Deciphering the developmental dynamics of the mouse liver transcriptome

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Gunewardena, Sumedha S ^a   Yoo, Byunggil ^b   Peng, Lai ^c   Lu, Hong ^d   Zhong, Xiaobo ^c   Klaassen, Curtis D ^e   Cui, Julia Yue ^e  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b CHILDREN S MERCY HOSPITAL   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GROWTH FACTOR; ION CHANNEL; PHOSPHATASE; PHOSPHOTRANSFERASE; TRANSCRIPTOME; MESSENGER RNA;

AGE; ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENETIC REGULATION; LIVER DEVELOPMENT; MALE; MATURITY; MOLECULAR GENETICS; MOUSE; NONHUMAN; ONTOGENY; POSTNATAL DEVELOPMENT; RNA SEQUENCE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; AGING; ANIMAL; C57BL MOUSE; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; MAMMALIAN EMBRYO; METABOLISM; MORPHOGENESIS; NEWBORN; RNA SPLICING; SEQUENCE ANALYSIS;

AGING; ANIMALS; ANIMALS, NEWBORN; EMBRYO, MAMMALIAN; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIVER; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE ANNOTATION; MORPHOGENESIS; RNA SPLICING; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84949431846     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141220     Document Type: Article

References (71)

1. Wilkinson GR. Drug metabolism and variability among patients in drug response. The New England journal of medicine. 2005; 352(21):2211-21. doi: 10.1056/NEJMra032424 PMID: 15917386.
2. Wei CY, Lee MT, Chen YT. Pharmacogenomics of adverse drug reactions: implementing personalized medicine. Human molecular genetics. 2012; 21(R1):R58-65. doi: 10.1093/hmg/dds341 PMID: 22907657.
3. Nathanson MH, Boyer JL. Mechanisms and regulation of bile secretion. Hepatology. 1991; 14(3):551-66. PMID: 1874500.
4. Levy P. Review of studies on the effect of bile acid sequestrants in patients with type 2 diabetes mellitus. Metabolic syndrome and related disorders. 2010; 8 Suppl 1:S9-13. doi: 10.1089/met.2010.0087 PMID: 20946010.
5. Prawitt J, Caron S, Staels B. Bile acid metabolism and the pathogenesis of type 2 diabetes. Current diabetes reports. 2011; 11(3):160-6. doi: 10.1007/s11892-011-0187-x PMID: 21431855; PubMed Central PMCID: PMC3338411.
6. Suzuki T, Oba K, Igari Y, Watanabe K, Matsumura N, Futami-Suda S, et al. Effects of bile-acid-binding resin (colestimide) on blood glucose and visceral fat in Japanese patients with type 2 diabetes mellitus and hypercholesterolemia: an open-label, randomized, case-control, crossover study. Journal of diabetes and its complications. 2012; 26(1):34-9. doi: 10.1016/j.jdiacomp.2011.11.008 PMID: 22240263.
7. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006; 439(7075):484-9. doi: 10.1038/nature04330 PMID: 16400329.
8. Isaksson OG, Jansson JO, Sjogren K, Ohlsson C. Metabolic functions of liver-derived (endocrine) insulin-like growth factor I. Hormone research. 2001; 55 Suppl 2:18-21. 63468. PMID: 11684870.
9. Sjogren K, Wallenius K, Liu JL, Bohlooly YM, Pacini G, Svensson L, et al. Liver-derived IGF-I is of importance for normal carbohydrate and lipid metabolism. Diabetes. 2001; 50(7):1539-45. PMID: 11423474.
10. Bannister P, Handley T, Chapman C, Losowsky MS. Hypogonadism in chronic liver disease: impaired release of luteinising hormone. British medical journal. 1986; 293(6556):1191-3. PMID: 3096427; PubMed Central PMCID: PMC1341976.
11. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Molecular & cellular proteomics: MCP. 2002; 1(11):845-67. PMID: 12488461.
12. Peters T Jr. Intracellular precursor forms of plasma proteins: their functions and possible occurrence in plasma. Clinical chemistry. 1987; 33(8):1317-25. PMID: 3301066.
13. Maes M, Sokal E, Otte JB. Growth factors in children with end-stage liver disease before and after liver transplantation: a review. Pediatric transplantation. 1997; 1(2):171-5. PMID: 10084777.
14. Stewart SM, Uauy R, Kennard BD, Waller DA, Benser M, Andrews WS. Mental development and growth in children with chronic liver disease of early and late onset. Pediatrics. 1988; 82(2):167-72. PMID: 3399290.
