Proteomic characteristics of the liver and skeletal muscle in the Chinese tree shrew (Tupaia belangeri chinensis)

Abstract

Valid animal models are useful for studying the pathophysiology of specific disorders, such as neural disease, diabetes and cancer. Previous molecular phylogeny studies indicate that the tree shrew is in the same order as (or a close sister to) primates, and thus may be an ideal model in which to study human disease. In this study, the proteome of liver and muscle tissue in tree the shrew was identified by combining peptide fractionation and LC-MS/MS identification. In total, 2146 proteins were detected, including 1759 proteins in liver samples and 885 proteins in skeletal muscle samples from the tree shrew. Further sub-source analysis revealed that nearly half of the identified proteins (846 proteins and 418 proteins) were derived from human database. In this study, we are the first to describe the characteristics of the proteome from the liver and skeletal muscle of the tree shrew. Phylogenetic tree analysis based on these proteomic data showed that the tree shrew is closer to primates (human) than to glires (the mouse and rat).

Keywords

proteome / Chinese tree shrew / phylogenetic tree / liver / muscle

References

[1] Abascal, F., Zardoya, R., and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105 .10.1093/bioinformatics/bti263
[2] Arnason, U., Adegoke, J.A., Bodin, K., Born, E.W., Esa, Y.B., Gullberg, A., Nilsson, M., Short, R.V., Xu, X., and Janke, A. (2002). Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci U S A 99, 8151-8156 .10.1073/pnas.102164299
[3] Cao, J., Yang, E.B., Su, J.J., Li, Y., and Chow, P. (2003). The tree shrews: adjuncts and alternatives to primates as models for biomedical research. J Med Primatol 32, 123-130 .10.1034/j.1600-0684.2003.00022.x
[4] Deng, W.J., Nie, S., Dai, J., Wu, J.R., and Zeng, R. (2010). Proteome, phosphoproteome, and hydroxyproteome of liver mitochondria in diabetic rats at early pathogenic stages. Mol Cell Proteomics 9, 100-116 .10.1074/mcp.M900020-MCP200
[5] Helgen, K.M., Wilson, Don E, Reeder, and DeeAnn M. (2005). Mammal Species of the World (3rd ed.). Baltimore: Johns Hopkins University Press, 104-109 .
[6] Janecka, J.E., Miller, W., Pringle, T.H., Wiens, F., Zitzmann, A., Helgen, K.M., Springer, M.S., and Murphy, W.J. (2007). Molecular and genomic data identify the closest living relative of primates. Science 318, 792-794 .10.1126/science.1147555
[7] Kennedy, R.T., and Jorgenson, J.W. (1989). Quantitative analysis of individual neurons by open tubular liquid chromatography with voltammetric detection. Anal Chem 61, 436-441 .10.1021/ac00180a012
[8] Lescuyer, P., Hochstrasser, D.F., and Sanchez, J.C. (2004). Comprehensive proteome analysis by chromatographic protein prefractionation. Electrophoresis 25, 1125-1135 .10.1002/elps.200305792
[9] Li, C., Ruan, H.Q., Liu, Y.S., Xu, M.J., Dai, J., Sheng, Q.H., Tan, Y.X., Yao, Z.Z., Wang, H.Y., Wu, J.R., . (2011). Quantitative proteomics reveal up-regulated protein expression of the SET complex associated with hepatocellular carcinoma. J Proteome Res 11, 871-885 .10.1021/pr2006999
[10] Liu, Y., Li, C., Xing, Z., Yuan, X., Wu, Y., Xu, M., Tu, K., Li, Q., Wu, C., Zhao, M., . (2010). Proteomic mining in the dysplastic liver of WHV/c-myc mice--insights and indicators for early hepatocarcinogenesis. FEBS J 277, 4039-4053 .10.1111/j.1742-4658.2010.07795.x
[11] Lu, W.D., Li, B.Y., Yu, F., Cai, Q., Zhang, Z., Yin, M., and Gao, H.Q. (2012). Quantitative proteomics study on the protective mechanism of phlorizin on hepatic damage in diabetic db/db mice. Mol Med Report 5, 1285-1294 .
