Tissue-specific expression and regulatory networks of pig microRNAome

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Martini, Paolo ^a   Sales, Gabriele ^a   Brugiolo, Mattia ^a   Gandaglia, Alessandro ^a   Naso, Filippo ^a   De Pittà, Cristiano ^a   Spina, Michele ^a   Gerosa, Gino ^a   Chemello, Francesco ^a   Romualdi, Chiara ^a   Cagnin, Stefano ^a   Lanfranchi, Gerolamo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; BIOLOGICAL MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CELLULAR DISTRIBUTION; CLUSTER ANALYSIS; COMPUTER MODEL; COMPUTER PREDICTION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC CONSERVATION; GENETIC CORRELATION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOMICS; HEART MUSCLE; LEUKOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA GENE; RNA SEQUENCE; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; SWINE; TISSUE DISTRIBUTION; VALIDATION STUDY; ANIMAL; ANTIBODY SPECIFICITY; BASE PAIRING; BIOLOGY; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; MOLECULAR GENETICS; MOUSE; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BASE PAIRING; BASE SEQUENCE; BIOLOGICAL MARKERS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SWINE;

EID: 84899127253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089755     Document Type: Article

References (94)

1. Wu CI, Li WH (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A 82: 1741-1745.
2. Huang PL (2009) eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 20: 295-302.
3. Granada JF, Kaluza GL, Wilensky RL, Biedermann BC, Schwartz RS, et al. (2009) Porcine models of coronary atherosclerosis and vulnerable plaque for imaging and interventional research. EuroIntervention 5: 140-148.
4. Zhang Q, Widmer G, Tzipori S (2013) A pig model of the human gastrointestinal tract. Gut Microbes 4: 193-200.
5. Kragh PM, Nielsen AL, Li J, Du Y, Lin L, et al. (2009) Hemizygous minipigs produced by random gene insertion and handmade cloning express the Alzheimer's disease-causing dominant mutation APPsw. Transgenic Res 18: 545-558.
6. Ross JW, Fernandez de Castro JP, Zhao J, Samuel M, Walters E, et al. (2012) Generation of an inbred miniature pig model of retinitis pigmentosa. Invest Ophthalmol Vis Sci 53: 501-507.
7. Maxmen A (2012) Model pigs face messy path. Nature 486: 453.
8. Sandrin MS, Loveland BE, McKenzie IF (2001) Genetic engineering for xenotransplantation. J Card Surg 16: 448-457. (Pubitemid 34242385)
9. Ekser B, Rigotti P, Gridelli B, Cooper DK (2009) Xenotransplantation of solid organs in the pig-to-primate model. Transpl Immunol 21: 87-92.
10. Valdes-Gonzalez RA, Dorantes LM, Garibay GN, Bracho-Blanchet E, Mendez AJ, et al. (2005) Xenotransplantation of porcine neonatal islets of Langerhans and Sertoli cells: a 4-year study. Eur J Endocrinol 153: 419-427. (Pubitemid 41410499)
11. Kadner A, Chen RH, Adams DH (2000) Heterotopic heart transplantation: experimental development and clinical experience. Eur J Cardiothorac Surg 17: 474-481. (Pubitemid 30204499)
12. Fosse J, Seegers H, Magras C (2009) Prevalence and risk factors for bacterial food-borne zoonotic hazards in slaughter pigs: a review. Zoonoses Public Health 56: 429-454.
13. Wellcome Trust Sanger Institute website. Available: http://www.sanger.ac. uk/resources/downloads/othervertebrates/pig.html. Accessed 2013 Jun 15.
14. Li M, Wu H, Luo Z, Xia Y, Guan J, et al. (2012) An atlas of DNA methylomes in porcine adipose and muscle tissues. Nat Commun 3: 850.
15. Dawson HD, Loveland JE, Pascal G, Gilbert JG, Uenishi H, et al. (2013) Structural and functional annotation of the porcine immunome. BMC Genomics 14: 332.
16. Fairbairn L, Kapetanovic R, Beraldi D, Sester DP, Tuggle CK, et al. (2013) Comparative Analysis of Monocyte Subsets in the Pig. J Immunol 190: 6389-6396.
17. Martins RP, Lorenzi V, Arce C, Lucena C, Carvajal A, et al. (2013) Innate and adaptive immune mechanisms are effectively induced in ileal Peyer's patches of Salmonella typhimurium infected pigs. Dev Comp Immunol 41: 100-104.
