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CRITICAL REVIEWS IN ORAL BIOLOGY & MEDICINE

SCPP Gene Evolution and the Dental Mineralization Continuum

K. Kawasaki and K.M. Weiss*

Department of Anthropology, Pennsylvania State University, 409 Carpenter Building, University Park, PA 16802, USA

Correspondence: * corresponding author, kenweiss{at}psu.edu


   ABSTRACT
TOP
 ABSTRACT
(I) INTRODUCTION
 (II) SCPP GENE FAMILY
 (III) ENAMEL, ENAMELOID, AND...
 (IV) DENTIN AND BONE
 (V) CONCLUDING REMARKS
 REFERENCES
 
Many genes critical to vertebrate skeletal mineralization are members of the secretory calcium-binding phosphoprotein (SCPP) gene family, which has evolved by gene duplication from a single ancestral gene. In humans, mutations in some of these SCPP genes have been associated with various diseases related to dentin or enamel hypoplasia. Recently, systematic searches for SCPP genes of various species have allowed us to investigate the history of phylogenetically variable dental tissues as a whole. One important conclusion is that not all disease-associated SCPP genes are present in tetrapods, and teleost fish probably have none, even in toothed species, having acquired their complement of SCPP genes through an independent duplication history. Here, we review comparative analyses of mineralized dental tissues, with particular emphasis on the use of SCPPs, within and between tetrapods and teleosts. Current knowledge suggests a close relationship among bone, dentin, teleost fish enameloid (enamel-like hard tissue), and tetrapod enamel. These tissues thus form a mineralized-tissue continuum. Contemporary dental tissues have evolved from an ancestral continuum through lineage-specific modifications.

Key Words: enamel • enameloid • dentin • bone • evolution • teeth • tooth


   (I) INTRODUCTION
TOP
 ABSTRACT
 (I) INTRODUCTION
(II) SCPP GENE FAMILY
 (III) ENAMEL, ENAMELOID, AND...
 (IV) DENTIN AND BONE
 (V) CONCLUDING REMARKS
 REFERENCES
 
The vertebrate tooth consists of 3 principal mineralized tissues: a hard surface enamel or enameloid, body dentin, and supportive attachment bone (Hall, 2005b). These tissues form on an extracellular matrix (ECM) containing distinct sets of proteins (Butler et al., 2003; Veis, 2003; Bartlett et al., 2006). Mutations in the genes coding the ECM proteins have been known to underlie human diseases, including dentin dysplasia (DD), dentinogenesis imperfecta (DGI), and amelogenesis imperfecta (AI). Among many non-syndromic forms of these diseases, mutations in the dentin sialophosphoprotein (DSPP) gene have been associated with both DD and DGI, and mutations in the amelogenin (AMEL) gene and the enamelin (ENAM) gene have been associated with AI (Stephanopoulos et al., 2005; MacDougall et al., 2006; Hart and Hart, 2007; Hu et al., 2007; Kim and Simmer, 2007). While these facts show the importance of these genes in dental tissue mineralization, the human tooth is not the only kind of tooth, which raises questions about the origin of human teeth and the use of animal models to study them. For example, not all of these human disease-associated genes are present in all tetrapod lineages and probably none in teleost fish, even though they have teeth with very similar structures (Kawasaki et al., 2005). To address diversity in distinct mineralized dental tissues within and between vertebrate species, we review here comparative studies of these tissues, with particular emphasis on ECM protein genes, whose expression and use reflect an interesting evolutionary history.

Paleozoic jawless vertebrates (Agnatha) had a structure similar to that of the tooth (Fig. 1Go); some of their dermal skeleton (head shield and body armor) consisted of tubercles or denticles, containing tissues comparable with those of teeth, along with underlying bony plates (Ørvig, 1977; Schaeffer, 1977; Reif, 1982; Smith and Hall, 1990; Smith and Coates, 2000; Donoghue and Sansom, 2002). This fossil evidence has led to the theory that teeth evolved from these ancient structures, co-opting them for feeding uses. The evolution of dental tissues is important to our understanding of vertebrate phylogeny in general, and is relevant to the investigation of dental development and perhaps even therapeutics. However, the story is complicated (Ørvig, 1967; Smith and Sansom, 2000; Donoghue et al., 2006). For instance, ’enameloid’, enamel-like hard tissue, covers the tooth surface in both teleosts and sharks. It has been reported that shark enameloid is distinct from teleost enameloid in its organic content, mechanism of mineralization, and the role of the epithelial cells, but other investigators argue that the differences between these two tissues are the result of lineage-specific divergence from a shared primitive state (Sasagawa, 2002; Gillis and Donoghue, 2007). Unfortunately, the molecular basis of tissue mineralization is largely unknown for cartilaginous fish (Chondrichthyes). In contrast, we have recently reported that a series of proteins forming the Secretory Calcium-binding Phospho-Protein (SCPP) family is crucial to skeletal mineralization in both teleosts and tetrapods (Kawasaki and Weiss, 2003, 2007; Kawasaki et al., 2005). Here, we will introduce the genes in the SCPP family (Section II), and then discuss their role in diversity within dental tissues, particularly in the two major vertebrate lineages, teleosts and tetrapods (Sections III and IV). The status of SCPP gene presence in other bony fish (Osteichthyes) as well as in cartilaginous fish remains to be known but is under investigation.


Figure 1
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  		Figure 1. Vertebrate phylogeny and the evolution of skeletal mineralization. Many extinct vertebrates (dashed lines) split from our ancestral lineage after the modern jawless vertebrates (lampreys and hagfish), but before cartilaginous fish (Chondrichthyes). The most ancient mineralized tissue has been found in conodonts. Subsequent jawless vertebrates evolved a dermal skeleton. The tooth arose before the divergence of cartilaginous fish. Two WGDs are thought to have taken place, first, in the stem jawless vertebrates (WGD1) and, second, in the stem jawed-vertebrates (WGD2). SPARCL1 arose from SPARC through the WGD2. SCPP genes originated from SPARCL1, but have been found only in teleosts and tetrapods to date. The initial SCPP gene arose before the divergence of ray-finned fish and lobe-finned fish. The vertebrate phylogeny is based on Donoghue et al.(2006).

