Significant modulation of the hepatic proteome induced by exposure to low temperature in Xenopus laevis

Biology Open

Volumn 2, Issue 10, 2013, Pages 1057-1069

  Nagasawa, Kazumichi ^a   Tanizaki, Yuta ^a,b   Okui, Takehito ^a   Watarai, Atsuko ^a   Ueda, Shinobu ^a   Kato, Takashi ^a  

^a WASEDA UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

Author keywords

Animal model; Liver; Low temperature; Pathway; Proteomics; Xenopus laevis

Indexed keywords

EID: 84979499884     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20136106     Document Type: Article

References (65)

1. Aizawa, Y., Nogawa, N., Kosaka, N., Maeda, Y., Watanabe, T., Miyazaki, H. and Kato, T. (2005). Expression of erythropoietin receptor-like molecule in Xenopus laevis and erythrocytopenia upon administration of its recombinant soluble form. J. Biochem. 138, 167-175.
2. Anderson, L. and Seilhamer, J. (1997). A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 18, 533-537.
3. Bacon, B. R. and Britton, R. S. (1990). The pathology of hepatic iron overload: a free radical-mediated process? Hepatology 11, 127-137.
4. Bechmann, L. P., Hannivoort, R. A., Gerken, G., Hotamisligil, G. S., Trauner, M. and Canbay, A. (2012). The interaction of hepatic lipid and glucose metabolism in liver diseases. J. Hepatol. 56, 952-964.
5. Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300.
6. Boutilier, R. G. (2001). Mechanisms of cell survival in hypoxia and hypothermia. J. Exp. Biol. 204, 3171-3181.
7. Boutilier, R. G., Donohoe, P. H., Tattersall, G. J. and West, T. G. (1997). Hypometabolic homeostasis in overwintering aquatic amphibians. J. Exp. Biol. 200, 387-400.
8. Burggren, W. W. and Warburton, S. (2007). Amphibians as animal models for laboratory research in physiology. ILAR J. 48, 260-269.
9. Chegini, N., Aleporou, V., Bell, G., Hilder, V. A. and Maclean, N. (1979). Production and fate of erythroid cells in anaemic Xenopus laevis. J. Cell Sci. 35, 403-415.
10. Chen, G., Gharib, T. G., Huang, C. C., Taylor, J. M., Misek, D. E., Kardia, S. L., Giordano, T. J., Iannettoni, M. D., Orringer, M. B., Hanash, S. M. et al. (2002). Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell. Proteomics 1, 304-313.
11. Cossins, A., Fraser, J., Hughes, M. and Gracey, A. (2006). Post-genomic approaches to understanding the mechanisms of environmentally induced phenotypic plasticity. J. Exp. Biol. 209, 2328-2336.
12. de Sousa Abreu, R., Penalva, L. O., Marcotte, E. M. and Vogel, C. (2009). Global signatures of protein and mRNA expression levels. Mol. Biosyst. 5, 1512-1526.
13. Dejong, C. H., van de Poll, M. C., Soeters, P. B., Jalan, R. and Olde Damink, S. W. (2007). Aromatic amino acid metabolism during liver failure. J. Nutr. 137, 1579S-1585S; discussion 1597S-1598S.
14. Dennis, G., Jr, Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol. 4, 3.
15. Devreese, B., Sergeant, K., Van Bakel, N. H., Debyser, G., Van Beeumen, J., Martens, G. J. and Van Herp, F. (2010). A proteome map of the pituitary melanotrope cell activated by black-background adaptation of Xenopus laevis. Proteomics 10, 574-580.
16. Driedzic, W. R., Clow, K. A., Short, C. E. and Ewart, K. V. (2006). Glycerol production in rainbow smelt (Osmerus mordax) may be triggered by low temperature alone and is associated with the activation of glycerol-3-phosphate dehydrogenase and glycerol-3-phosphatase. J. Exp. Biol. 209, 1016-1023.
17. Epperson, L. E., Dahl, T. A. and Martin, S. L. (2004). Quantitative analysis of liver protein expression during hibernation in the golden-mantled ground squirrel. Mol. Cell. Proteomics 3, 920-933.
18. Epperson, L. E., Rose, J. C., Carey, H. V. and Martin, S. L. (2010). Seasonal proteomic changes reveal molecular adaptations to preserve and replenish liver proteins during ground squirrel hibernation. Am. J. Physiol. 298, R329-R340.
19. Falcón-Pérez, J. M., Lu, S. C. and Mato, J. M. (2010). Sub-proteome approach to the knowledge of liver. Proteomics Clin. Appl. 4, 407-415.
20. Ghazalpour, A., Bennett, B., Petyuk, V. A., Orozco, L., Hagopian, R., Mungrue, I. N., Farber, C. R., Sinsheimer, J., Kang, H. M., Furlotte, N. et al. (2011). Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet. 7, e1001393.
