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Dean, M.C.; Garrevoet, J.; Van Malderen, S.J.M.; Santos, F.; Mirazón Lahr, M.; Foley, R.; Le Cabec, A. Zinc in Modern and Fossil Hominoid Teeth. Encyclopedia. Available online: https://encyclopedia.pub/entry/52584 (accessed on 14 May 2024).
Dean MC, Garrevoet J, Van Malderen SJM, Santos F, Mirazón Lahr M, Foley R, et al. Zinc in Modern and Fossil Hominoid Teeth. Encyclopedia. Available at: https://encyclopedia.pub/entry/52584. Accessed May 14, 2024.
Dean, M. Christopher, Jan Garrevoet, Stijn J. M. Van Malderen, Frédéric Santos, Marta Mirazón Lahr, Robert Foley, Adeline Le Cabec. "Zinc in Modern and Fossil Hominoid Teeth" Encyclopedia, https://encyclopedia.pub/entry/52584 (accessed May 14, 2024).
Dean, M.C., Garrevoet, J., Van Malderen, S.J.M., Santos, F., Mirazón Lahr, M., Foley, R., & Le Cabec, A. (2023, December 11). Zinc in Modern and Fossil Hominoid Teeth. In Encyclopedia. https://encyclopedia.pub/entry/52584
Dean, M. Christopher, et al. "Zinc in Modern and Fossil Hominoid Teeth." Encyclopedia. Web. 11 December, 2023.
Zinc in Modern and Fossil Hominoid Teeth
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This entry is adapted from the peer-reviewed paper 10.3390/biology12121455

Teeth begin to grow in the jaws before birth and continue to appear in an overlapping sequence until each is complete in length. Subsequently, the central pulp (nerve) chamber of each tooth slowly fills in with dentine and the root of the tooth continues to accumulate thin layers of cementum until the individual dies. Each of the tooth tissues, the hard enamel cap, the dentine core of the tooth and the root cementum grow incrementally and incorporate small quantities of blood-born trace elements ingested from our diet into their structure. A chronological record of zinc incorporation exists in each tooth tissue and can be visualised in thin sections, or slices, of teeth using a beam of synchrotron light. Zinc markings in teeth are especially useful and occur at birth in enamel and dentine and annually in the cementum layers. This work shows that zinc is consistently concentrated within surface enamel and in the dentine surrounding the central pulp chamber. Knowing where to sample Zn in modern and fossil teeth enables us to reconstruct a chronology of growth and to determine something about diet in the past from the remnants of different Zn isotopes contained in different foodstuffs.

trace elements neonatal line enamel SXRF enamel thickness mineralisation process

1. Introduction

Zinc is an essential biological trace element. Besides this, Zn also has an affinity for bone and the three mineralised tooth tissues, enamel, dentine and cementum. Not only does the distribution of Zn vary among the three tooth tissues, but its origins also derive from different physiological, developmental and chemical processes. Ultimately, the Zn source is either from the intestinal absorption of ingested dietary Zn, or from the mother perinatally, via a direct-blood-borne maternal–placental transfer to the fetus. Zinc retrieved from tooth tissues in an archaeological and palaeontological context offers strong potential for revealing aspects of an individual’s life history, for example, as a marker of birth or of annual increments of tissue laid down during life, or as an indicator of diet. Reviewing the role and function of Zn in the body, and of how it comes to distribute differently in each of the tooth tissues, provides some insight into how and where it might best be sampled and of where its incorporation into each of the mineralised tooth tissues is likely to be tightly chronologically circumscribed or not. Fossil tooth tissues are often, if not always, altered through diagenesis, and a comparison of Zn distribution and preservation in fossils from contrasting sites may point to similarities or differences with modern teeth and so indicate where within the tooth tissues Zn of biogenic origin persists for longest.