 

   (II) SCPP GENE FAMILY
TOP
 ABSTRACT
 (I) INTRODUCTION
 (II) SCPP GENE FAMILY
(III) ENAMEL, ENAMELOID, AND...
 (IV) DENTIN AND BONE
 (V) CONCLUDING REMARKS
 REFERENCES
 
(a) SCPP Genes
Type-I collagen (COL1) fibrils serve as the mineralization scaffold for bone, dentin, and teleost enameloid. However, collagen alone cannot initiate mineralization; many non-collagenous ECM proteins and other molecules cooperate to regulate tissue mineralization (Bonucci, 1992). We have previously shown that many of these proteins are evolutionarily related, and form the SCPP family. The SCPP genes arose through a history of iterative gene duplication, descending from a single common ancestral gene (Kawasaki et al., 2004, 2007). In humans, DSPP, DMP1 (dentin matrix acidic phosphoprotein 1), IBSP (integrin-binding sialoprotein), MEPE (matrix extracellular phosphoglycoprotein), and SPP1 (secreted phosphoprotein 1) belong to this family (TableGo) (Kawasaki and Weiss, 2007). A subfamily of these proteins has also been called SIBLINGs (Fisher et al., 2001), but we refer to them as dentin/bone, or acidic SCPPs, based on the localization patterns of their coded proteins, their principal biochemical characteristics, and their membership in the larger SCPP family.


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  		Table. Human SCPP Genes
 
Another subfamily is enamel SCPPs, including AMEL, ENAM, AMBN (ameloblastin), AMTN (amelotin), and ODAM (odontogenic, ameloblast associated), all involved in enamel formation [see Section III(b) for the classification of AMTN and ODAM]. The enamel SCPPs have additional relatives, milk caseins and some salivary proteins (Kawasaki and Weiss, 2006). These proteins include CSN1S1 ({alpha}s1-casein), CSN2 (β-casein), STATH (statherin), HTN1 (histatin 1), HTN3 (histatin 3), LOC401137 (hypothetical protein LOC401137), FDCSP (follicular dendritic cell secreted peptide), CSN3 ({kappa}-casein), PROL5 (proline-rich 5), PROL3 (proline-rich 3), PROL1 (proline-rich 1), and MUC7 (mucin 7) (TableGo). With the exception of histidine-rich HTN1 and HTN3, these milk/saliva/enamel SCPPs all have many Pro and Gln residues; thus, we also call these proteins P/Q-rich SCPPs.

SCPPs are all secreted from the cells where they are produced. Many then directly associate with calcium ions, and most have at least one, usually many, calcium-binding phospho-Ser residues (Kawasaki and Weiss, 2003). The amino acid sequence identity among different SCPPs is limited, usually detectable only in the signal peptide (a short N-terminal stretch, leading the mature protein to the extracellular domain or cell membrane), but not in the remaining functional regions of the SCPPs. For many years, this made it difficult to identify SCPP genes or demonstrate that they were a single gene family. However, when we used criteria that also include the common exon-intron structure of SCPP genes, their close evolutionary relationship became clear (for details, see Kawasaki et al., 2004; Kawasaki and Weiss, 2007). In addition, with the exception of AMEL, which resides on the sex chromosomes, all the human SCPP genes form 2 gene clusters: one consisting of 5 acidic SCPP genes, and the other 16 P/Q-rich SCPP genes, with the clusters separated by a 17-megabase region on chromosome 4 (Fig. 2Go). This configuration is conserved across most mammalian species (Huq et al., 2005; Kawasaki et al., 2007).


Figure 2
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  		Figure 2. SCPP gene clusters in the human (A), chicken (B), frog (C), fugu (D), and zebrafish (E) genomes. Location and transcriptional orientation of SPARCL1 (open box), P/Q-rich SCPP (closed box), acidic SCPP (shaded box), and ARHGAP6 (dashed-line box) genes are schematically illustrated. (A,C) AMEL is located within ARHGAP6 on human chromosome X and in the frog genome. (A) Two large SCPP gene clusters, enamel/milk/saliva and dentin/bone classes, are separated by 17 megabases (Mb). (D) Linkage of SPP1 and the other SCPP genes is unknown. (E) SPP1 and the other SCPP genes reside on different chromosomes. SCPP2-SCPP5 and SPARCL1-SCPP1 clusters are separated by 10 Mb by an intrachromosomal re-arrangement. These results are based on the following sequence assemblies: hg18 (human), galGal3 (chicken), xenTrop2 (frog), fr2 (fugu), and danRer5 (zebrafish).

 
This shared exon-intron structure has been found only in the SCPP genes and 2 closely related genes that are the ancestors of the SCPP genes, SPARC (secreted protein, acidic, cysteine-rich; also called osteonectin) and SPARCL1 (SPARC-like 1 protein) (Kawasaki et al., 2004). These genes both code multifunctional ECM proteins (Yan and Sage, 1999; Sullivan and Sage, 2004). SPARC is known to be a major non-collagenous protein in dentin and bone, whereas SPARCL1 is more abundant in nerve tissues (Termine et al., 1981; Mothe and Brown, 2001; Chun et al., 2006). SPARC and SPARCL1 both consist of the signal peptide and 3 functional modules, known as domain-I, -II, and -III, of which exons coding domain-I and the upstream region have the common structure characteristic of SCPP genes. Moreover, SPARCL1 is located adjacent to the acidic SCPP gene cluster (Fig. 2Go), while SPARC resides on a different chromosome. From these shared characteristics, we concluded that the SCPP genes initially arose from a 5' region of SPARCL1 that had earlier originated from SPARC (see below) (Kawasaki et al., 2004).