21. Gillardin, V., Silvestre, F., Dieu, M., Delaive, E., Raes, M., Thomé, J. P. and Kestemont, P. (2009). Protein expression profiling in the African clawed frog Xenopus laevis tadpoles exposed to the polychlorinated biphenyl mixture aroclor 1254. Mol. Cell. Proteomics 8, 596-611.
22. Gracey, A. Y. (2007). Interpreting physiological responses to environmental change through gene expression profiling. J. Exp. Biol. 210, 1584-1592.
23. Graff, D. and Allen, K. (1963). Glycogen content in Moniliformis dubius (Acanthocephala). J. Parasitol. 49, 204-208.
24. Griffin, T. J., Gygi, S. P., Ideker, T., Rist, B., Eng, J., Hood, L. and Aebersold, R. (2002). Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol. Cell. Proteomics 1, 323-333.
25. Hellsten, U., Harland, R. M., Gilchrist, M. J., Hendrix, D., Jurka, J., Kapitonov, V., Ovcharenko, I., Putnam, N. H., Shu, S., Taher, L. et al. (2010). The genome of the Western clawed frog Xenopus tropicalis. Science 328, 633-636.
26. Hochachka, P. W. (1986). Defense strategies against hypoxia and hypothermia. Science 231, 234-241.
27. Honmyo, I. (2007). A pioneer with strong reliance on advanced technology. Asia Pac. Biotech. News 11, 1033-1035.
28. Hopkins, W. A. (2007). Amphibians as models for studying environmental change. ILAR J. 48, 270-277.
29. Hosack, D. A., Dennis, G., Jr, Sherman, B. T., Lane, H. C. and Lempicki, R. A. (2003). Identifying biological themes within lists of genes with EASE. Genome Biol. 4, R70.
30. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009a). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
31. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009b). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13.
32. Ibarz, A., Martín-Pérez, M., Blasco, J., Bellido, D., de Oliveira, E. and Fernández-Borràs, J. (2010). Gilthead sea bream liver proteome altered at low temperatures by oxidative stress. Proteomics 10, 963-975.
33. Ideker, T., Thorsson, V., Ranish, J. A., Christmas, R., Buhler, J., Eng, J. K., Bumgarner, R., Goodlett, D. R., Aebersold, R. and Hood, L. (2001). Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292, 929-934.
34. Irwin, J. T. and Lee, R. E., Jr. (2003). Geographic variation in energy storage and physiological responses to freezing in the gray treefrogs Hyla versicolor and H. chrysoscelis. J. Exp. Biol. 206, 2859-2867.
35. King, M. W., Neff, A. W. and Mescher, A. L. (2009). Proteomics analysis of regenerating amphibian limbs: changes during the onset of regeneration. Int. J. Dev. Biol. 53, 955-969.
36. Kiss, A. J., Muir, T. J., Lee, R. E., Jr and Costanzo, J. P. (2011). Seasonal variation in the hepatoproteome of the dehydration and freeze-tolerant wood frog, Rana sylvatica. Int. J. Mol. Sci. 12, 8406-8414.
37. Kolkman, A., Daran-Lapujade, P., Fullaondo, A., Olsthoorn, M. M., Pronk, J. T., Slijper, M. and Heck, A. J. (2006). Proteome analysis of yeast response to various nutrient limitations. Mol. Syst. Biol. 2, 2006.0026.
38. Lai, K. K., Kolippakkam, D. and Beretta, L. (2008). Comprehensive and quantitative proteome profiling of the mouse liver and plasma. Hepatology 47, 1043-1051.
39. Maekawa, S., Iemura, H., Kuramochi, Y., Nogawa-Kosaka, N., Nishikawa, H., Okui, T., Aizawa, Y. and Kato, T. (2012). Hepatic confinement of newly produced erythrocytes caused by low-temperature exposure in Xenopus laevis. J. Exp. Biol. 215, 3087-3095.
40. Maier, T., Güell, M. and Serrano, L. (2009). Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583, 3966-3973.
41. Mehra, A., Lee, K. H. and Hatzimanikatis, V. (2003). Insights into the relation between mRNA and protein expression patterns: I. Theoretical considerations. Biotechnol. Bioeng. 84, 822-833.
42. Nogawa-Kosaka, N., Hirose, T., Kosaka, N., Aizawa, Y., Nagasawa, K., Uehara, N., Miyazaki, H., Komatsu, N. and Kato, T. (2010). Structural and biological properties of erythropoietin in Xenopus laevis. Exp. Hematol. 38, 363-372.
43. Nogawa-Kosaka, N., Sugai, T., Nagasawa, K., Tanizaki, Y., Meguro, M., Aizawa, Y., Maekawa, S., Adachi, M., Kuroki, R. and Kato, T. (2011). Identification of erythroid progenitors induced by erythropoietic activity in Xenopus laevis. J. Exp. Biol. 214, 921-927.
44. Nordlie, R. C., Foster, J. D. and Lange, A. J. (1999). Regulation of glucose production by the liver. Annu. Rev. Nutr. 19, 379-406.
