Comparative Analysis of Telomere Lengths and Erosion with Age in Human Epidermis and Lingual Epithelium

Abstract

We investigated progressive telomere shortening in normal human epidermis and lingual epithelium during aging, and attempted, in particular, to ascertain whether the telomere shortening that accompanies aging occurs at the same rate in different tissues. We studied telomeric DNA integrity, and estimated annual telomere loss, in 52 specimens of epidermis and 48 specimens of lingual epithelium collected at autopsy from subjects who had died at ages between 0 and 101 y. Most of the DNA samples were measured twice by southern blot hybridization. In addition, the correlation between telomere lengths in the two types of tissues was examined. The telomere reduction rates in epidermis and lingual epithelium were 36 bp and 30 bp per y, respectively, and these were significantly different. The rates obtained by the second measurements in epidermis and lingual epithelium were 39 and 32 bp per y, respectively, and these were also significantly different. The mean telomere lengths in the epidermis of eight neonates and the lingual epithelium of seven neonates were 13.2+/-1.0 and 13.8+/-1.0 kb, respectively. Comparison of telomere lengths in the two tissues for 41 paired samples showed that the mean telomere length in the epidermis (10.7+/-2.3 kb) was less than that in the lingual epithelium (12.4+/-2.5 kb); however, statistical analysis revealed a very significant relationship between epidermal and lingual epithelial telomere length (r=0.842, p<0.0001). These results indicate that the telomeres in epidermis and lingual epithelium are characterized by tissue-specific loss rates.

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“…It is important to note that the epidermis is one of the few regenerative tissues to express telomerase [13]. Further, in a recent investigation of progressive telomere shortening, in 52 specimens of normal human epidermis and 48 specimens of lingual epithelium collected at autopsy from subjects who died between 0 and 101 years of age, researchers determined that the telomere shortening associated with ageing is characterized by tissue-specific loss rates [14]. Indeed, the natural, progressive shortening of telomeres may be one of the primary mechanisms of cellular ageing in skin [15].…”

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“…For other taxa, telomere dynamics have generally not been investigated in epidermis samples, but in blood samples (Monaghan and Haussmann, 2006), with some exceptions in humans (e.g. Nakamura et al, 2002;Sugimoto et al, 2006). Significant correlations were found between telomere lengths in different tissues within individual humans Takubo et al, 2002).…”

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“…Similarly, another study conducted on newborns found a strong correlation (r =.89) between TL of white blood cells and TL of umbilical artery cells [43]. And in two post-mortem samples of 41 and 21 subjects from 0 to 101 years of age, Nakamura reported significant associations in lingual epithelium cell TL and epidermis TL (r =.84 and r =.93, respectively) [42]. By additionally controlling for donor age, Friedrich and colleagues found significant correlations in tissue samples from 9 patients (age 75-95 years) between epidermis TL and leukocyte TL (R2 =.79), epidermis TL and synovial sample TL (R 2 =.71), and synovial sample TL and leukocyte TL (R 2 =.54) [45].…”

“…So far, only few studies have compared TL concordance across different tissues [40][41][42][43][44][45], and to date no study observed TL dynamics in different tissue samples across multiple time points to compare TL dynamics between tissues over time. Still, some cross-sectional studies report synchrony over different tissues.…”