(b) SCPP Evolution by Gene Gain-and-Loss
It has become clear that the gain-and-loss (or birth-and-death) of genes in gene families has played a significant role in the evolution of both the genome and its diversified functions, especially when family members are tandemly arrayed in chromosome clusters (Nei and Rooney, 2005). This is the case for the SCPP genes, of which we have identified a total of 22 in the human genome (TableGo). While the milk/saliva SCPP genes have been found only in mammals, and their number and repertoire vary across species, dentin/bone and enamel SCPP genes are more stable among the known tetrapod whole-genome sequences. The genome sequences of non-placental mammals are tentative (Mikkelsen et al., 2007), but our analysis identified either all or portions of dentin/bone or enamel SCPP genes in the opossum (DSPP, DMP1, IBSP, MEPE, SPP1, AMEL, ENAM, AMBN, AMTN, FDCSP, and ODAM in version monDom4) and in the duckbilled platypus (DSPP, DMP1, IBSP, SPP1, AMEL, ENAM, AMBN, AMTN, and ODAM in ornAna1).

In the chicken genome, 3 dentin/bone SCPP genes, DMP1, IBSP, and SPP1, are clustered with a major eggshell matrix protein gene, OC116 (ovocleidin 116), which is orthologous to mammalian dentin/bone-class MEPE (Fig. 2Go) (Kawasaki and Weiss, 2006). However, no enamel-class SCPP genes or DSPP has been identified in the chicken genome. Because we have identified AMEL, ENAM, AMBN, AMTN, and DSPP genes in the lizard genome (Anolis carolinensis; version anoCar1), these SCPP genes, mainly used for enamel or dentin, apparently have been lost from the bird genome, probably after the ancestors of modern birds lost teeth in the Late Cretaceous period (Zhou, 2004).

In the frog (Xenopus tropicalis) genome, P/Q-rich AMBN is located near the acidic SCPP gene cluster consisting of DMP1 and IBSP (Fig. 2Go). This suggests that the 2 types of SCPP genes were originally located adjacent to each other, but were split by an intrachromosomal re-arrangement in the lineage leading to mammals. Frog AMEL resides within an intron of the Rho GTPase activating protein 6 gene (ARHGAP6) on a chromosome different from that in mammalian genomes, suggesting that AMEL was translocated from the ancient SCPP gene cluster before the divergence of amniotes and anamniotes (Fig. 2Go) (Iwase et al., 2007).

An SPP1 ortholog has been identified in the zebrafish and trout (Bobe and Goetz, 2001; Kawasaki et al., 2004), as well as in fugu, medaka, stickleback, sea bream, and fathead minnow (Fonseca et al., 2007). Although SPP1 and the ancestral SPARCL1 remain in a linked chromosomal region in tetrapod genomes, these 2 genes appear to be separated by an interchromosomal re-arrangement in these teleost fish (Fig. 2Go). In addition to SPP1, we identified 7 fugu SCPP genes that, based on sequence and feature analysis, are apparently not orthologous to any tetrapod genes (Kawasaki et al., 2005). These genes are clustered around SPARCL1: acidic SCPP1 upstream of SPARCL1, and P/Q-rich SCPP2, SCPP3A, SCPP3B, SCPP3C, SCPP4, and SCPP5 downstream of SPARCL1 (Fig. 2Go). Our comparative genome analysis suggests that the arrangement of these 2 subfamilies of SCPP genes arose in the common ancestor of teleosts and tetrapods (Kawasaki et al., 2007). In the zebrafish genome, we identified only 4 genes—SCPP1, SCPP2, SCPP5, and SPP1—orthologous to fugu SCPP genes. Among these zebrafish genes, SCPP1 is clustered with SPARCL1 and SCPP2 with SCPP5, but these 2 clusters are 10 megabases apart on a single chromosome, presumably by an intrachromosomal rearrangement (Fig. 2Go). Many of these teleost SCPP genes are expressed in dental tissues, as will be described later (Fig. 3Go).


Figure 3
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  		Figure 3. Tooth formation. (A) Tooth with enamel. Through the reciprocal interactions between dental epithelial cells and the underlying ectomesenchymal cells, odontoblasts (Od) develop from the ectomesenchymal cells. As odontoblasts retreat centripetally (shaded arrow), these cells deposit the ECM proteins for dentin between the odontoblast layer and the dental epithelial cell layer. Subsequently, ameloblasts (Am), now fully differentiated from the dental epithelial cells, lay down the ECM proteins for enamel on the mineralizing dentin surface. Enamel thus grows centrifugally away from the pulp (closed arrow). As enamel grows to its final thickness, enamel structural proteins are degraded and resorbed by ameloblasts, and further deposition of calcium and phosphates facilitates enamel maturation. (B) Tooth with enameloid. The histogenesis of teleost teeth is considerably different from that of tetrapod teeth covered with enamel. Initially, the ECM proteins for enameloid, not dentin, are secreted by both the inner dental epithelial (IDE) cells and odontoblasts and deposited below the basal lamina abutting the IDE cells (closed arrow). While the activity of the IDE cells diminishes, odontoblasts continue to retreat centripetally (shaded arrow) and deposit ECM proteins for dentin. Major ECM proteins secreted by ameloblasts, odontoblasts, and the IDE cells are shown at the bottom. Note that the deposition of AMTN and ODAM is known only at the enamel maturation stage.

 
(c) The Origin of the SCPP Family
Because SPARCL1 is the last common ancestor of the SCPP gene family, the origin of this gene is relevant to the evolution of vertebrate skeletal mineralization. Our phylogenetic analysis of SPARC and SPARCL1 suggested that these 2 genes split in an early vertebrate after the divergence of lampreys, but before sharks (Fig. 1Go) (Kawasaki et al., 2007). Using a molecular clock estimate, Sire and his colleagues calculated the divergence date of AMBN and AMEL to be more than 600 million years ago in the Precambrian period, and they estimated the origin of SPARCL1 to be earlier than this date (Delgado et al., 2001; Sire et al., 2005, 2007). Unfortunately, the result of our phylogenetic analysis cannot be directly compared with the geological timescale. However, our phylogenetic result is consistent with comparative analysis of the chromosomal regions around SPARC and SPARCL1 in the human genome. This suggests that these 2 genes split through 2 rounds of whole genome duplication (WGD). While SPARC and SPARCL1 have differentiated since the second round, 2 other duplicates were deleted from the genome (Kawasaki et al., 2007). The 2 rounds of WGD are thought to have taken place early in vertebrate evolution, and the second round has been estimated to have occurred after the origin of modern jawless vertebrates, hagfish and lampreys, but before the divergence of cartilaginous fish and bony fish (Fig. 1Go) (Ohno, 1970; Holland et al., 1994; Gu et al., 2002; McLysaght et al., 2002; Dehal and Boore, 2005; Meyer and Van de Peer, 2005).