2. Zinc as an Essential Trace Element in the Body

Zinc is an essential trace element involved in many physiological processes as both a catalyst in biochemical reactions, in the maintenance of protein quaternary structure and as a component of many essential enzymes [1]. Zinc is required, among other things, for cell division, tissue growth and wound healing, but also for intestinal electrolyte absorption, neurotransmission, the immune response, thymus activity and vision [1][2]. It is the most abundant trace element found in bone mineral, being present in concentrations of between 200–300 ppm [2][3]. Zinc is also present in muscle, red blood cells and skin as well as in bone and the mineralised tooth tissues [2][4]. Zinc is required for the DNA binding proteins involved in regulating gene transcription and expression [5]. It is also a critical component of several hundred essential enzymes and proteins [4]. At least 10% of human proteins contain Zn as a cofactor [6]. These include many metalloproteins and enzymes that are involved in most of the major metabolic pathways [1].
Among metalloenzymes, Zn is a component of carbonic anhydrase, alcohol dehydrogenase [7] and of alkaline phosphatase that is crucially involved in the process of mineralisation through the generation of free phosphate groups that are then taken up by newly forming bone and tooth tissues [8][9][10][11]. The zinc-finger proteins that control a variety of fundamental cellular activities require Zn to maintain their precise quaternary structure and functional integrity [1]. Some zinc-finger proteins have been identified as specific regulators of skeletal development and mineralised tissues formation [5][11]. Zinc in bone is concentrated at the sites of mineralisation and has been shown to stimulate osteoblast differentiation and proliferation [9][10][12]. Kim et al. [13] have also demonstrated that a Zn finger-containing transcription factor (Osterix; Osx) is an essential site-specific regulator of odontoblast differentiation, maturation and of tooth root elongation.

3. Zinc in Enamel Secretion and Maturation

Matrix metalloproteinase 20, or MMP-20, (sometimes also referred to as enamelysin), is a protease that is secreted with enamel proteins during the early (secretory) stage of amelogenesis, when the enamel crystallites are growing predominantly in length [11][14]. MMP-20 cleaves the enamel proteins surrounding crystallites to allow their slow growth in width, after which these cleavage products are reabsorbed by secretory ameloblasts and degraded. The more aggressive serine protease, kallikrein 4, or KLK-4, is a protease that is secreted during the later transition and maturation stages of amelogenesis. KLK-4 degrades what remains of the enamel organic matrix after enamel secretion is completed [11][14]. The principal functions of MMP-20 and KLK-4 in dental enamel formation are to facilitate the orderly replacement of organic matrix with mineral to form hard dense enamel. This occurs in a low-calcium environment that favours the slow controlled formation of hydroxyapatite that is maintained by the tight barrier filter of the secretory ameloblast sheet; this excludes or removes excess Ca [15]. MMP-20 itself contains Zn, but Zn in enamel is a potent inhibitor of serine proteases and so may have an important controlling influence, especially on KLK-4 during the maturation phase [11]. For these reasons, it has been suggested that Zn enrichment in the outer enamel [16][17], but also at the EDJ [18] and in dentine [19], may result from metalloprotease activity and degradation that results in the retention and sequestration of Zn originally involved in the mineralisation and/or enamel maturation process.

4. Zinc Absorption and Maternal–Fetal Transfer

Zinc absorption from the gut involves first binding to a surface receptor on the gut wall enterocytes and then subsequently being taken up into the enterocytes [10][20]. Zn has five stable isotopes of which the most abundant are 64Zn and 66Zn. The detection and distribution of Zn isotopes in dental tissues and their relation to diet are discussed more fully below. However, the intestinal absorption of Zn is inhibited and undergoes isotopic fractionation by, for example, plant phytates which precipitate dietary Zn, and because there is a preferential precipitation of the lighter Zn isotopes (64Zn) with plant phytates, this then favours heavier 66Zn absorption and enrichment relative to 64Zn [21]. Thus, the isotopic composition of Zn found in body tissues may not directly reflect the dietary isotopic composition [21][22]. A proportion of absorbed Zn then remains bound to metallothionein within the enterocyte, and as this accumulates, it inhibits further Zn absorption from the gut, thus regulating Zn uptake. It follows that as dietary Zn intake increases beyond the threshold required, Zn absorption decreases relative to intake [20]. The proportion of Zn that remains bound to metallothionein within the cell, eventually returns to the bowel lumen when the enterocyte is shed. Consequently, faecal loss of unabsorbed Zn increases with excess Zn uptake as the Zn-containing enterocytes are shed. Zn is also lost through urinary excretion and through sweat; this has practical implications when performing Synchrotron X-ray fluorescence (SXRF) experiments to map Zn distribution in tooth and bone samples, as surfaces under investigation must remain completely clean and untouched. Zn is an important essential metal ion such that recent research has identified metallochaperone proteins that escort or direct Zn to specific crucial cellular enzymes, ensuring the correct Zn allocation when levels are scarce [6].
Some Zn becomes bound in serum to albumin or an alpha-2 macroglobulin after absorption; this may be transported to the liver [2][20], but beyond the Zn component in bone mineral, there are no real functional reserves of Zn in the body [1]. The exception is in neonates where, at term, Zn accumulated during gestation is stored in the liver and then released postnatally. Most Zn is transferred to the fetus from the mother after the 24th week of gestation and stored in the fetal liver [1]. Pre-term birth, therefore, reduces the amount of Zn that can accumulate with the risk of Zn deficiency in the neonate [1][23]. Maternal-fetal placental transfer of Zn is an active process and fetal Zn concentrations are maintained constantly higher than maternal levels. While Zn in human milk varies in concentration between 0.7–1.6 mg/L, and declines with time, colostrum contains 8–12 mg/L, falling to 3–6 mg/L within a week [1].

