1986)
Calcif. Tissue Int.
38,
135-141
[Medline]
[Order article via Infotrieve]
-
Fujisawa, R.,
Kuboki, Y.
(1992)
Calcif. Tissue Int.
51,
438-442
[CrossRef][Medline]
[Order article via Infotrieve]
-
Traub, W.,
Jodaikin, A.,
Arad, T.,
Veis, A.,
Sabsay, B.
(1992)
Matrix
12,
197-201
[Medline]
[Order article via Infotrieve]
-
Ritchie, H. H.,
Hou, H.,
Veis, A.,
Butler, W. T.
(1994)
J. Biol. Chem.
269,
3698-3702
[Abstract/Free Full Text]
-
Richardson, W. S.,
Beegle, W. F.,
Butler, W. T.,
Munksgaard, E. C.
(1977)
J. Dent. Res.
56,
233-237
[Abstract/Free Full Text]
-
DiMuzio, M.,
Veis, A.
(1978)
Calcif. Tissue Res.
225,
169-178
-
Termine, J.,
Belcourt, A.,
Miyamoto, M. S.,
Conn, K. M.,
Nylen, M.
U.
(1980)
J. Biol. Chem.
255,
9769-9772
[Abstract/Free Full Text]
-
Stetler-Stevenson, W.,
Veis, A.
(1983)
Biochemistry
22,
4326-4335
[CrossRef][Medline]
[Order article via Infotrieve]
-
Takagi, Y.,
Veis, A.
(1984)
Calcif. Tissue Int.
36,
259-265
[CrossRef][Medline]
[Order article via Infotrieve]
-
Linde, A.
(1985)
Chemistry and Biology of Mineralized Tissues
(Butler, W. T.,
eds)
, p. 344, EBSCO Media, Birmingham,
AL
-
Sambrook, J.,
Fritsch, E. F.,
Maniatis, T.
(1989)
Molecular Cloning: A Laboratory Manual
, 2nd Ed.
, Cold Spring Harbor
Laboratory, Cold Spring Harbor, NY
-
Sanger, F.,
Nicklen, S.,
Coulson, A. R.
(1977)
Proc. Natl. Acad. Sci. U. S. A.
74,
5463-5467
[Abstract/Free Full Text]
-
Kozak, M.
(1986)
Cell
44,
283-292
[CrossRef][Medline]
[Order article via Infotrieve]
-
Butler, W. T.,
Bhown, M.,
DiMuzio, M. T.,
Cothran, W. C.,
Linde, A.
(1983)
Arch. Biochem. Biophys.
225,
178-186
[CrossRef][Medline]
[Order article via Infotrieve]
-
DiMuzio, M. T.,
Veis, A.
(1978)
J. Biol. Chem.
253,
6845-6852
[Free Full Text]
-
Munksgaard, E.,
Richardson, W.,
Butler, W. T.
(1978)
Arch. Oral. Biol.
23,
583-585
[CrossRef][Medline]
[Order article via Infotrieve]
-
Wu, C.,
Pelech, S.,
Veis, A.
(1992)
J. Biol. Chem.
267,
16588-16594
[Abstract/Free Full Text]
-
Pinna, L.
(1990)
Biochim. Biophys. Acta
1054,
267-284
[Medline]
[Order article via Infotrieve]
-
Tuazon, P.,
Traugh, J.
(1991)
Adv. Second Messenger Phosphoprotein Res.
23,
123-164
[Medline]
[Order article via Infotrieve]
-
Marshall, R.
(1972)
Annu. Rev. Biochem.
41,
673-702
[CrossRef][Medline]
[Order article via Infotrieve]
-
Bause, E.
(1983)
Biochem. J.
209,
331-336
[Medline]
[Order article via Infotrieve]
-
Crossley, M. A.,
Huq, N. L.,
Kirszbaum, L.,
Reynolds, E. C.
(1996)
J. Dent. Res.
75,
154
-
Flotow, H.,
Roach, P. J.
(1989)
J. Biol. Chem.
264,
9126-9128
[Abstract/Free Full Text]
-
Flotow, H.,
Graves, P. R.,
Wang, A.,
Fiol, C. J.,
Roeske, R. W.,
Roach, P. J.
(1990)
J. Biol. Chem.
265,
14264-14269
[Abstract/Free Full Text]
-
Flotow, H.,
Roach, P. J.
(1991)
J. Biol. Chem.
266,
3724-3727
[Abstract/Free Full Text]
-
Evans, J.,
Chiu, T.,
Chan, S.
(1994)
Biopolymers
34,
1359-1375
[CrossRef][Medline]
[Order article via Infotrieve]
-
Evans, J.,
Chan, S.
(1994)
Biopolymers
34,
507-527
[CrossRef][Medline]
[Order article via Infotrieve]
-
Meggio, F.,
Marchiori, F.,
Borin, G.,
Chessa, G.,
Pinna, L. A.
(1984)
J. Biol Chem.
259,
14576-14579
[Abstract/Free Full Text]
-
Kuenzel, E.,
Mulligan, J. A.,
Summercorn, J.,
Krebs, E. G.
(1987)
J. Biol. Chem.
262,
9136-9140
[Abstract/Free Full Text]
-
Meggio, F.,
Perich, J. W.,
Meyer, H. E.,
Hoffmann-Posorske, E.,
Lennon, D. P. W.,
Johns, R. B.,
Pinna, L. A.
(1989)
Eur. J. Biochem.
186,
459-464
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.

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Copyright © 1996 by the American Society for Biochemistry and Molecular Biology.
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