Further, our estimate of the SPARC-SPARCL1 divergence date falls precisely in the interval in which mineralized skeleton is known, from the fossil record, to have emerged (Donoghue and Sansom, 2002; Janvier, 2003; Donoghue et al., 2006). We thus speculate that SPARCL1 arose from SPARC in vertebrates around the origin of skeletal mineralization (Fig. 1Go). The initial SCPP gene then arose before the divergence of ray-finned fish (Actinopterygii) and lobe-finned fish (Sarcopterygii), as shown by SPP1 found in both of these lineages. Subsequent tandem gene duplications have created many more SCPP genes around the ancestral SPARCL1; however, significant numbers of SCPP genes have also been deleted from the genome. This birth-and-death process, together with the fluid evolution of exon number, size, and protein coding sequence of SCPP genes, has resulted in many lineage-specific genes (Kawasaki et al., 2007). Thus, in an example of phenogenetic drift in evolution, mineralized teeth have long been maintained by selection in ray-finned fish and lobe-finned fish, while the underlying mineralization genes have changed considerably in the 2 lineages (Weiss and Fullerton, 2000; Weiss and Buchanan, 2004; Kawasaki et al., 2005). This whole story—the origin of skeletal mineralization and the 2 rounds of WGD, followed by the establishment of the SCPP gene family through sequential tandem gene duplication—is consistent with the view of the gradual acquisition of important vertebrate traits (Donoghue and Purnell, 2005).


   (III) ENAMEL, ENAMELOID, AND DENTIN
TOP
 ABSTRACT
 (I) INTRODUCTION
 (II) SCPP GENE FAMILY
 (III) ENAMEL, ENAMELOID, AND...
(IV) DENTIN AND BONE
 (V) CONCLUDING REMARKS
 REFERENCES
 
(a) The Development of Enamel and Enameloid
Enamel and enameloid are both highly mineralized, wear-resistant tissues covering dentin, and thus are thought to be functionally equivalent. Enamel forms on the ECM proteins deposited solely by epithelial cells, whereas enameloid refers non-specifically to any enamel-like tissues with the matrix secreted by both epithelial and mesenchymal cells (Poole, 1967; Huysseune and Sire, 1998).

Tetrapod teeth are covered with enamel, with the notable exceptions of the tooth of larval urodele, which is covered with enameloid, and of some toothed mammals (aardvark, armadillo, and sloth; and molars of dugong and sperm whale) that lost this tissue secondarily (Owen, 1844; Peyer, 1968; Smith and Miles, 1971; Kogaya, 1999; Davit-Béal et al., 2007). During the development of tetrapod teeth, ECM proteins for dentin are initially deposited by odontoblasts that originated from neural-crest-derived ectomesenchymal cells (Linde and Goldberg, 1993; Nanci, 2003). As dentin grows, odontoblasts lining the surface of the pulp retreat centripetally (Fig. 3Go). These retreating odontoblasts leave behind cell processes (odontoblast processes), which run through dentinal tubules extending from the dentino-enamel junction. After the initial mineralization of dentin, ameloblasts, the fully differentiated inner dental epithelial (IDE) cells, begin to deposit enamel ECM proteins (Fincham et al., 1999; Paine and Snead, 2005; Bartlett et al., 2006). Enamel thus grows centrifugally away from the pulp (Meinke and Thomson, 1983; Butler and Ritchie, 1995). During enamel maturation, proteinases actively secreted by ameloblasts degrade enamel ECM proteins (Bartlett and Simmer, 1999; Hu et al., 2002; Simmer and Hu, 2002). This process facilitates the active removal of enamel proteins and the subsequent growth of enamel crystallites. The enamel thus grows into highly mineralized, very hard tissue, devoid of organic components and consisting of virtually inorganic apatitic crystals (Carlson, 1990; Simmer and Fincham, 1995).

In contrast, the initial ECM proteins secreted during teleost fish tooth development are pre-enameloid, instead of predentin. Similar to enamel, these enameloid proteins are digested by proteinases, secreted by the IDE cells, and develop into a highly mineralized tissue (Kawasaki et al., 1987). After the enameloid matrix begins mineralization, the IDE cells continue to secrete proteins into the enameloid for a short period of time, while odontoblasts deposit ECM proteins for dentin (Shellis and Miles, 1974). The odontoblast cell processes thus originally extend from the basal lamina, beneath the IDE cells, but these processes gradually disappear, and radiating fibers take their place as enameloid begins to calcify (Kerr, 1960; Sasagawa, 1995). Due to continuous extensions of cell processes and fibers, the junction between enameloid and dentin is often less distinct than that between enamel and dentin (Shellis and Miles, 1974).

The tissue origin of the teleost enameloid scaffold, collagen fibrils, has long been a matter of controversy (Kvam, 1946, 1950; Kerr, 1960). By monitoring the pathway of radiolabeled amino acids, Shellis and Miles concluded that odontoblasts secrete collagen (Shellis and Miles, 1974). In contrast, ultrastructural studies by Prostak and Skobe detected secretory granules containing procollagen in the IDE cells, but not in odontoblasts. These authors concluded that the IDE cells synthesize and secrete enameloid matrix collagen (Prostak and Skobe, 1985, 1986). However, Sasagawa detected secretory granules also in odontoblasts, and suggested that both types of cells synthesize collagen fibrils (Sasagawa, 1995). Results of our investigation into the mineralization processes in teleost teeth at the molecular level allow us to compare tetrapod enamel and teleost enameloid, based on the characteristics of SCPPs used in these 2 tissues.