18. Hulst M, Smits M, Vastenhouw S, de Wit A, Niewold T, et al. (2013) Transcription networks responsible for early regulation of Salmonella-induced inflammation in the jejunum of pigs. J Inflamm (Lond) 10: 18.
19. Adler M, Murani E, Brunner R, Ponsuksili S, Wimmers K (2013) Transcriptomic response of porcine PBMCs to vaccination with tetanus toxoid as a model antigen. PLoS One 8: e58306.
20. Freeman TC, Ivens A, Baillie JK, Beraldi D, Barnett MW, et al. (2012) A gene expression atlas of the domestic pig. BMC Biol 10: 90.
21. Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139.
22. McDaneld TG, Smith TP, Harhay GP, Wiedmann RT (2012) Next-generation sequencing of the porcine skeletal muscle transcriptome for computational prediction of microRNA gene targets. PLoS One 7: e42039.
23. Zhou B, Liu HL, Shi FX, Wang JY (2010) MicroRNA expression profiles of porcine skeletal muscle. Anim Genet 41: 499-508.
24. Liu Y, Li M, Ma J, Zhang J, Zhou C, et al. (2013) Identification of differences in microRNA transcriptomes between porcine oxidative and glycolytic skeletal muscles. BMC Mol Biol 14: 7.
25. Siengdee P, Trakooljul N, Murani E, Schwerin M, Wimmers K, et al. (2013) Transcriptional profiling and miRNA-dependent regulatory network analysis of longissimus dorsi muscle during prenatal and adult stages in two distinct pig breeds. Anim Genet 44: 398-407.
26. McDaneld TG, Smith TP, Doumit ME, Miles JR, Coutinho LL, et al. (2009) MicroRNA transcriptome profiles during swine skeletal muscle development. BMC Genomics 10: 77.
27. Huang TH, Zhu MJ, Li XY, Zhao SH (2008) Discovery of porcine microRNAs and profiling from skeletal muscle tissues during development. PLoS One 3: e3225.
28. Timoneda O, Balcells I, Nunez JI, Egea R, Vera G, et al. (2013) miRNA expression profile analysis in kidney of different porcine breeds. PLoS One 8: e55402.
29. Li A, Song T, Wang F, Liu D, Fan Z, et al. (2012) MicroRNAome and expression profile of developing tooth germ in miniature pigs. PLoS One 7: e52256.
30. Sharbati S, Friedlander MR, Sharbati J, Hoeke L, Chen W, et al. (2010) Deciphering the porcine intestinal microRNA transcriptome. BMC Genomics 11: 275.
31. Podolska A, Kaczkowski B, Kamp Busk P, Sokilde R, Litman T, et al. (2011) MicroRNA expression profiling of the porcine developing brain. PLoS One 6: e14494.
32. Zhou Y, Tang X, Song Q, Ji Y, Wang H, et al. (2013) Identification and characterization of pig embryo microRNAs by Solexa sequencing. Reprod Domest Anim 48: 112-120.
33. Lian C, Sun B, Niu S, Yang R, Liu B, et al. (2012) A comparative profile of the microRNA transcriptome in immature and mature porcine testes using Solexa deep sequencing. FEBS J 279: 964-975.
34. Li M, Liu Y, Wang T, Guan J, Luo Z, et al. (2011) Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing. Int J Biol Sci 7: 1045-1055.
35. Curry E, Safranski TJ, Pratt SL (2011) Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76: 1532-1539.
36. Luo L, Ye L, Liu G, Shao G, Zheng R, et al. (2010) Microarray-based approach identifies differentially expressed microRNAs in porcine sexually immature and mature testes. PLoS One 5: e11744.
37. Li H, Xi Q, Xiong Y, Cheng X, Qi Q, et al. (2011) A comprehensive expression profile of microRNAs in porcine pituitary. PLoS One 6: e24883.
38. Li HY, Xi QY, Xiong YY, Liu XL, Cheng X, et al. (2012) Identification and comparison of microRNAs from skeletal muscle and adipose tissues from two porcine breeds. Anim Genet 43: 704-713.
39. Chen C, Ai H, Ren J, Li W, Li P, et al. (2011) A global view of porcine transcriptome in three tissues from a full-sib pair with extreme phenotypes in growth and fat deposition by paired-end RNA sequencing. BMC Genomics 12: 448.
40. Xie SS, Li XY, Liu T, Cao JH, Zhong Q, et al. (2011) Discovery of porcine microRNAs in multiple tissues by a Solexa deep sequencing approach. PLoS One 6: e16235.