[12] Murphy, W.J., Eizirik, E., O'Brien, S.J., Madsen, O., Scally, M., Douady, C.J., Teeling, E., Ryder, O.A., Stanhope, M.J., de Jong, W.W., . (2001). Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348-2351 .10.1126/science.1067179
[13] Nielsen, P.A., Olsen, J.V., Podtelejnikov, A.V., Andersen, J.R., Mann, M., and Wisniewski, J.R. (2005). Proteomic mapping of brain plasma membrane proteins. Mol Cell Proteomics 4, 402-408 .10.1074/mcp.T500002-MCP200
[14] Orengo, J.P., and Cooper, T.A. (2007). Alternative splicing in disease. Adv Exp Med Biol 623, 212-223 .10.1007/978-0-387-77374-2_13
[15] Perkins, D.N., Pappin, D.J., Creasy, D.M., and Cottrell, J.S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 .10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2
[16] Rappsilber, J., Mann, M., and Ishihama, Y. (2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat protoc 2, 1896-1906 .10.1038/nprot.2007.261
[17] Schmitz, J., Ohme, M., and Zischler, H. (2000). The complete mitochondrial genome of Tupaia belangeri and the phylogenetic affiliation of scandentia to other eutherian orders. Mol Biol Evol 17, 1334-1343 .10.1093/oxfordjournals.molbev.a026417
[18] Shevchenko, A., Jensen, O.N., Podtelejnikov, A.V., Sagliocco, F., Wilm, M., Vorm, O., Mortensen, P., Boucherie, H., and Mann, M. (1996). Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci U S A 93, 14440-14445 .10.1073/pnas.93.25.14440
[19] Staunton, L., Jockusch, H., and Ohlendieck, K. (2011). Proteomic analysis of muscle affected by motor neuron degeneration: the wobbler mouse model of amyotrophic lateral sclerosis. Biochem Biophys Res Commun 406, 595-600 .10.1016/j.bbrc.2011.02.099
[20] Tieleman, A.A., den Broeder, A.A., van de Logt, A.E., and van Engelen, B.G. (2009). Strong association between myotonic dystrophy type 2 and autoimmune diseases. J Neurol Neurosurg Psychiatry 80, 1293-1295 .10.1136/jnnp.2008.156562
[21] van der Worp, H.B., Howells, D.W., Sena, E.S., Porritt, M.J., Rewell, S., O'Collins, V., and Macleod, M.R. (2010). Can animal models of disease reliably inform human studies?PLoS Med 7, e1000245.10.1371/journal.pmed.1000245
[22] Wang, J., Zhou, Q.X., Tian, M., Yang, Y.X., and Xu, L. (2011). Tree shrew models: a chronic social defeat model of depression and a one-trial captive conditioning model of learning and memory. Dongwuxue Yanjiu 32, 24-30 .
[23] Wilkins, M.R., Sanchez, J.C., Williams, K.L., and Hochstrasser, D.F. (1996). Current challenges and future applications for protein maps and post-translational vector maps in proteome projects. Electrophoresis 17, 830-838 .10.1002/elps.1150170504
[24] Wilm, M., and Mann, M. (1996). Analytical properties of the nanoenanoelectrospray ion source. Anal Chem 68, 1-8 .10.1021/ac9509519
[25] Wisniewski, J.R., Zougman, A., Nagaraj, N., and Mann, M. (2009). Universal sample preparation method for proteome analysis. Nat Methods 6, 359-362 .10.1038/nmeth.1322
[26] Wu, C.Y., Whye, D., Glazewski, L., Choe, L., Kerr, D., Lee, K.H., Mason, R.W., and Wang, W. (2011). Proteomic assessment of a cell model of spinal muscular atrophy. BMC Neurosci 12, 25.10.1186/1471-2202-12-25
[27] Xu, L., Chen, S.Y., Nie, W.H., Jiang, X.L., and Yao, Y.G. (2012). Evaluating the phylogenetic position of Chinese tree shrew (Tupaia belangeri chinensis) based on complete mitochondrial genome: implication for using tree shrew as an alternative experimental animal to primates in biomedical research. J Genet Genomics 39, 131-137 .10.1016/j.jgg.2012.02.003
[28] Zhang, H., Stoeckli, M., Andren, P.E., and Caprioli, R.M. (1999). Combining solid-phase preconcentration, capillary electrophoresis and off-line matrix-assisted laser desorption/ionization mass spectrometry: intracerebral metabolic processing of peptide E in vivo. J Mass Spectrom 34, 377-383 .10.1002/(SICI)1096-9888(199904)34:4<377::AID-JMS778>3.0.CO;2-D