(b) Enamel Formation and SCPPs
The enamel matrix is continuously secreted from ameloblasts, self-assembled, processed, and mineralized, and thus is a forming matrix instead of a pre-formed matrix (Fincham et al., 1999; Moradian-Oldak and Goldberg, 2005). This characteristic mineralization process is distinct from that of other mineralizing tissues, including enameloid (Fearnhead, 1979; Bartlett et al., 2006), and is probably linked to the use of the SCPP-based, non-collagenous mineralization scaffold. Secreted AMEL self-assembles through hydrophobic interactions between and among the molecules, which results in the formation of thermodynamically stable structures. This structure appears to be the basic building block of the enamel ECM framework, regulating crystal spacing (Fincham et al., 1999).

AMEL consists of 3 distinct regions: the N-terminal tyrosine-rich region, a hydrophobic core region, and the C-terminal hydrophilic region, which is well-conserved among tetrapod species and has been thought to be important to the self-assembly of this molecule (Toyosawa et al., 1998; Snead, 2003; Sire et al., 2005; Margolis et al., 2006). In fact, the core region can be further divided into 2 portions: the N-terminal half, with dispersed Pro and Gln residues with a pattern of hydrophilicity and hydrophobicity alternating ca. every 5 amino acids; and the C-terminal half, with incomplete Pro-Xaa-Yaa repeats (where Xaa and Yaa indicate any amino acid in this position, although Gln and Pro appear frequently). Although the amino acid sequence of the hydrophobic core region varies among tetrapods, this characteristic structure, consisting of these 2 portions, is present in all known AMELs, but not in any other SCPPs found in tetrapods or teleosts.

As noted earlier, AMEL resides within an intron of ARHGAP6 in both mammals and frogs (Fig. 2Go). We found 2 ARHGAP6 or closely related genes in the zebrafish genome and 3 such genes in the fugu genome. However, no SCPP genes have been identified within these genes. These results suggest that AMEL is not present in the genomes of these teleost species.

Three enamel SCPPs—AMEL, AMBN and ENAM—have been referred to as the major structural proteins in developing mammalian enamel (Fincham et al., 1999; Hu et al., 2007). Of biomedical relevance is the fact that mutations in AMEL or ENAM have been associated with AI, and AMBN-null mice develop severe enamel hypoplasia (Hart et al., 2002; Hu and Yamakoshi, 2003; Wright et al., 2003; Fukumoto et al., 2004, 2005). Among these enamel SCPP genes, AMEL and AMBN have been found in all major tetrapod clades, whereas ENAM remains unidentified in amphibians (Fig. 2Go). We have reported that these proteins show a slight, but significant, sequence homology in the signal peptide and the N-terminal region of the mature protein, and all these genes code 1, or 2 overlapping, Ser-Xaa-Glu (SXE; Glu may be replaced by phospho-Ser or Asp) sequences at the 3'-end of a small exon (typically exon 3) (Kawasaki and Weiss, 2003). So far, no sequence similarity has been detected between the N-terminal mature protein of these enamel SCPPs and that of other known tetrapod or teleost SCPPs. In addition, both AMBN and ENAM have well-conserved short amino acid sequences, but none of these sequences has been found in teleost SCPPs (Kawasaki et al., 2005). These results suggest that no major enamel SCPP genes are present in the fugu genome, which is supported by our recent analysis of the zebrafish genome (unpublished). Significantly, among teleost SCPPs, SCPP2, involved in enameloid mineralization, has 2 overlapping SXE sequences coded at the 3'-end of small exon 3; that is, SCPP2 retains an ancient characteristic common to the major enamel SCPPs.

Because recent studies have revealed that both ODAM and AMTN are involved in enamel maturation, we tentatively refer to ODAM and AMTN as enamel SCPP genes (Iwasaki et al., 2005; Moffatt et al., 2006a,b, 2008; Park et al., 2007). ODAM was first purified from amyloid associated with human calcified epithelial odontogenic tumors (Solomon et al., 2003). No mutations in these 2 genes have yet been associated with AI (Hu et al., 2007). In addition to ameloblasts, ODAM is also expressed in lactating mammary glands, nasal and salivary glands, and gingiva (Rijnkels et al., 2003; Moffatt et al., 2008), but is similar to the major enamel SCPP genes in that this gene codes 3 contiguous SXE sequences at the end of small exon 3. In contrast, AMTN has no SXE at the equivalent position, although the expression is more specific to ameloblasts.

(c) Enameloid Formation and ECM Proteins
Among the fugu SCPP genes involved in enameloid mineralization, only SCPP2 and SCPP5 have been identified in zebrafish. SCPP2 in both fugu and zebrafish has an Arg-Gly-Asp integrin binding sequence, which is common in mammalian dentin/bone SCPPs, but uncommon in enamel SCPPs (Fisher et al., 2001). A strong expression of SCPP2 (and SCPP4) has been found only in the IDE cells. In contrast, SCPP5 is highly expressed in both the IDE cells and odontoblasts, unique among the SCPP genes known to date (Kawasaki et al., 2005). We have also detected strong expression of COL1 in both types of these cells. SPARC was recently proposed to play a role in collagen fibrillogenesis, not only in the ECM, but also within the cell, where SPARC ensures that only correctly folded procollagens exit the endoplasmic reticulum (Martinek et al., 2007). Consistent with this idea, we have detected the expression of SPARC in both the IDE cells and odontoblasts. We initially determined the expression patterns of these genes in fugu pharyngeal teeth, but we recently confirmed a similar pattern in zebrafish, which also have pharyngeal teeth, but which are phylogenetically distant from fugu among teleosts. Prostak et al. analyzed specialized fugu oral teeth, consisting largely of enameloid, and reported that the odontoblasts, less numerous than the IDE cells, also contained procollagen granules (Prostak et al., 1993). Suzuki et al. confirmed strong expression of COL1 in both the IDE cells and odontoblasts in the oral tooth of fugu (unpublished observations). These results all support the argument by Sasagawa (1995), that the IDE cells and odontoblasts both contribute to the production of collagen, although their proportion of collagen production may vary among teleost species.