5. The Distribution of Zinc in Mineralised Tissues

Zinc is the only trace element in teeth where the concentrations approach that of fluoride, an element with which Zn shares a similar distribution across the various tooth tissues [7][24]. Brudevold et al. [7] used spectrography on serial sections of teeth to describe the distribution and concentration of Zn in unerupted and erupted human permanent teeth from patients of known age and of diverse geographical origin. They reported the highest concentrations of Zn in the outer surface layers of enamel (1300–2100 ppm) and quantified a steep decline in Zn concentration towards the enamel dentine junction (EDJ) where it was ~200 ppm (Figure 1). Brudevold et al. [7] conclude that most of the Zn uptake occurred prior to eruption, as attested by the high levels in Zn in the unerupted teeth. They further state that, although some Zn uptake may occur, the post-eruptive data are too irregular to support a continuous Zn uptake with age [7]. Yet, there was a variation in Zn concentration between the teeth of diverse worldwide origins where outer enamel values ranged between 900–2100 ppm [7]. More recently, Lynch [4] has shown that post-eruptive Zn uptake can occur and may, for example, be derived from accumulated Zn in the salivary pellicle and oral mucosa. In modern teeth, it is also possible, but remains to be demonstrated, that further Zn enrichment may occur at the very outer enamel surface following a prolonged use of dentifrices, to which Zn is added as an anti-bacterial agent to control plaque accumulation and reduce calculus formation [4].
Biology 12 01455 g001
Figure 1. The distribution and concentration (ppm) of Zn from the outer enamel surface (OES) to the EDJ (enamel–dentine junction) and from the EDJ to the pulp in crowns of unerupted teeth collected from Schenectady, New York. Adapted from Figure 1 in Brudevold et al. [7].
Other studies have also reported a gradient of Zn concentration in enamel with maximal values in outer enamel (e.g., [25][26][27]). Sanchez-Quevedo et al. [28] noted a rise in the Zn gradient from inner to outer enamel, and Humphrey et al. [29][30][31] and Müller et al. [17] have shown that Zn/Ca ratios in deciduous enamel increase near exponentially, some 20–30 times [17], towards the outermost enamel layers from values close to the EDJ using laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). In both a modern human sample and in a sample of mostly thin-enamelled, non-primate fossil taxa (but including one Macaca sp.), Bourgon et al. [32] reported the same gradient of Zn distribution where the range of maximum concentrations in outer enamel was between ~100–700 ppm in both samples, and Brozou et al. [26] also reported the Zn concentration within the “first tens of microns of the enamel surface” as ~650 ppm. Just one study, however, based on atomic absorption spectrometry of permanent upper central incisor labial enamel, reported a reverse pattern of Zn enrichment with lower concentrations at the surface enamel and higher concentrations at the EDJ [11].
Kang and colleagues [33] again used LA-ICP-MS and reported high concentrations of Zn at the enamel neonatal line (NNL) and, since then, Dean et al. [34] have used synchrotron X-ray fluorescence (SXRF) to quantify Zn concentration at the NNL and the enamel-dentine junction (EDJ), where it was between 200–500 ppm, compared with Zn concentration at the outer deciduous enamel surface, where it was slightly higher (400–500 ppm).
In dentine, Brudevold et al. [7] reported that the greatest concentration of Zn (as high as 1000 ppm) was in secondary dentine, adjacent to the pulp chamber, with a decreasing gradient in concentration towards the EDJ in the crown and towards the cementum–dentine junction (CDJ) in the root dentine (Figure 1; see also [25][26]). Noticeably, there was a small rise in Zn concentration (of between 150–300 ppm) in the mantle dentine immediately adjacent to the EDJ, and Dean et al. [34] have also reported Zn concentrations of up to 500 ppm along the EDJ of deciduous teeth. Stock et al. [35] and Dean et al. [36] have each identified high concentrations of Zn in slow forming peritubular dentine. Kang and colleagues [33], using LA-ICP-MS again, identified elevated levels of Zn at the dentine NNL, along the EDJ and in secondary dentine adjacent to the pulp. Studies of deciduous dentine using SXRF [34] have also identified high levels of Zn in the dentine NNL itself, but also in dentine formed prenatally.
At the tooth root surface, Brudevold et al. [7][37] first reported that the Zn concentration in cementum was also high, ranging from 500 to 1500 ppm; subsequently, Martin et al. [38][39] also demonstrated high levels of Zn in cementum as compared with the underlying root dentine (Figure 2). Since this time, several papers have observed and quantified the distribution and concentration of Zn in both cellular and acellular cementum [19][26][36][40][41]. At higher resolution, it becomes clear that there are fine Zn-rich lines or bands in cementum that define what have been shown to be annual incremental markings (see [42] for a review; see e.g., [43][44] for further visualisation of these incremental markings) with greater resolution than transmitted light microscopy or than SXRF intensity maps for Ca or Sr [26][36].
Biology 12 01455 g002
Figure 2. The distribution and concentration (ppm) of Zn from the tooth root surface to the pulp in unerupted teeth collected from Schenectady, New York. Adapted from Figure 2 in Brudevold et al. [7].
Zinc is also present in bone at the boundary between the forming pre-calcified and calcified bone matrix where it is associated with alkaline phosphatase, a metalloenzyme that itself contains two functional Zn atoms. However, unlike dentine or cementum, Zn does not persist in bone [12] but may well play an important role in stimulating bone cell proliferation and collagen formation [9][41][45]. These observations about Zn at the bone-forming front of Haversian systems have prompted suggestions that the Zn-rich incremental markings in cementum may also reflect periods of cell proliferation and initiation of cementoblast secretory activity [36].

