doi: 10.1073/pnas.182423299. Epub 2002 Aug 22.
Circadian genes in a blind subterranean mammal II: conservation and uniqueness of the three Period homologs in the blind subterranean mole rat, Spalax ehrenbergi superspecies
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- PMID:12193657
- PMCID: PMC129335
- DOI: 10.1073/pnas.182423299
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Circadian genes in a blind subterranean mammal II: conservation and uniqueness of the three Period homologs in the blind subterranean mole rat, Spalax ehrenbergi superspecies
Aaron Avivi et al. Proc Natl Acad Sci U S A..
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Abstract
We demonstrated that a subterranean, visually blind mammal has a functional set of three Per genes that are important components of the circadian clockwork in mammals. The mole rat superspecies Spalax ehrenbergi is a blind subterranean animal that lives its entire life underground in darkness. It has degenerated eyes, but the retina and highly hypertrophic harderian gland are involved in photoperiodic perception. All three Per genes oscillate with a periodicity of 24 h in the suprachiasmatic nuclei, eye, and harderian gland and are expressed in peripheral organs. This oscillation is maintained under constant conditions. The light inducibility of sPer1 and sPer2, which are similar in structure to those of other mammals, indicates the role of these genes in clock resetting. However, sPer3 is unique in mammals and has two truncated isoforms, and its expressional analysis leaves its function unresolved. Per's expression analysis in the harderian gland suggests an important participation of this organ in the stabilization and resetting mechanism of the central pacemaker in the suprachiasmatic nuclei and in unique adaptation to life underground.
Figures
Similarity tree of the three Per-deduced proteins. The unrooted tree depicts the similarity relationships of the three PER proteins (amino acids) inSpalax, mice, rats, humans, andDrosophila.
Diurnal expression ofsPer1,sPer2, andsPer3 ofSpalax in the SCN: coronal sections through the brain. Blue color represents Hoechst-stained nuclei. (Top) The yellow signal shows the expression ofSpalaxPer1 over 24 h measured at 6-h time intervals (ZT0: lights on; ZT12: lights off). Maximal expression is seen at ZT6. (Middle) The red signal shows the expression ofsPer2 in representative sections. Maximal expression is seen at ZT12. (Bottom) The green signal shows the expression ofsPer3 in representative sections. Maximal expression is at ZT12. Note thatsPer1 andsPer2 expression is mainly in the SCN, whereassPer3 expression is weaker and spreads in different areas of the brain. (Magnification: ×20.)
Expression ofSpalax Per genes in peripheral tissues. (A) Densitometric analysis of silver grainin situ staining in the eye. The maximal expression in the eye shows that the expression of the threesPer genes is shifted by 6 h as compared with their expression in the SCN (Fig. 2). The oscillation ofsPer3 is very weak (P > 0.05). (B) Expression of the threesPER genes in the harderian gland and liver quantitated by RT-PCR. The expression peaks of all threesPer genes in the harderian gland are synchronized with the SCN (see Fig. 2), whereas the peak of expression in the liver is shifted by 6 h. As in the SCN, the difference insPer3 expression in ZT6 and ZT12 is very small (P > 0.05).
Light inducibility of the threeSpalax Per genes' expression. Animals were given a 15-min light pulse at ZT14 and ZT22 and killed 1 h later. Coronal sections through the brain and ISH were performed on treated (ZT14 pulse and ZT22 pulse) and control animals that were killed at the same time. Relative mRNA induction was analyzed by densitometric analysis ofin situ silver grain staining.sClock inducibility is given as negative control. (Top) In the SCN,sPer1 is equally inducible at ZT14 and ZT22.sPer2 is inducible only at ZT14, whereassPer3 gene shows no measurable changes in expression levels at the two time points. (Middle) Inducibility ofsPer1,sPer2, andsPer3 in the eye is similar to that in the SCN. (Lower) In the harderian gland,sPer1 is highly inducible at ZT14 and less at ZT22 whereassPer2 expression is light sensitive only at ZT14.sPer3 shows no light inducibility at either time point. Note the significantly (P < 0.01) higher induction ofsPer1 in the harderian gland compared with the other tissues after light pulse at ZT14. Note the differenty-axis scales in SCN, eye, and harderian.
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