(d) Enamel-Enameloid-Dentin as a Continuum
Fearnhead has suggested that there is convincing evidence that enameloid is a tissue ancestor to "true" enamel (Fearnhead, 1979). It has been proposed that, during teleost enameloid formation, odontoblasts secrete collagen, while the IDE cells lay down enameloid matrix proteins that are similar to mammalian enamel proteins (Shellis and Miles, 1974, 1976). The rationale behind this view is developmental heterochrony in the transition of enameloid to enamel: In tetrapods, the time at which the IDE begins to secrete protein has been delayed, so that enamel matrix is secreted only after the odontoblasts have produced and mineralized a layer of dentin (Shellis and Miles, 1974).

Conversely, it has been argued that enameloid evolved from enamel through a peramorphic process of heterochrony, a shift of epithelial activity to an earlier time to coincide with the initiation of dentin formation (Smith and Hall, 1990; Smith, 1992, 1995). This peramorphic hypothesis was supported by the ancient origin of enamel in conodonts, the stratigraphically earliest fossils of jawless vertebrates (Fig. 1Go). However, recent studies failed to find further supportive evidence for unequivocal enamel in other extinct or extant vertebrates, more closely related to bony fish (Janvier, 1996; Donoghue, 2001; Donoghue and Sansom, 2002; Donoghue et al., 2006). In contrast, enameloid has been identified from many vertebrates, including basal cartilaginous fish (Gillis and Donoghue, 2007). It is thus likely that the conodont enamel and the tetrapod enamel represent an interesting incidence of independent origin and functional convergence, and at present there is no strong support for the view that teleost enameloid was derived from the precursor of tetrapod enamel (Donoghue and Sansom, 2002).

Our findings only partially support the hypothesis by Shellis and Miles (1974): Teleost IDE cells indeed secrete enamel-protein-like proteins (SCPP2 and SCPP4), whereas these cells also deposit proteins common to dentin (COL1, SPARC, and SCPP5). It thus appears that the teleost IDE cell has a gene expression (or protein secretion) profile apparently intermediate between the odontoblast and the tetrapod ameloblast, and that the heterochrony hypothesis may not fully explain the evolutionary relationship between enameloid and enamel. Although some of the characteristics of teleost enameloid may have been secondarily derived in the ray-finned fish lineage, it seems that enamel-enameloid and enameloid-dentin are closely related in mode of mineralization, tissue origin, and constitutive proteins. This view is also supported by the observation of urodele tooth formation, in which successive dental epithelial cells are involved in both enameloid and enamel formation (Smith and Miles, 1971; Kogaya, 1999; Davit-Béal et al., 2007). This is all consistent with a previous hypothesis that the enamel/enameloid/dentin system forms a continuum of tissues that have diverged from one another (Meinke, 1982).


   (IV) DENTIN AND BONE
TOP
 ABSTRACT
 (I) INTRODUCTION
 (II) SCPP GENE FAMILY
 (III) ENAMEL, ENAMELOID, AND...
 (IV) DENTIN AND BONE
(V) CONCLUDING REMARKS
 REFERENCES
 
(a) At the Structural Level
Odontoblasts and osteoblasts both originate from neural crest cells (Hall, 1999). While the production of dentin is unique to neural-crest-derived cells, bone also arises from mesodermal tissues (Hall, 2005a). Typical dentin (orthodentin) is characterized by many sub-parallel, polarized single-cell processes extending from the cell body, located at the pulp surface, to the dentin-enamel junction (Smith and Sansom, 2000). These odontoblast cell processes are connected to one another through fine branches, forming a canalicular system (Nanci, 2003). In contrast, the osteocyte cell body is embedded in a lacuna within the matrix and extends radiating non-polarized cell processes, also forming a canalicular system. A recent study revealed a striking similarity in the morphological distribution of the canalicular system in dentin and attachment (alveolar) bone, suggesting that both systems may work similarly in mechanical signal transduction (Lu et al., 2007).

The average inorganic composition of human dentin and bone is estimated to be 70% and 65%, respectively (Carlson, 1990). However, the mineral density of bone varies considerably across species, anatomical sites, ages, and genders. It was reported that the density of fish bone (1.80 g/cm3) is considerably lower than that of rat (2.24 g/cm3), and that the range of bone density varies from 1.7 g/cm3 for deer antler to 2.7 g/cm3 for porpoise petrosal (Biltz and Pellegrino, 1969; Lees, 1987). The rostral bones of the toothed whale consist mainly of highly mineralized secondary osteons, with a remarkably sparse collagenous component (Lees, 1987; Zylberberg et al., 1998). The degree of mineralization (86.7% at the weight level) of this bone is much higher than that of human dentin (70%), showing that the mineral density can overlap between these 2 tissues. The mineral density also varies within dentin, which will be described later.

(b) The Evolving SCPP Contribution to Dentin and Bone
Dentin and bone use different compositional mixtures of the same ECM proteins. Among the 5 mammalian dentin/bone SCPPs, DSPP and DMP1 are especially rich in potentially phosphorylated Ser residues (George et al., 1993; Butler and Ritchie, 1995; Butler et al., 2003). DSPP is rapidly cleaved by proteinases into 3 domains, dentin sialoprotein (DSP), dentin glycoprotein, and dentin phosphoprotein (DPP) (Yamakoshi et al., 2005, 2006). These DSPP-derived proteins constitute the most abundant non-collagenous proteins in dentin. The expression of DSPP has also been detected in osteoblasts, and DSP has been found in the long bone of the rat (Qin et al., 2002). However, the amount of DSP is only 1/400 in bone relative to dentin. Mutations in DSPP have been associated with autosomal-dominant DD and DGI, but their known mutations have no effect other than in teeth, except for occasional association with hearing loss (Patel, 2001; Xiao et al., 2001; Zhang et al., 2001). Dmp1-null mice show tooth phenotypes strikingly similar to those of Dspp-null mice, and these mice share some pathological features of DGI (Sreenath et al., 2003; Ye et al., 2004). Immunohistochemical analysis revealed striking co-localization of DSPP and DMP1 during dentinogenesis, suggesting complementary and/or synergistic roles for these 2 proteins in the formation and maintenance of dentin (Baba et al., 2004). However, Dmp1-null mice are severely hypophosphatemic, and in humans the loss of DMP1 activity has been associated with autosomal-recessive hypophosphatemic rickets (no dentin defect has been reported) (Feng et al., 2006; Lorenz-Depiereux et al., 2006). Moreover, in addition to odontoblasts, strong expression of DMP1 has been detected in pre-osteocytes and osteocytes, but not in osteoblasts, suggesting that DMP1 is also important in bone homeostasis (Toyosawa et al., 2001, 2004; Qin et al., 2007). The pleiotropic roles of DMP1 may explain its maintenance in modern birds, whereas more specialized DSPP was secondarily lost after birds became toothless (Toyosawa et al., 2000).