6. Zinc Incorporation into Hydroxyapatite

Brudevold et al. [7] and Lynch [4] have proposed that Zn is likely to be incorporated directly into the hydroxyapatite crystal lattice during crystal formation as well as at the crystal surface (depending on the Zn/Ca ratio present in the enamel fluid). In enamel, Zn also continues to be incorporated into hydroxyapatite during further mineral deposition during the pre-eruptive phase by exchange of Ca2+ and Zn2+, and then subsequently through the post-eruptive acquisition of Zn by surface enamel from saliva, plaque, water and food [4]. However, Zn also readily binds to proteins present in the organic components of dental tissues, which make up a much greater proportion of mature dentine and cementum than enamel. Raising dietary levels of Zn does not seem to raise levels of Zn measured in teeth [46], suggesting there is tight regulation of Zn (and other ion) levels by secretory ameloblasts [47]. If this is indeed the case, it begs the question of how the observed variation in Zn concentration in both forming enamel and dentine can arise in the first place. It implies that fluctuations in Zn concentration would result largely from periods of Zn depletion that fall below a threshold maximum rather than from bouts of Zn enrichment.
High levels of Zn in enamel, secondary dentine and cementum may be adaptive in that it reduces acid solubility and inhibits the resorption of cementum by osteoclasts and thus protects the root surface [3][36][48][49][50][51][52]. When the solution concentration of Zn2+ ions at the hydroxyapatite crystal surface exceeds 1 ppm [53], the precipitation of a zinc phosphate, alpha-Hopeite, (α-Zn3(PO4)2.4H2O), occurs [4]. Mohammed et al. [50] have demonstrated that the likely mechanism for the reduction in the acid dissolution of hydroxyapatite is through Zn interacting and binding with PO43− sites at the crystal surface where it forms a Hopeite-like phase, suppressing the release of further phosphate ions and reducing mineral loss from the apatite structure at low pH. While Zn certainly reduces the acid solubility of hydroxyapatite, to a similar degree as fluoride, it appears to have little or no effect in reducing the incidence of caries [4][7]. Nonetheless, Zn has been shown to selectively and strongly inhibit osteoclast activity in bone resorption [3]. Similarly, at the cementum surface, Zn may well inhibit osteoclast activity, and cementum resorption and Zn at the inner aspect of the pulp chamber may well also protect dentine from resorption by blood-borne osteoclasts present in the pulp [36]. The presence of Zn2+ ions is also effective in inhibiting hydroxyapatite crystal growth [53] and so Zn may well play a role in controlling the rate of crystallite growth in enamel, dentine and cementum formation. It is for this reason that Zn is an effective inhibitor of calculus formation in the mouth and why, therefore, as well as being bacteriostatic, it is incorporated into so many dental health products [4].

