DOI: 10.3724/SP.J.1141.2013.E02E35

Zoological Research (动物学研究) 2013/34:2 PP.E35-E41

Comparative systems biology between human and animal models based on next-generation sequencing methods

Animal models provide myriad benefits to both experimental and clinical research. Unfortunately, in many situations, they fall short of expected results or provide contradictory results. In part, this can be the result of traditional molecular biological approaches that are relatively inefficient in elucidating underlying molecular mechanism. To improve the efficacy of animal models, a technological breakthrough is required. The growing availability and application of the high-throughput methods make systematic comparisons between human and animal models easier to perform. In the present study, we introduce the concept of the comparative systems biology, which we define as “comparisons of biological systems in different states or species used to achieve an integrated understanding of life forms with all their characteristic complexity of interactions at multiple levels”. Furthermore, we discuss the applications of RNA-seq and ChIP-seq technologies to comparative systems biology between human and animal models and assess the potential applications for this approach in the future studies.

Key words:Animal models,Comparative systems biology,Next-generation sequencing,RNA-seq,ChIP-seq

ReleaseDate:2015-04-16 19:34:19

Akkers RC, van Heeringen SJ, Jacobi UG, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Veenstra GJC. 2009. A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus Embryos. Dev Cell, 17(3): 425-434.

Alini M, Eisenstein SM, Ito K, Little C, Kettler AA, Masuda K, Melrose J, Ralphs J, Stokes I, Wilke HJ. 2008. Are animal models useful for studying human disc disorders/degeneration? Eur Spine J, 17(1): 2-19.

Alvarado AS, Tsonis PA. 2006. Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet, 7(11): 873-884.

Barabasi AL, Gulbahce N, Loscalzo J. 2011. Network medicine: a network-based approach to human disease. Nate Rev Genet, 12(1): 56-68.

Benfey PN, Mitchell-Olds T. 2008. From genotype to phenotype: Systems biology meets natural variation. Science, 320(5875): 495-497.

Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng ZP, Snyder M, Dermitzakis ET, Stamatoyannopoulos JA and others. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature, 447(7146): 799-816.

Birol I, Jackman SD, Nielsen CB, Qian JQ, Varhol R, Stazyk G, Morin RD, Zhao YJ, Hirst M, Schein JE, Horsman DE, Connors JM, Gascoyne RD, Marra MA, Jones SJM. 2009. De novo transcriptome assembly with ABySS. Bioinformatics, 25(21): 2872-2877.

Blow MJ, McCulley DJ, Li ZR, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F and others. 2010. ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet, 42(9): 806-810.

Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M and others. 2011. The evolution of gene expression levels in mammalian organs. Nature, 478(7369): 343-348.

Brown S, Teo A, Pauklin S, Hannan N, Cho CHH, Lim B, Vardy L, Dunn NR, Trotter M, Pedersen R and others. 2011. Activin/nodal signaling controls divergent transcriptional networks in human embryonic stem cells and in endoderm progenitors. Stem Cells, 29(8): 1176-1185.

Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, Piccolboni A, Sementchenko V, Cheng J, Williams AJ and others. 2004. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell, 116(4): 499-509.

Chakraborty C, Hsu CH, Wen ZH, Lin CS, Agoramoorthy G. 2009. Zebrafish: A complete animal model for in vivo drug discovery and development. Curr Drug Metab, 10(2): 116-124.

Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang WW, Jiang JM and others. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell, 133(6): 1106-1117.

Cox B, Kotlyar M, Evangelou AI, Ignatchenko V, Ignatchenko A, Whiteley K, Jurisica I, Adamson SL, Rossant J, Kislinger T. 2009. Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol, 5: 279.

Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, Giavalisco P, Nieselt-Struwe K, Muchmore E, Varki A, Ravid R and others. 2002. Intra-and interspecific variation in primate gene expression patterns. Science, 296(5566): 340-343.

Faith JJ, McNulty NP, Rey FE, Gordon JI. 2011. Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science, 333(6038): 101-104.

Farmer MA, Baliki MN, Apkarian AV. 2012. A dynamic network perspective of chronic pain. Neurosci Lett, 520(2): 197-203.

Francia G, Cruz-Munoz W, Man S, Xu P, Kerbel RS. 2011. Mouse models of advanced spontaneous metastasis for experimental therapeutics. Nat Rev Cancer, 11(2): 135-141.

Friese MA, Montalban X, Willcox N, Bell JI, Martin R, Fugger L. 2006. The value of animal models for drug development in multiple sclerosis. Brain, 129(8): 1940-1952.

Fuentes R, Petersson P, Siesser WB, Caron MG, Nicolelis MAL. 2009. Spinal cord stimulation restores locomotion in animal models of Parkinson's disease. Science, 323(5921): 1578-1582.

Garber M, Grabherr MG, Guttman M, Trapnell C. 2011. Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods, 8(6): 469-477.

Gianchandani EP, Brautigan DL, Papin JA. 2006. Systems analyses characterize integrated functions of biochemical networks. Trends Biochem Sci, 31(5): 284-291.

Gottesman II, Hanson DR. 2005. Human development: Biological and genetic processes. Annu Rev Psychol, 56(1): 263-286.

Götz J, Ittner LM. 2008. Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci, 9(7): 532-544.