We have reported the expression of fugu SCPP1 in odontoblasts (Kawasaki et al., 2005). Recently, we also identified weak expression of zebrafish SCPP1 in osteoblasts surrounding attachment bone. Whereas the molecular weight of teleost SCPP1 is approximately half that of tetrapod DMP1, their proportionate amino acid composition is surprisingly similar. Not only are they composed of 20–30% of acidic amino acids, common to other acidic SCPPs, but SCPP1 and DMP1 also contain an especially high proportion (10–20%) of potential phospho-Ser residues within SXE sequences (Qin et al., 2004). The extraordinarily high proportion of phospho-Ser residues is also a characteristic of DPP (Veis and Perry, 1967), one of the DSPP-derived proteins, suggesting that a high proportion of phospho-Ser residues plays a distinct role in dentin mineralization. Despite these similarities, teleost SCPP1 is not apparently orthologous to tetrapod DMP1 or DPP (Kawasaki et al., 2005). Moreover, only SPP1 has been found in both tetrapods and teleosts, as we describe next. We assume that, while current dentin/bone SCPP genes have taken over part of the functions of ancient acidic SCPP genes, they also evolved new functions independently. This idea will be tested experimentally.

The expression of SPP1 has also been found in many soft tissues, and mice deficient in SPP1 have severely impaired cell-mediated immunity (Ashkar et al., 2000; Sodek et al., 2000). In bone, the Spp1-deficient mice show an increased amount of mineral and crystal size, suggesting that SPP1 is a potent inhibitor of mineral crystal growth (Boskey et al., 2002). In the developing calvaria, the expression of SPP1 was detected at an especially high level in osteoblasts only on the endocranial surface, showing that the expression level of this gene varies among osteoblasts (Candeliere et al., 2001). Despite these pleiotropic functions, SPP1 has not yet been found in the frog genome, even though teleosts have this gene (Fig. 2Go). In mammals, SPP1 has been detected in dentin extracts at a level either less than one-tenth or 1/70th of bone (Fujisawa et al., 1993; Qin et al., 2001). Consistent with this, we detected strong expression of zebrafish SPP1 in osteoblasts surrounding attachment bone, and marginal expression in odontoblasts, both in contrast to the expression levels of SCPP1 as described above. In addition, an up-regulated expression of SPP1 has been reported in an osteoblast-like cell line of the gilthead sea bream after the induction of ECM mineralization (Fonseca et al., 2007). These observations suggest some conserved function of this protein in dentin and bone mineralization between teleosts and mammals, despite their divergent amino acid sequences.

It has been reported that the expression of IBSP is strong in osteoblasts but weak in odontoblasts, and that the amount of IBSP is ~ 10 times more abundant in bone than in dentin (Chen et al., 1991; Fujisawa et al., 1993; Ganss et al., 1999). However, approximately equal amounts of IBSP were subsequently detected in these 2 tissues (Qin et al., 2001). Similar to SPP1, the expression of IBSP is different within bone. In the developing calvaria, IBSP is highly expressed in all osteoblasts at the osteogenic front and on the ectocranial surfaces of the growing bone, but in only some osteoblasts on the surfaces of more mature remodeling bone trabeculae (Candeliere et al., 2001). This expression pattern suggests a role of IBSP in promoting mineral crystallization (Chen et al., 1994). IBSP and DMP1 are the 2 dentin/bone SCPP genes widely conserved in tetrapods, but neither has been found in teleosts (Fig. 2Go).

The expression of MEPE has been detected in both osteocytes and odontoblasts (Petersen et al., 2000; MacDougall et al., 2002). A targeted disruption of this gene in mice shows increased bone mass, suggesting an inhibitory role of MEPE in bone formation (Gowen et al., 2003). Although the C-terminus of mammalian MEPE has many potential phospho-Ser residues clustered with charged, especially acidic, amino acids, the net charge of the entire molecule is slightly basic. In contrast, chicken OC116, thought to be eggshell-specific (Hincke et al., 1999), is slightly acidic, which is closer to the other acidic SCPPs. Whether this biochemical change is associated with the evolutionary shift of MEPE from bone to eggshell use, or whether it represents functional specialization of this gene in bone formation in the mammalian lineage is not known.

(c) Dentin-Bone as a Continuum
As described above, it has been known that the expression profile of these SCPP genes is different within bone, osteoblasts, and osteocytes. Even within osteoblasts, anatomical site, developmental age, species, and mode of ossification all influence the expression profiles of these genes (Candeliere et al., 2001; Franz-Odendaal et al., 2006). It thus appears that, in this sense, not all bone is the same (Gorski, 1998).

Differences in the ECM protein composition are also known in dentin, which actually consists of different types of dentins. Mantle dentin, the interfacial region between the circumpulpal dentin and enamel, has lower mineral content and reduced hardness and elastic modulus, which supposedly provide toughness and arrest cracks before they expand (Tesch et al., 2001; Imbeni et al., 2005). IBSP and SPP1 were both detected as prominent organic constituents of mantle dentin, while these proteins were minimal in circumpulpal dentin (McKee et al., 1996). In contrast, the peritubular dentin, surrounding odontoblast processes, is known to be highly mineralized, that is, more heavily mineralized than the nearby intertubular dentin, and enhances dentin stiffness. Although the matrix proteins comprising this tissue are not well-understood, the bulk amino acid composition is significantly different from that of the intertubular dentin; this tissue does not appear to contain collagen or DSPP-derived proteins as major constituents (Weiner et al., 1999; Gotliv et al., 2006; Gotliv and Veis, 2007).