7. Zinc Distribution in Modern and Fossil Teeth

Zinc concentration in outer enamel is universally high across all the deciduous, permanent and fossil hominoid teeth studied so far. Where secondary dentine has formed, or is preserved, Zn concentrations are also higher than in primary dentine. Besides enamel and dentine, cementum layers also contain Zn at greater concentrations than the underlying root dentine. Figure 3 shows synchrotron X-ray fluorescence (SXRF) maps of the Zn distribution in seven permanent teeth of varying tooth types.

Figure 3. Zinc intensity maps revealed with synchrotron X-ray fluorescence (SXRF) of permanent modern great ape and human teeth, (a) Pan lower first molar tooth, (b) Pan lower third molar tooth, (c) Pongo female canine, (d) modern human upper canine (e) Gorilla lower second molar tooth, (f) Gorilla unerupted lower third molar tooth from the same individual as (e), (g) modern human lower third molar tooth. In all teeth, including the unerupted lower third molar, surface enamel is Zn-rich. In all cases, where it has formed, secondary dentine and cementum are Zn-rich. The Zn distribution in dentine in each tooth broadly follows the incremental formation pattern. Images are not to scale.

The thickness of the Zn-enriched surface enamel layer was observed not to be proportionate in thickness to the regional linear enamel thickness and varied considerably between and within teeth in both the maximum Zn concentration measured in outer enamel (197–1743 ppm), and in the rate of the exponential rise of concentration towards the surface. Zinc levels at the cusp, mid-crown and cervix of the same tooth may vary, but mid-crown measurements are as good a representation of the overall average concentrations as any, and perhaps the most consistently high. The Zn concentration range and maximum values in outer enamel overlap in the modern human, great ape and fossil hominoid deciduous and permanent tooth samples studied here. Zinc is also laid down in teeth prenatally and at the birth line (or neonatal line) in deciduous teeth and along the enamel-dentine junction (Figure 4). Figure 4 shows a thin section of a modern deciduous tooth cusp with the neonatal line as it appears in transmitted light and with synchrotron X-ray fluorescence (SXRF) to reveal the Zn distribution corresponding with the neonatal line in both enamel and dentine.

Figure 4. (a) Transmitted light micrograph and (b) matching Zn SXRF intensity image of the cuspal region of a modern human second deciduous molar tooth showing the neonatal line and enamel-dentine junction. In the SXRF Zn map, the neonatal line in both enamel (white arrows) and dentine (black arrows) is Zn-rich as is the prenatal dentine (black asterisks) and enamel-dentine junction. In prenatal enamel (white asterisks), the SXRF intensity map suggests this is Zn-depleted relative to postnatal enamel. Adapted from Figs. 2e and h in Dean et al [34].

Zinc is also tenacious compared to other trace elements contained in fossil tooth tissues and distributes within many fossil teeth exactly as it does in modern teeth. It can even be preserved at the neonatal line in fossil teeth for millions of years (Figure 5) and used as a marker of birth, with the caveat that Zn lines in enamel and dentine may also be indicative of other stress events in life.

Figure 5. (a) Transmitted light micrograph (TLM) and (b) matching Zn SXRF intensity image of the cuspal region of a fossil first molar tooth showing the neonatal line (white arrows) and enamel-dentine junction. This fossil hominoid tooth is attributed to Ekembo heseloni and dates to ~17.5 million years from Rusinga Island, Kenya.

The consistent distribution of Zn in both modern and fossil hominoid teeth allows us to take samples with greater confidence and precision. New high-resolution sampling and analytical techniques now enable access to the chronological record of Zn laid down in dentine and cementum layers through life with good prospects for tracking dietary shifts, stress events and seasonal changes far back into the archaeological and fossil records.

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Subjects: Evolutionary Biology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
M. Christopher Dean
,
Jan Garrevoet
,
Stijn J. M. Van Malderen
,
Frédéric Santos
,
Marta Mirazón Lahr
,
Robert Foley
,
Adeline Le Cabec
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Revisions: 5 times (View History)
Update Date: 12 Dec 2023
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