41. Li M, Xia Y, Gu Y, Zhang K, Lang Q, et al. (2010) MicroRNAome of porcine pre- and postnatal development. PLoS One 5: e11541.
42. Martini P, Sales G, Calura E, Brugiolo M, Lanfranchi G, et al. (2013) Systems Biology Approach to the Dissection of the Complexity of Regulatory Networks in the S. scrofa Cardiocirculatory System. Int J Mol Sci 14: 23160-23187.
43. Nelson PT, Baldwin DA, Scearce LM, Oberholtzer JC, Tobias JW, et al. (2004) Microarray-based, high-throughput gene expression profiling of microRNAs. Nat Methods 1: 155-161.
44. Berezikov E, van Tetering G, Verheul M, van de Belt J, van Laake L, et al. (2006) Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysis. Genome Res 16: 1289-1298. (Pubitemid 44506962)
45. Alexiou P, Maragkakis M, Papadopoulos GL, Reczko M, Hatzigeorgiou AG (2009) Lost in translation: an assessment and perspective for computational microRNA target identification. Bioinformatics 25: 3049-3055.
46. Xue C, Li F, He T, Liu GP, Li Y, et al. (2005) Classification of real and pseudo microRNA precursors using local structure-sequence features and support vector machine. BMC Bioinformatics 6: 310.
47. Helvik SA, Snove O Jr, Saetrom P (2007) Reliable prediction of Drosha processing sites improves microRNA gene prediction. Bioinformatics 23: 142-149. (Pubitemid 46189602)
48. Kim J, Cho IS, Hong JS, Choi YK, Kim H, et al. (2008) Identification and characterization of new microRNAs from pig. Mamm Genome 19: 570-580.
49. Kim HJ, Cui XS, Kim EJ, Kim WJ, Kim NH (2006) New porcine microRNA genes found by homology search. Genome 49: 1283-1286.
50. Li M, Xia Y, Gu Y, Zhang K, Lang Q, et al. (2010) MicroRNAome of porcine pre- and postnatal development. PLoS One 5: e11541.
51. Nielsen M, Hansen JH, Hedegaard J, Nielsen RO, Panitz F, et al. (2010) MicroRNA identity and abundance in porcine skeletal muscles determined by deep sequencing. Anim Genet 41: 159-168.
52. Suzuki Y, Yeung AC, Ikeno F (2011) The representative porcine model for human cardiovascular disease. J Biomed Biotechnol 2011: 195483.
53. Stangl K, Gunther C, Frank T, Lorenz M, Meiners S, et al. (2002) Inhibition of the ubiquitin-proteasome pathway induces differential heat-shock protein response in cardiomyocytes and renders early cardiac protection. Biochem Biophys Res Commun 291: 542-549. (Pubitemid 34687378)
54. Dudley AM, Aach J, Steffen MA, Church GM (2002) Measuring absolute expression with microarrays with a calibrated reference sample and an extended signal intensity range. Proc Natl Acad Sci U S A 99: 7554-7559. (Pubitemid 34568729)
55. Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, et al. (2004) Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5: R68.
56. Liang Y, Ridzon D, Wong L, Chen C (2007) Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 8: 166.
57. Cagnin S, Biscuola M, Patuzzo C, Trabetti E, Pasquali A, et al. (2009) Reconstruction and functional analysis of altered molecular pathways in human atherosclerotic arteries. BMC Genomics 10: 13.
58. McGregor CG, Carpentier A, Lila N, Logan JS, Byrne GW (2011) Cardiac xenotransplantation technology provides materials for improved bioprosthetic heart valves. J Thorac Cardiovasc Surg 141: 269-275.
59. Rajani R, Mukherjee D, Chambers JB (2007) Doppler echocardiography in normally functioning replacement aortic valves: a review of 129 studies. J Heart Valve Dis 16: 519-535. (Pubitemid 47527402)
60. Reddy AM, Zheng Y, Jagadeeswaran G, Macmil SL, Graham WB, et al. (2009) Cloning, characterization and expression analysis of porcine microRNAs. BMC Genomics 10: 65.
61. Brattelid T, Aarnes EK, Helgeland E, Guvag S, Eichele H, et al. (2011) The Normalization Strategy is Critical for the Outcome of miRNA Expression Analyses in the Rat Heart. Physiol Genomics 43: 604-10.
62. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, et al. (2005) A microRNA polycistron as a potential human oncogene. Nature 435: 828-833. (Pubitemid 40839734)
63. Zhao JJ, Lin J, Lwin T, Yang H, Guo J, et al. (2010) microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood 115: 2630-2639.
