Radiocarbon dating of the human eye lens crystallines reveal proteins without carbon turnover throughout life

Abstract

Background: Lens crystallines are special proteins in the eye lens. Because the epithelial basement membrane (lens capsule) completely encloses the lens, desquamation of aging cells is impossible, and due to the complete absence of blood vessels or transport of metabolites in this area, there is no subsequent remodelling of these fibers, nor removal of degraded lens fibers. Human tissue ultimately derives its (14)C content from the atmospheric carbon dioxide. The (14)C content of the lens proteins thus reflects the atmospheric content of (14)C when the lens crystallines were formed. Precise radiocarbon dating is made possible by comparing the (14)C content of the lens crystallines to the so-called bomb pulse, i.e. a plot of the atmospheric (14)C content since the Second World War, when there was a significant increase due to nuclear-bomb testing. Since the change in concentration is significant even on a yearly basis this allows very accurate dating.

Methodology/principal findings: Our results allow us to conclude that the crystalline formation in the lens nucleus almost entirely takes place around the time of birth, with a very small, and decreasing, continuous formation throughout life. The close relationship may be further expressed as a mathematical model, which takes into account the timing of the crystalline formation.

Conclusions/significance: Such a life-long permanence of human tissue has hitherto only been described for dental enamel. In confront to dental enamel it must be held in mind that the eye lens is a soft structure, subjected to almost continuous deformation, due to lens accommodation, yet its most important constituent, the lens crystalline, is never subject to turnover or remodelling once formed. The determination of the (14)C content of various tissues may be used to assess turnover rates and degree of substitution (for example for brain cell DNA). Potential targets may be nervous tissues in terms of senile or pre-senile degradation, as well as other highly specialised structures of the eyes. The precision with which the year of birth may be calculated points to forensic uses of this technique.

Figure 1. The formation of eye lens crystallines determined by ¹⁴C.

Nuclear bomb tests during 1955–63 produced large amounts of ¹⁴C, which after this period has declined exponentially (thin, grey line). Comparing the amount of ¹⁴C in eye-lens crystallines (red circles, plotted as a function of the year of birth) with the atmospheric concentration in units of pmC (percent modern Carbon) has made it possible to investigate the timing of the formation process. The red curve shows the output from our resulting lens-formation model, which provides the basis for predicting the year of birth accurately (Fig. 2).

Figure 2. Predicting the year of birth by the ¹⁴C of eye lens crystallines.

The year of birth of a person may be predicted from the ¹⁴C content of the eye-lens crystallines. In an over-simplistic picture the eye lens crystallines are formed at the birth year of the individual. The year of birth predicted in that way (red circles, showing only the centre value of the 95% confidence interval) is close to the actual yeat but evidently different, in particular for the oldest individuals. More accurate results are obtained by using our model, because it takes into account that the crystallines grow later in life too: The resulting predictions (black vertical bars, showing the 95% confidence interval) are in agreement with the actual values in all cases. The two ways of predicting the year of birth correspond to using the black (atmospheric) or the red (eye-lens model) curve in Fig. 1, respectively. The red line shows the ideal 1∶1 ratio between the predicted and actual year of birth.