45. Oda, T., Shimizu, K., Yamaguchi, A., Satoh, K. and Matsumoto, K. (2012). Hypothermia produces rat liver proteomic changes as in hibernating mammals but decreases endoplasmic reticulum chaperones. Cryobiology 65, 104-112.
46. Okui, T., Yamamoto, Y., Maekawa, S., Nagasawa, K., Yonezuka, Y., Aizawa, Y. and Kato, T. (2013). Quantification and localization of erythropoietin-receptorexpressing cells in the liver of Xenopus laevis. Cell Tissue Res. 353, 153-164.
47. Rao, R. V., Peel, A., Logvinova, A., del Rio, G., Hermel, E., Yokota, T., Goldsmith, P. C., Ellerby, L. M., Ellerby, H. M. and Bredesen, D. E. (2002). Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett. 514, 122-128.
48. Rauen, U., Polzar, B., Stephan, H., Mannherz, H. G. and de Groot, H. (1999). Coldinduced apoptosis in cultured hepatocytes and liver endothelial cells: mediation by reactive oxygen species. FASEB J. 13, 155-168.
49. Rose, J. C., Epperson, L. E., Carey, H. V. and Martin, S. L. (2011). Seasonal liver protein differences in a hibernator revealed by quantitative proteomics using whole animal isotopic labeling. Comp. Biochem. Physiol. 6D, 163-170.
50. Sahyun, M. (1931). Determination of glycogen in tissues. J. Biol. Chem. 93, 227-234.
51. Salt, R. W. (1949). Cold and cold-blooded animals. Can. J. Comp. Med. Vet. Sci. 13, 177-181.
52. Schmid, W. D. (1982). Survival of frogs in low temperature. Science 215, 697-698.
53. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W. and Selbach, M. (2011). Global quantification of mammalian gene expression control. Nature 473, 337-342.
54. Serrano, J., Higgins, L., Witthuhn, B. A., Anderson, L. B., Markowski, T., Holcombe, G.W., Kosian, P. A., Korte, J. J., Tietge, J. E. and Degitz, S. J. (2010). In vivo assessment and potential diagnosis of xenobiotics that perturb the thyroid pathway: Proteomic analysis of Xenopus laevis brain tissue following exposure to model T4 inhibitors. Comp. Biochem. Physiol. 5D, 138-150.
55. Shao, C., Liu, Y., Ruan, H., Li, Y., Wang, H., Kohl, F., Goropashnaya, A. V., Fedorov, V. B., Zeng, R., Barnes, B. M. et al. (2010). Shotgun proteomics analysis of hibernating arctic ground squirrels. Mol. Cell. Proteomics 9, 313-326.
56. Shi, R., Kumar, C., Zougman, A., Zhang, Y., Podtelejnikov, A., Cox, J., Wiśniewski, J. R. and Mann, M. (2007). Analysis of the mouse liver proteome using advanced mass spectrometry. J. Proteome Res. 6, 2963-2972.
57. Silva, J. E. (2006). Thermogenic mechanisms and their hormonal regulation. Physiol. Rev. 86, 435-464.
58. Sonna, L. A., Fujita, J., Gaffin, S. L. and Lilly, C.M. (2002). Invited review: Effects of heat and cold stress on mammalian gene expression. J. Appl. Physiol. 92, 1725-1742.
59. Tabata, T., Sato, T., Kuromitsu, J. and Oda, Y. (2007). Pseudo internal standard approach for label-free quantitative proteomics. Anal. Chem. 79, 8440-8445.
60. Tinsley, R. C. and McCoid, M. J. (1996). Feral populations of Xenopus outside of Africa. In The Biology Of Xenopus (ed. R. C. Tinsley and H. R. Kobel), pp. 81-94. New York, NY: Oxford University Press.
61. Tinsley, R. C., Loumont, C. and Kobel, H. R. (1996). Geographical distribution and ecology. In The Biology Of Xenopus (ed. R. C. Tinsley and H. R. Kobel), pp. 35-60. New York, NY: Oxford University Press.
62. Trzcionka, M., Withers, K. W., Klingenspor, M. and Jastroch, M. (2008). The effects of fasting and cold exposure on metabolic rate and mitochondrial proton leak in liver and skeletal muscle of an amphibian, the cane toad Bufo marinus. J. Exp. Biol. 211, 1911-1918.
63. van Herp, F., van Bakel, N. H., Coenen, A. J., Sergeant, K., Devreese, B. and Martens, G. J. (2008). Physiological manipulation of cellular activity tunes protein and ultrastructural profiles in a neuroendocrine cell. J. Endocrinol. 198, 607-616.
64. Wamelink, M. M., Struys, E. A. and Jakobs, C. (2008). The biochemistry, metabolism and inherited defects of the pentose phosphate pathway: a review. J. Inherit. Metab. Dis. 31, 703-717.
65. Wang, X., Nookala, S., Narayanan, C., Giorgianni, F., Beranova-Giorgianni, S., McCollum, G., Gerling, I., Penn, J. S. and Jablonski, M. M. (2009). Proteomic analysis of the retina: removal of RPE alters outer segment assembly and retinal protein expression. Glia 57, 380-392.