15. Cash WJ, McConville P, McDermott E, McCormick PA, Callender ME, McDougall NI. Current concepts in the assessment and treatment of hepatic encephalopathy. QJM: monthly journal of the Association of Physicians. 2010; 103(1):9-16. doi: 10.1093/qjmed/hcp152 PMID: 19903725.
16. Collier JD, Ninkovic M, Compston JE. Guidelines on the management of osteoporosis associated with chronic liver disease. Gut. 2002; 50 Suppl 1:i1-9. PMID: 11788576; PubMed Central PMCID: PMC1867644.
17. Cordeiro A, Souza LL, Einicker-Lamas M, Pazos-Moura CC. Non-classic thyroid hormone signalling involved in hepatic lipid metabolism. The Journal of endocrinology. 2013; 216(3):R47-57. doi: 10.1530/JOE-12-0542 PMID: 23297113.
18. Ginsberg G, Hattis D, Sonawane B. Incorporating pharmacokinetic differences between children and adults in assessing children's risks to environmental toxicants. Toxicology and applied pharmacology. 2004; 198(2):164-83. doi: 10.1016/j.taap.2003.10.010 PMID: 15236952.
19. Hines RN. The ontogeny of drug metabolism enzymes and implications for adverse drug events. Pharmacology & therapeutics. 2008; 118(2):250-67. doi: 10.1016/j.pharmthera.2008.02.005 PMID: 18406467.
20. Kearns GL, Abdel-Rahman SM, Alander SW, Blowey DL, Leeder JS, Kauffman RE. Developmental pharmacology-drug disposition, action, and therapy in infants and children. The New England journal of medicine. 2003; 349(12):1157-67. doi: 10.1056/NEJMra035092 PMID: 13679531.
21. Naspitz CK, Warner JO. Children are pharmaco-therapeutic orphans. Pediatric allergy and immunology: official publication of the European Society of Pediatric Allergy and Immunology. 2010; 21(2 Pt 1):249-50. doi: 10.1111/j.1399-3038.2010.01044.x PMID: 20444165.
22. Shirkey HC. Therapeutic orphans: who speaks for children? Southern medical journal. 1970; 63 (11):1361-3. PMID: 5475304.
23. Tauer C. Children as research subjects: guinea pigs or therapeutic orphans? Bioethics examiner. 2003; 7(2):1-2, 4-5. PMID: 15025108.
24. Gualdi R, Bossard P, Zheng M, Hamada Y, Coleman JR, Zaret KS. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes & development. 1996; 10(13):1670-82. PMID: 8682297.
25. Hata S, Namae M, Nishina H. Liver development and regeneration: from laboratory study to clinical therapy. Development, growth & differentiation. 2007; 49(2):163-70. doi: 10.1111/j.1440-169X.2007. 00910.x PMID: 17335437.
26. Marie S, Cresteil T. Phenobarbital-inducible gene expression in developing rat liver: relationship to hepatocyte function. Biochimica et biophysica acta. 1989; 1009(3):221-8. PMID: 2480807.
27. Sasaki K, Sonoda Y. Histometrical and three-dimensional analyses of liver hematopoiesis in the mouse embryo. Archives of histology and cytology. 2000; 63(2):137-46. PMID: 10885450.
28. Hines RN, McCarver DG. The ontogeny of human drug-metabolizing enzymes: phase I oxidative enzymes. The Journal of pharmacology and experimental therapeutics. 2002; 300(2):355-60. PMID: 11805191.
29. Leeder JS, Gaedigk R, Marcucci KA, Gaedigk A, Vyhlidal CA, Schindel BP, et al. Variability of CYP3A7 expression in human fetal liver. The Journal of pharmacology and experimental therapeutics. 2005; 314(2):626-35. doi: 10.1124/jpet.105.086504 PMID: 15845858.
30. Vyhlidal CA, Gaedigk R, Leeder JS. Nuclear receptor expression in fetal and pediatric liver: correlation with CYP3A expression. Drug metabolism and disposition: the biological fate of chemicals. 2006; 34 (1):131-7. doi: 10.1124/dmd.105.005967 PMID: 16243958.
31. McLin VA, Zorn AM. Molecular control of liver development. Clinics in liver disease. 2006; 10(1):1-25, v. doi: 10.1016/j.cld.2005.10.002 PMID: 16376792.
32. Li T, Huang J, Jiang Y, Zeng Y, He F, Zhang MQ, et al. Multi-stage analysis of gene expression and transcription regulation in C57/B6 mouse liver development. Genomics. 2009; 93(3):235-42. doi: 10.1016/j.ygeno.2008.10.006 PMID: 19015022; PubMed Central PMCID: PMC2995988.
