Differential Effects of Two Period Genes on the Physiology and Proteomic Profiles of Mouse Anterior Tibialis Muscles

  • Bae, Kiho (Department of Life Science, Yonsei University) ;
  • Lee, Kisoo (Department of Life Science, Yonsei University) ;
  • Seo, Younguk (Department of Life Science, Yonsei University) ;
  • Lee, Haesang (Department of Life Science, Yonsei University) ;
  • Kim, Dongyong (Department of Life Science, Yonsei University) ;
  • Choi, Inho (Department of Life Science, Yonsei University)
  • Received : 2006.06.12
  • Accepted : 2006.09.10
  • Published : 2006.12.31

Abstract

The molecular components that generate and maintain circadian rhythms of physiology and behavior in mammals are present both in the brain (suprachiasmatic nucleus; SCN) and in peripheral tissues. Examination of mice with targeted disruptions of either mPer1 or mPer2 has shown that these two genes have key roles in the SCN circadian clock. Here we show that loss of the clock gene mPer2 affects forced locomotor performance in mice without altering muscle contractility. A proteomic analysis revealed that the anterior tibialis muscles of the mPer2 knockout mice had higher levels of glycolytic enzymes such as triose phosphate isomerase and enolase than those of either the wild type or mPer1 knockout mice. In addition, the level of expression of HSP90 in the mPer2 mutant mice was also significantly higher than in wildtype mice. These results suggest that the reduced locomotor endurance of the mPer2 knockout mice reflects a greater dependence on anaerobic metabolism under stress conditions, and that the two canonical clock genes, mPer1 and mPer2, play distinct roles in the physiology of skeletal muscle.