64. Foucar K, Reichard K, Czuchlewski D (2010) Bone Marrow Pathology, Third Ed. 2.
65. Kronick MN (2004) Creation of the whole human genome microarray. Expert Rev Proteomics 1: 19-28.
66. Sales G, Coppe A, Bisognin A, Biasiolo M, Bortoluzzi S, et al. (2010) MAGIA, a web-based tool for miRNA and Genes Integrated Analysis. Nucleic Acids Res 38: W352-359.
67. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115: 787-798. (Pubitemid 38058492)
68. Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154: 26-46.
69. Fatica A, Bozzoni I (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15: 7-21.
70. Xu S, Zhao L, Larsson A, Venge P (2009) The identification of a phospholipase B precursor in human neutrophils. FEBS J 276: 175-186.
71. Kikuchi K, Poss KD (2012) Cardiac regenerative capacity and mechanisms. Annu Rev Cell Dev Biol 28: 719-741.
72. Yada H, Murata M, Shimoda K, Yuasa S, Kawaguchi H, et al. (2007) Dominant negative suppression of Rad leads to QT prolongation and causes ventricular arrhythmias via modulation of L-type Ca2+ channels in the heart. Circ Res 101: 69-77. (Pubitemid 47094625)
73. Mayr JA, Merkel O, Kohlwein SD, Gebhardt BR, Bohles H, et al. (2007) Mitochondrial phosphate-carrier deficiency: a novel disorder of oxidative phosphorylation. Am J Hum Genet 80: 478-484.
74. Stark C, Breitkreutz BJ, Chatr-Aryamontri A, Boucher L, Oughtred R, et al. (2011) The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 39: D698-704.
75. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, et al. (2003) A uniform system for microRNA annotation. RNA 9: 277-279. (Pubitemid 36246165)
76. Bissels U, Wild S, Tomiuk S, Holste A, Hafner M, et al. (2009) Absolute quantification of microRNAs by using a universal reference. RNA 15: 2375-2384.
77. Ma Y, Chen Y, Yang Y, Chen B, Liu D, et al. (2013) Proteasome inhibition attenuates heart failure during the late stages of pressure overload through alterations in collagen expression. Biochem Pharmacol 85: 223-233.
78. Miller E, Hoschler K, Hardelid P, Stanford E, Andrews N, et al. (2010) Incidence of 2009 pandemic influenza A H1N1 infection in England: a cross-sectional serological study. Lancet 375: 1100-1108.
79. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, et al. (2005) A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 65: 9628-9632. (Pubitemid 41541436)
80. Cox MB, Cairns MJ, Gandhi KS, Carroll AP, Moscovis S, et al. (2010) MicroRNAs miR-17 and miR-20a inhibit T cell activation genes and are under-expressed in MS whole blood. PLoS One 5: e12132.
81. McGraw-Hill (2005) McGraw-Hill concise encyclopedia of bioscience. New York: McGraw-Hill. 972 p.
82. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, et al. (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208. (Pubitemid 37329583)
83. Guo L, Lu Z (2010) The fate of miRNA*strand through evolutionary analysis: implication for degradation as merely carrier strand or potential regulatory molecule? PLoS One 5: e11387.
84. Pillai RS (2005) MicroRNA function: multiple mechanisms for a tiny RNA? RNA 11: 1753-1761.
85. Lu Y, Zhang Y, Wang N, Pan Z, Gao X, et al. (2010) MicroRNA-328 contributes to adverse electrical remodeling in atrial fibrillation. Circulation 122: 2378-2387.
86. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
87. Hofacker IL, Priwitzer B, Stadler PF (2004) Prediction of locally stable RNA secondary structures for genome-wide surveys. Bioinformatics 20: 186-190. (Pubitemid 38195676)
88. Risso D, Massa MS, Chiogna M, Romualdi C (2009) A modified LOESS normalization applied to microRNA arrays: a comparative evaluation. Bioinformatics 25: 2685-2691.
89. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17: 10-12.
90. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
91. Biscontin A, Casara S, Cagnin S, Tombolan L, Rosolen A, et al. (2010) New miRNA labeling method for bead-based quantification. BMC Mol Biol 11: 44.
92. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20. (Pubitemid 40094598)
93. Sales G, Coppe A, Bisognin A, Biasiolo M, Bortoluzzi S, et al. (2010) MAGIA, a web-based tool for miRNA and Genes Integrated Analysis. Nucleic Acids Res 38: W352-359.
94. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504. (Pubitemid 37428274)