Many researchers, especially cell biologists, have utilized these dentin/bone SCPP genes as markers for osteogenic and odontogenic cells. However, as described above, osteogenic and odontogenic cells both express these genes, but not all of these cells consistently express these genes. It is thus difficult to distinguish odontogenic cells from osteogenic cells solely by gene expression and protein production at the single-cell level (Franz-Odendaal et al., 2006). This could have an impact on efforts to create specifically differentiated cells for gene-based dental prosthetics or therapy.

Nevertheless, at the tissue or organ level, teleost SCPP genes may work as good markers. We previously reported the development of specialized fugu jaw plates, in which many lamellar teeth grow (Andreucci, 1968; Andreucci et al., 1982; Kawasaki et al., 2005). This jaw structure grows from a mesenchymal condensation, similar to bone. However, the mesenchymal cells surrounding the jaw extend polarized cell processes into the mineralizing matrix (Kawasaki et al., 2005). Moreover, these odontoblast-like cells express both SCPP1 and SCPP5, and the overlying oral epithelial cells SCPP3A and SCPP3B, an expression pattern similar to that of tooth dentin, but not detected in any other tissues (Kawasaki et al., 2005). We thus proposed that the fugu jaw develops similarly to bone, but is composed of dentin. This idea is supported by the fact that the mineral density of the jaw is higher than that of adjacent bones. The specialized fugu jaw well illustrates the blurred border between dentin and bone. This view is consistent with the suggestion that the skeletal tissues apparently intermediate between the dentin and bone found in early vertebrates may reflect different SCPP repertoires and accompanying mineralization processes used in their skeleton (Hall, 1975; Hall, 2005b; Donoghue et al., 2006).


   (V) CONCLUDING REMARKS
TOP
 ABSTRACT
 (I) INTRODUCTION
 (II) SCPP GENE FAMILY
 (III) ENAMEL, ENAMELOID, AND...
 (IV) DENTIN AND BONE
 (V) CONCLUDING REMARKS
REFERENCES
 
Much of the work that we have reported here is based on expression studies. Demonstrating tissue-specific function is complex and usually open to interpretations for various reasons. Many genes are expressed in diverse tissues and patterns during embryogenesis. However, the SCPP gene expression reported here is, with respect to the tissues within teeth, relatively specific and replicable within closely related species. In addition, the expression patterns of SCPP genes in previously untested and diverse taxa are consistent with our ideas about the subfamilies, their genomic organization, and their functions (Kawasaki and Weiss, 2003; Kawasaki et al., 2004). So, while further experimental intervention studies will be informative and important, we think that expression does reveal the phylogenetic story that we have described in this review.

Above, we have described how bone-dentin, dentin-enameloid, and enameloid-enamel are closely related to each other, especially in their various uses of SCPPs, within and between tetrapod and teleost lineages. Our overview corroborates the important conclusion by Donoghue et al.(2006), that there are no rigid or fundamental distinctions between the various grades of bone, dentin, enamel/loid, and cartilage. It was also proposed that the bone-dentin-enameloid-enamel continuum arose early in vertebrate history, and some tissues in the continuum have repeatedly disappeared and reappeared in some lineages (Meinke and Thomson, 1983). We consider that this view is critical to an understanding of distinct mineralized tissues, and is potentially important for regenerative dentistry and medicine. We expect that this view will be further enhanced by experimental evidence and by the identification of more SCPP genes from species other than tetrapods or teleosts.

Phenogenetic drift is common in dental tissue mineralization, and probably widespread in biomineralization, as in fact it must be in any complex tissue in which multiple genotypes can generate similar phenotypes (Weiss and Buchanan, 2004). In phenogenetic drift, essentially the same tissue can persist over long time periods, supported by natural selection, yet its underlying genetic basis changes, as we see in the birth-and-death history.

An interesting and indirectly supportive finding was recently made in the biomineralization-related, spicule matrix proteins of the sea urchin (Wilt and Ettensohn, 2007). Many genes coding these proteins arose by tandem duplication; some of these proteins are P/Q-rich, and contain a variable number of Pro-Xaa-Yaa repeats, similar to AMEL; and others are acidic (Livingston et al., 2006). These surprising similarities to the SCPP family, however, are entirely the result of evolutionary convergence, because SCPP genes arose in vertebrates after the separation from all non-vertebrate lineages, including sea urchins (Sea urchin genome sequencing consortium, 2006; Kawasaki et al., 2007). Yet the functional characteristics shared by SCPPs and the sea urchin spicule matrix proteins suggest that neither specific gene number nor particular sequences of ECM proteins are themselves so important or specific for maintaining mineralized tissues.

We assume that the changing genetic basis of tissue mineralization has facilitated lineage-specific modifications in the continuum of mineralized tissues, and hence no 2 homologous mineralized tissues are genetically the same, especially in phylogenetically distant lineages. Thus, the mineralized tissue continuum itself changes during vertebrate evolution. These findings have clear and challenging implications for research in dental therapeutics, especially when based on the use of distant animals as experimental models for human dental research.


   ACKNOWLEDGMENTS
 
We thank Prof. Tohru Suzuki at Tohoku University for unpublished results, Dr. Pierre Moffatt at Shriners Hospital for Children for providing preprints, Prof. Ichiro Sasagawa at the Nippon Dental University, Dr. Anne V. Buchanan, and Mr. Samuel Sholtis at Penn State University for critical discussion, and three anonymous reviewers for helpful comments. This work was made possible by the financial support from awards SBR9804907, SBE0343442, and BCS0343442 from the U.S. National Science Foundation, and by research funds from Penn State University to K.M.W.

Received for publication October 2, 2007. Revision received February 6, 2008. Accepted for publication March 5, 2008.


   REFERENCES
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 (I) INTRODUCTION
 (II) SCPP GENE FAMILY
 (III) ENAMEL, ENAMELOID, AND...
 (IV) DENTIN AND BONE
 (V) CONCLUDING REMARKS
 REFERENCES
 

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Journal of Dental Research, Vol. 87, No. 6, 520-531 (2008)
DOI: 10.1177/154405910808700608
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