33. Lee JS, Ward WO, Knapp G, Ren H, Vallanat B, Abbott B, et al. Transcriptional ontogeny of the developing liver. BMC Genomics. 2012; 13:33. doi: 10.1186/1471-2164-13-33 PMID: 22260730; PubMed Central PMCID: PMC3306746.
34. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annual review of biochemistry. 2003; 72:291-336. doi: 10.1146/annurev.biochem.72.121801.161720 PMID: 12626338.
35. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nature genetics. 2008; 40(12):1413-5. doi: 10.1038/ng.259 PMID: 18978789.
36. Miceli V, Cocciadiferro L, Fregapane M, Zarcone M, Montalto G, Polito LM, et al. Expression of wildtype and variant estrogen receptor alpha in liver carcinogenesis and tumor progression. Omics: a journal of integrative biology. 2011; 15(5):313-7. doi: 10.1089/omi.2010.0108 PMID: 21348637.
37. Pellanda H, Namour F, Fofou-Caillierez M, Bressenot A, Alberto JM, Chery C, et al. A splicing variant leads to complete loss of function of betaine-homocysteine methyltransferase (BHMT) gene in hepatocellular carcinoma. The international journal of biochemistry & cell biology. 2012; 44(2):385-92. doi: 10.1016/j.biocel.2011.11.014 PMID: 22138536.
38. Torres-Padilla ME, Fougere-Deschatrette C, Weiss MC. Expression of HNF4alpha isoforms in mouse liver development is regulated by sequential promoter usage and constitutive 3′ end splicing. Mechanisms of development. 2001; 109(2):183-93. PMID: 11731232.
39. Blencowe BJ, Ahmad S, Lee LJ. Current-generation high-throughput sequencing: deepening insights into mammalian transcriptomes. Genes & development. 2009; 23(12):1379-86. doi: 10.1101/gad. 1788009 PMID: 19528315.
40. Fullwood MJ, Wei CL, Liu ET, Ruan Y. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome research. 2009; 19(4):521-32. doi: 10.1101/gr.074906. 107 PMID: 19339662; PubMed Central PMCID: PMC3807531.
41. Cui JY, Gunewardena SS, Yoo B, Liu J, Renaud HJ, Lu H, et al. RNA-Seq reveals different mRNA abundance of transporters and their alternative transcript isoforms during liver development. Toxicological sciences: an official journal of the Society of Toxicology. 2012; 127(2):592-608. doi: 10.1093/toxsci/kfs107 PMID: 22454430; PubMed Central PMCID: PMC3355312.
42. Lu H, Cui JY, Gunewardena S, Yoo B, Zhong XB, Klaassen CD. Hepatic ontogeny and tissue distribution of mRNAs of epigenetic modifiers in mice using RNA-sequencing. Epigenetics: official journal of the DNA Methylation Society. 2012; 7(8):914-29. doi: 10.4161/epi.21113 PMID: 22772165; PubMed Central PMCID: PMC3427287.
43. Peng L, Yoo B, Gunewardena SS, Lu H, Klaassen CD, Zhong XB. RNA sequencing reveals dynamic changes of mRNA abundance of cytochromes P450 and their alternative transcripts during mouse liver development. Drug metabolism and disposition: the biological fate of chemicals. 2012; 40(6):1198-209. doi: 10.1124/dmd.112.045088 PMID: 22434873; PubMed Central PMCID: PMC3362789.
44. Garber M, Grabherr MG, Guttman M, Trapnell C. Computational methods for transcriptome annotation and quantification using RNA-seq. Nature methods. 2011; 8(6):469-77. doi: 10.1038/nmeth.1613 PMID: 21623353.
45. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature methods. 2008; 5(7):621-8. doi: 10.1038/nmeth.1226 PMID: 18516045.
46. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nature reviews Genetics. 2009; 10(1):57-63. doi: 10.1038/nrg2484 PMID: 19015660; PubMed Central PMCID: PMC2949280.
47. Mak HC. Trends in computational biology-2010. Nature biotechnology. 2011; 29(1):45-9. doi: 10.1038/nbt0111-45b PMID: 21221103.
48. Malone JH, Oliver B. Microarrays, deep sequencing and the true measure of the transcriptome. BMC biology. 2011; 9:34. doi: 10.1186/1741-7007-9-34 PMID: 21627854; PubMed Central PMCID: PMC3104486.
49. Li JJ, Jiang CR, Brown JB, Huang H, Bickel PJ. Sparse linear modeling of next-generation mRNA sequencing (RNA-Seq) data for isoform discovery and abundance estimation. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(50):19867-72. doi: 10.1073/pnas.1113972108 PMID: 22135461; PubMed Central PMCID: PMC3250192.
50. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, et al. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science. 2008; 320(5881):1344-9. doi: 10.1126/science.1158441 PMID: 18451266; PubMed Central PMCID: PMC2951732.