Keywords

Acknowledgement

Supported by : Korea Research Foundation

References

  1. Bae, K., Jin, X., Maywood, E. S., Hastings, M. H., Reppert, S. M., et al. (2001) Differential functions of mPer1, mPer2 and mPer3 in the SCN circadian clock. Neuron 30, 525−536
  2. Baker, E. J. and Gleeson, T. T. (1999) The effects of intensity on the energetics of brief locomotor activity. J. Exp. Biol. 202, 3081−3087
  3. Balsalobre, A., Marcacci, L., and Schibler, U. (2000) Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr. Biol. 10, 1291−1294 https://doi.org/10.1016/S0960-9822(00)00758-2
  4. Bunger, M. K., Wilsbacher, L. D., Moran, S. M., Clendenin, C., Radcliffe, L. A., et al. (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009−1017
  5. Challet, E., Malan, A., Turek, F. W., and van Reeth, O. (2003) Daily variations of blood glucose, acid-base state and $PCO_{2}$ in rats: effect of light exposure. Neurosci. Lett. 355, 131−135 https://doi.org/10.1016/j.neulet.2003.10.041
  6. Dallmann, R., Touma, C., Palme, R., Albrecht, U., and Steinlechner, S. (2006) Impaired daily glucocorticoid rhythm in $Per1^{Brd}$ mice. J. Comp. Physiol. A. 192, 769−775 https://doi.org/10.1007/s00359-006-0114-9
  7. Damiola, F., Minh, L., Preitner, N., Kornmann, B., Fleury-Olela, F., et al. (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14, 2950−2961 https://doi.org/10.1101/gad.183500
  8. Dawson, B., Fitzsimons, M., Green, S., Goodman, C., Carey, M., et al. (1998) Changes in performance, muscle metabolites, enzymes and fibre types after short sprint training. Eur. J. Appl. Physiol. Occup. Physiol. 78, 163−169
  9. Dowson, M. N., Nevill, M. E., Lakomy, H. K., Nevill, A. M., and Hazeldine, R. J. (1998) Modeling the relationship between isokinetic muscle strength and sprint running performance. J. Sports Sci. 16, 257−265
  10. Fu, L., Pelicano, H., Liu, J., Huang, P., and Lee, C. C. (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111, 41−50
  11. Gekakis, N., Staknis, D., Nguyen, H. B., Davis, F. C., Wilsbacher, L. D., et al. (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280, 1564−1569
  12. Hirano, M., Rakwal, R., Shibato, J., Agrawal, G. K., Jwa, N-S., et al. (2006) New protein extraction/solubilization protocol for gel-based proteomics of rat (female) whole brain and brain regions. Mol. Cells 22, 119−125
  13. Hornberger, T. A. and Esser, K. A. (2004) Mechanotransduction and the regulation of protein synthesis in skeletal muscle. Proc. Nutr. Soc. 63, 331−335
  14. Huang, T. H., Yang, R. S., Hsieh, S. S., and Liu, S. H. (2002) Effects of caffeine and exercise on the development of bone: a densitometric and histomorphometric study in young wistar rats. Bone 30, 293−299
  15. Isfort, R. J., Wang, F., Greis, K. D., Sun, Y., Keough, T. W., et al. (2002) Proteomic analysis of rat soleus muscle undergoing hindlimb suspension-induced atrophy and reweighting hypertrophy. Proteomics 2, 543−550 https://doi.org/10.1002/1615-9861(200205)2:5<543::AID-PROT543>3.0.CO;2-K
  16. Kaasik, K. and Lee, C. C. (2004) Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430, 467−477 https://doi.org/10.1038/nature02724
  17. Kim, H.-G. and Bae, K. (2006) Effect of mPER1 on the expression of HSP105 gene in the mouse SCN. J. Exp. Biomed. Sci. 12, 53−56
  18. Kregel, K. C. (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92, 2177−2186
  19. Lee, J. W. and Bae, K. (2004) Functional implications of the mammalian clock gene, mPer expression in the peripheral tissues. J. Nano Bio. Tech. 2, 94−99
  20. Lee, M., Choi, I., and Park, K. (2002) Activation of stress signaling molecules in bat brain during arousal from hibernation. J. Neurochem. 82, 867−873
  21. Lee, C., Weaver, D. R., and Reppert, S. M. (2004a) Direct association between mouse PERIOD and CKI$\varepsilon$ is critical for a functioning circadian clock. Mol. Cell. Biol. 24, 584−594 https://doi.org/10.1128/MCB.24.2.584-594.2004
  22. Lee, K., Lee, Y. S., Lee, M., Yamashita, M., and Choi, I. (2004b) Mechanics and fatigability of the rat soleus muscle during early reloading. Yonsei Med. J. 45, 690−702
  23. Lowrey, P. L. and Takahashi, J. S. (2004) Mammalian circadian biology: Elucidating genome-wide levels of temporal organization. Ann. Rev. Genomics Hum. Genet. 5, 407−441 https://doi.org/10.1146/annurev.genom.5.061903.175925
  24. Merkulova, T., Dehaupas, M., Nevers, M., Creminon, C., Alameddine, H., et al. (2000) Differential modulation of $\alpha$, $\beta$ and $\gamma$ enolase isoforms in regenerating mouse skeletal muscle. Eur. J. Biochem. 267, 3735−3743 https://doi.org/10.1046/j.1432-1327.2000.01408.x
  25. Payne, R. C., Veenman, P., and Wilson, A. M. (2005) The role of the extrinsic thoracic limb muscles in equine locomotion. J. Anat. 206, 193−204 https://doi.org/10.1111/j.1469-7580.2005.00353.x
  26. Reppert, S. M. and Weaver, D. R. (2001) Molecular analysis of mammalian circadian rhythms. Ann. Rev. Physiol. 63, 647− 676 https://doi.org/10.1146/annurev.physiol.63.1.647
  27. Rome, L. C. (1998) Some advances in integrative muscle physiology. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 120, 51−72
  28. Rudic, R. D., McNamara, P., Curtis, A. M., Boston, R. C., Panda, S., et al. (2004) BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLosbiology 2, 1893−1899
  29. Rutter, J., Reick, M., Wu, L. C., and McKnight, S. L. (2001) Regulation of Clock and Npas2 DNA binding by the redox state of NAD cofactors. Science 293, 510−514
  30. Sehgal, A. (2004) Molecular biology of circadian rhythms. pp. 131−140 and 221−229, John Wiley & Sons, Inc., Hoboken
  31. Seo, Y., Lee, K., Park, K., Bae, K., and Choi, I. (2006) A proteomic assessment of muscle contractile alterations during unloading and reloading. J. Biochem. 139, 71−80 https://doi.org/10.1093/jb/mvj007
  32. Shearman, L. P., Sriram, S., Weaver, D. R., Maywood, E. S., Chaves, I., et al. (2000) Interacting molecular loops in the mammalian circadian clock. Science 288, 1013−1019
  33. Silver, R., LeSauter, J., Tresco, P. A., and Lehman, M. N. (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382, 810−813 https://doi.org/10.1038/382813a0
  34. Srikakulam, R. and Winkelmann, D. A. (2004) Chaperonemediated folding and assembly of myosin in striated muscle. J. Cell Sci. 117, 641−652 https://doi.org/10.1242/jcs.00899
  35. Stokkan, K., Yamazaki, S., Tei, H., Sakaki, Y., and Menaker, M. (2001) Entrainment of the circadian clock in the liver by feeding. Science 293, 490−493
  36. Ueda, H. R., Hayashi, S., Chen, W., Sano, M., Machida, M., et al. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genetics 37, 187−192 https://doi.org/10.1038/ng1504
  37. van der Horst, G. T. J., Muijtjens, M., Kobayashi, K., Takano, R., Kanno, S., et al. (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398, 627−630
  38. Yan, L. and Silver, R. (2004) Resetting the brain clock: time course and localization of mPer1 and mPer2 protein expression in suprachiasmatic nuclei during phase shifts. Eur. J. Neurosci. 19, 1105−1109 https://doi.org/10.1111/j.1460-9568.2004.03189.x
  39. Yoo, S. H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., et al. (2004) PERIOD::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 101, 5339−5346
  40. Zheng, B., Albrecht, U., Kaasik, K., Sage, M., Lu, W., et al. (2001) Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 105, 683−694