Greber B, Wu GM, Bernemann C, Joo JY, Han DW, Ko K, Tapia N, Sabour D, Sterneckert J, Tesar P and others. 2010. Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell, 6(3): 215-226.

Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C and others. 2010. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol, 28(5): 503-510.

Hasenfuss G. 1998. Animal models of human cardiovascular disease, heart failure and hypertrophy. Cardiovasc Res, 39(1): 60-76.

Heintzman ND, Stuart RK, Hon G, Fu YT, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu CX, Ching KA and others. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet, 39(3): 311-318.

Henkelman RM. 2010. Systems biology through mouse imaging centers: experience and new directions. Annu Rev Biomed Eng, 12(1): 143-166.

Ho JWK, Bishop E, Karchenko PV, Negre N, White KP, Park PJ. 2011. ChIP-chip versus ChIP-seq: Lessons for experimental design and data analysis. Bmc Genomics, 12: 134.

Huh Y, Ju MS, Park H, Han SJ, Bang YM, Ferris CF, Koppe GA, King JA, Kim ML, Kim DJ and others. 2010. Clavulanic acid protects neurons in pharmacological models of neurodegenerative diseases. Drug Develop Res, 71(6): 351-357.

Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A and others. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature, 431(7011): 946-957.

Johnson DS, Mortazavi A, Myers RM, Wold B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science, 316(5830): 1497-1502.

Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, Green RD, Zhang MQ, Lobanenkov VV, Ren B. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell, 128(6): 1231-1245.

Liao BY, Zhang JZ. 2006. Evolutionary conservation of expression profiles between human and mouse orthologous genes. Mol Biol Evol, 23(3): 530-540.

Liao BY, Zhang JZ. 2008. Null mutations in human and mouse orthologs frequently result in different phenotypes. Proc Natl Acad Sci USA, 105(19): 6987-6992.

Lieschke GJ, Currie PD. 2007. Animal models of human disease: zebrafish swim into view. Nat Rev Genet, 8(5): 353-367.

Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. 2011. Epigenetics in alternative Pre-mRNA splicing. Cell, 144(1): 16-26.

Macilwain C. 2011. Systems biology: evolving into the mainstream. Cell, 144(6): 839-841.

Mardis ER. 2007. ChIP-seq: welcome to the new frontier. Nat Methods, 4(8): 613-614.

Marques AC, Vinckenbosh N, Brawand D, Kaessmann H. 2008. Functional diversification of duplicate genes through subcellular adaptation of encoded proteins. Genome Biol, 9(3): 5R4.

McGaughey DM, Vinton RM, Huynh J, Al-Saif A, Beer MA, McCallion AS. 2008. Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b. Genome Res, 18(2): 252-260.

Merchenthaler I, Shughrue PJ. 2005. Neuroprotection by estrogen in animal models of ischemia and Parkinson's disease. Drug Develop Res, 66(2): 172-181.

Miller JA, Horvath S, Geschwind DH. 2010. Divergence of human and mouse brain transcriptome highlights Alzheimer disease pathways. Proc Natl Acad Sci USA, 107(28): 12698-12703.

Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods, 5(7): 621-628.

Nestler EJ, Hyman SE. 2010. Animal models of neuropsychiatric disorders. Nat Neurosci, 13(10): 1161-1169.

Northoff G. 2009. Comparison between animal models and human imaging findings in major depressive disorder-convergences and divergences. Biol Psychiat, 65(8): 18S-18S.

Ogawa Y, Arakawa K, Kaizu K, Miyoshi F, Nakayama Y, Tomita M. 2008. Comparative study of circadian oscillatory network models of Drosophila. Artif Life, 14(1): 29-48.

Park PJ. 2009. ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet, 10(10): 669-680.

Pokholok DK, Zeitlinger J, Hannett NM, Reynolds DB, Young RA. 2006. Activated signal transduction kinases frequently occupy target genes. Science, 313(5786): 533-536.

Rowley JW, Oler AJ, Tolley ND, Hunter BN, Low EN, Nix DA, Yost CC, Zimmerman GA, Weyrich AS. 2011. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood, 118(14): E101-E111.

Schmid CD, Bucher P. 2007. ChIP-Seq data reveal nucleosome architecture of human promoters. Cell, 131(5): 831-832.

Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, Kutter C, Watt S, Martinez-Jimenez CP, Mackay S and others. 2010. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science, 328(5981): 1036-1040.

Schulz MH, Zerbino DR, Vingron M, Birney E. 2012. Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics, 28(8): 1086-1092.

Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol, 28(5): 511-515.

van den Heuvel S, Dyson NJ. 2008. Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Bio, 9(9): 713-724.

Visel A, Blow MJ, Li ZR, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F and others. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature, 457(7231): 854-858.

Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet, 10(1): 57-63.

Werner E. 2007. All systems go. Nature, 446(7135): 493-494.

Yanai I, Graur D, Ophir R. 2004. Incongruent expression profiles between human and mouse orthologous genes suggest widespread neutral evolution of transcription control. Omics, 8(1): 15-24.

Zhao YQ, Sheng ZZ, Huang JF. 2012. A systematic analysis of heart transcriptome highlights divergent cardiovascular disease pathways between animal models and humans. Mol Biosyst, 8(2): 504-510.

Zhu XW, Gerstein M, Snyder M. 2007. Getting connected: analysis and principles of biological networks. Gene Dev, 21(9): 1010-1024.