51. Araujo PR, Yoon K, Ko D, Smith AD, Qiao M, Suresh U, et al. Before It Gets Started: Regulating Translation at the 5′ UTR. Comp Funct Genomics. 2012; 2012:475731. doi: 10.1155/2012/475731 PMID: 22693426; PubMed Central PMCID: PMC3368165.
52. Tata F, Henry I, Markham AF, Wallis SC, Weil D, Grzeschik KH, et al. Isolation and characterisation of a cDNA clone for human apolipoprotein CI and assignment of the gene to chromosome 19. Hum Genet. 1985; 69(4):345-9. PMID: 2985493.
53. Mullany LK, White P, Hanse EA, Nelsen CJ, Goggin MM, Mullany JE, et al. Distinct proliferative and transcriptional effects of the D-type cyclins in vivo. Cell Cycle. 2008; 7(14):2215-24. PMID: 18635970; PubMed Central PMCID: PMC4000162.
54. Kopin IJ. Monoamine oxidase and catecholamine metabolism. J Neural Transm Suppl. 1994; 41:57-67. PMID: 7931266.
55. Kaakkola S. Clinical pharmacology, therapeutic use and potential of COMT inhibitors in Parkinson's disease. Drugs. 2000; 59(6):1233-50. PMID: 10882160.
56. Wu C, Macleod I, Su AI. BioGPS and MyGene.info: organizing online, gene-centric information. Nucleic acids research. 2013; 41(Database issue):D561-5. doi: 10.1093/nar/gks1114 PMID: 23175613; PubMed Central PMCID: PMC3531157.
57. Kramer A, Green J, Pollard J Jr., Tugendreich S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics. 2014; 30(4):523-30. doi: 10.1093/bioinformatics/btt703 PMID: 24336805; PubMed Central PMCID: PMC3928520.
58. Davidson E, Levin M. Gene regulatory networks. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(14):4935. doi: 10.1073/pnas.0502024102 PMID: 15809445; PubMed Central PMCID: PMC556010.
59. Davidson EH. The regulatory genome: gene regulatory networks in development and evolution. Amsterdam; Boston: Elsevier/Academic Press; 2006. xi, 289 p. p.
60. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature. 2001; 409(6822):860-921. doi: 10.1038/35057062 PMID: 11237011.
61. Sharov AA, Dudekula DB, Ko MS. Genome-wide assembly and analysis of alternative transcripts in mouse. Genome research. 2005; 15(5):748-54. doi: 10.1101/gr.3269805 PMID: 15867436; PubMed Central PMCID: PMC1088304.
62. Roberts A, Pimentel H, Trapnell C, Pachter L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics. 2011; 27(17):2325-9. doi: 10.1093/bioinformatics/btr355 PMID: 21697122.
63. Csanaky IL, Lu H, Zhang Y, Ogura K, Choudhuri S, Klaassen CD. Organic anion-transporting polypeptide 1b2 (Oatp1b2) is important for the hepatic uptake of unconjugated bile acids: Studies in Oatp1b2-null mice. Hepatology. 2011; 53(1):272-81. doi: 10.1002/hep.23984 PMID: 20949553; PubMed Central PMCID: PMC3186067.
64. Stieger B. The role of the sodium-taurocholate cotransporting polypeptide (NTCP) and of the bile salt export pump (BSEP) in physiology and pathophysiology of bile formation. Handb Exp Pharmacol. 2011;(201:):205-59. doi: 10.1007/978-3-642-14541-4-5 PMID: 21103971.
65. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25(9):1105-11. doi: 10.1093/bioinformatics/btp120 PMID: 19289445; PubMed Central PMCID: PMC2672628.
66. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature biotechnology. 2010; 28(5):511-5. doi: 10.1038/nbt.1621 PMID: 20436464; PubMed Central PMCID: PMC3146043.
67. Horn JL. A Rationale and Test for the Number of Factors in Factor Analysis. Psychometrika. 1965; 30:179-85. PMID: 14306381.
68. Durbin J, Watson GS. Testing for serial correlation in least squares regression. III. Biometrika. 1971; 58 (1):1-19.
69. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological). 1995:289-300.
70. Florea L, Song L, Salzberg SL. Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues. F1000Research. 2013; 2:188. doi: 10.12688/f1000research.2-188.v2 PMID: 24555089; PubMed Central PMCID: PMC3892928.
71. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al. The human genome browser at UCSC. Genome research. 2002; 12(6):996-1006. doi: 10.1101/gr.229102 Article published online before print in May 2002. PMID: 12045153; PubMed Central PMCID: PMC186604.