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Marine Biotechnology

, Volume 18, Issue 4, pp 485–499 | Cite as

Long Non-Coding RNAs (lncRNAs) of Sea Cucumber: Large-Scale Prediction, Expression Profiling, Non-Coding Network Construction, and lncRNA-microRNA-Gene Interaction Analysis of lncRNAs in Apostichopus japonicus and Holothuria glaberrima During LPS Challenge and Radial Organ Complex Regeneration

  • Chuang Mu
  • Ruijia WangEmail author
  • Tianqi Li
  • Yuqiang Li
  • Meilin Tian
  • Wenqian Jiao
  • Xiaoting Huang
  • Lingling Zhang
  • Xiaoli Hu
  • Shi Wang
  • Zhenmin BaoEmail author
Original Article

Abstract

Long non-coding RNA (lncRNA) structurally resembles mRNA but cannot be translated into protein. Although the systematic identification and characterization of lncRNAs have been increasingly reported in model species, information concerning non-model species is still lacking. Here, we report the first systematic identification and characterization of lncRNAs in two sea cucumber species: (1) Apostichopus japonicus during lipopolysaccharide (LPS) challenge and in heathy tissues and (2) Holothuria glaberrima during radial organ complex regeneration, using RNA-seq datasets and bioinformatics analysis. We identified A. japonicus and H. glaberrima lncRNAs that were differentially expressed during LPS challenge and radial organ complex regeneration, respectively. Notably, the predicted lncRNA-microRNA-gene trinities revealed that, in addition to targeting protein-coding transcripts, miRNAs might also target lncRNAs, thereby participating in a potential novel layer of regulatory interactions among non-coding RNA classes in echinoderms. Furthermore, the constructed coding-non-coding network implied the potential involvement of lncRNA-gene interactions during the regulation of several important genes (e.g., Toll-like receptor 1 [TLR1] and transglutaminase-1 [TGM1]) in response to LPS challenge and radial organ complex regeneration in sea cucumbers. Overall, this pioneer systematic identification, annotation, and characterization of lncRNAs in echinoderm pave the way for similar studies and future genetic, genomic, and evolutionary research in non-model species.

Keywords

Long non-coding RNA (lncRNA) RNA-seq Sea cucumber Innate immune response Tissue regeneration 

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31502165) and Shandong Provincial Natural Science Foundation, China (ZR2015CQ001). The authors wish to thank Dr. Yan Sun, and Xue Li, Jing Wang, Xiaogang Xun and Liheng Zhang for their assistance in bioinformatics analysis.

Compliance with ethical standards

Conflict of Interests

No conflicts of interest are declared.

Supplementary material

10126_2016_9711_Fig6_ESM.jpg (82 kb)
Supplementary Fig. 1

Details of the correlation coefficients in the correlation matrices of A. japonicus and H. glaberrima. Details of correlation coefficients and p values in the correlation matrices of A. japonicus and H. glaberrima. (a) Distribution of correlation coefficients in the correlation matrix of A. japonicas; (b) correlation coefficients and p values in the correlation matrix of A. japonicas; (c) distribution of correlation coefficients in the correlation matrix of H. glaberrima; (d) correlation coefficients and p values in the correlation matrix of H. glaberrima. The plots were generated using correlation coefficients, p values, and the frequency (counts) of lncRNA/gene pairs in each interval. Blue dots correspond to highly significantly correlated lncRNAs/genes pairs (|correlation coefficient| >0.95 and a two-tailed p value <0.05); green dots correspond to significantly correlated lncRNAs/genes pairs (|correlation coefficient| >0.75 and a two-tailed p value <0.05); red dots correspond to other lncRNAs/genes pairs (|correlation coefficient| <0.75 or p value >0.05) (JPG 82 kb)

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High resolution image (TIF 1319 kb)
10126_2016_9711_Fig7_ESM.jpg (68 kb)
Supplementary Fig. 2

The molecular function and cellular component enrichment networks of A. japonicus and H. glaberrima. The coding-non-coding enrichment network corresponding to the ontologies of molecular function and cellular component for A.japonicus and H. glaberrima. (a) The cellular component network of A.japonicus; (b) the molecular function network of A.japonicus; (c) the cellular component network of H. glaberrima; (d) the molecular function network of H. glaberrima (JPG 67 kb)

10126_2016_9711_MOESM2_ESM.tif (6.6 mb)
High resolution image (TIF 6711 kb)
10126_2016_9711_Fig8_ESM.jpg (66 kb)
Supplementary Fig. 3

Clusters of biological process networks in A. japonicus and H. glaberrima. Clusters of biological process networks for the two species, including the three clusters in biological process network of A. japonicus (a, b, and c) and the three clusters in biological process network of H. glaberrima (d, e, and f) (JPG 65 kb)

10126_2016_9711_MOESM3_ESM.tif (5.9 mb)
High resolution image (TIF 6029 kb)
10126_2016_9711_Fig9_ESM.jpg (104 kb)
Supplementary Fig. 4

A summary of the GO enrichment analysis of the microRNA-targeted genes in A. japonicus and H. glaberrima. The GO enrichment analysis of the microRNA-targeted genes in (a) A. japonicus and (b) H. glaberrima. The x-axis corresponds to the GO terms of the three ontological categories, and the y-axis corresponds to the percentage of gene sequences (JPG 104 kb)

10126_2016_9711_MOESM4_ESM.tif (2.9 mb)
High resolution image (TIF 2931 kb)
10126_2016_9711_MOESM5_ESM.xlsx (814 kb)
Supplementary Table 1 List of lncRNAs in A. japonicus and H. glaberrima (XLSX 814 kb)
10126_2016_9711_MOESM6_ESM.xlsx (10 kb)
Supplementary Table 2 Summary of lncRNA hits in other species (XLSX 10 kb)
10126_2016_9711_MOESM7_ESM.xlsx (14 kb)
Supplementary Table 3 Summary of reciprocal blast results for lncRNAs in A. japonicus and H. glaberrima (XLSX 13 kb)
10126_2016_9711_MOESM8_ESM.xlsx (214 kb)
Supplementary Table 4 Differentially expressed genes and lncRNAs in A. japonicus and H. glaberrima (XLSX 214 kb)
10126_2016_9711_MOESM9_ESM.xlsx (33 kb)
Supplementary Table 5 Details of significantly enriched GO terms in the coding-non-coding enrichment networks of A. japonicus and H. glaberrima (XLSX 33 kb)
10126_2016_9711_MOESM10_ESM.xlsx (238 kb)
Supplementary Table 6 The lncRNA-microRNA-gene trinities in A. japonicus and H. glaberrima (XLSX 238 kb)
10126_2016_9711_MOESM11_ESM.docx (845 kb)
ESM 1 (DOCX 844 kb)
10126_2016_9711_MOESM12_ESM.docx (864 kb)
ESM 2 (DOCX 864 kb)
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ESM 3 (DOCX 58 kb)

References

  1. Agard M, Asakrah S, Morici LA (2013) PGE2 suppression of innate immunity during mucosal bacterial infection. Front Cell Infect Microbiol 3(45):1–11Google Scholar
  2. Anholt RR (2014) Olfactomedin proteins: central players in development and disease. Front Cell Dev Biol 26:6Google Scholar
  3. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233PubMedPubMedCentralCrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57(1):289–300Google Scholar
  5. Blunt JW, Copp BR, Munro MH, Northcote PT, Prinsep MR (2011) Review: marine natural products. Nat Prod Rep 18(1):1R–49RGoogle Scholar
  6. Borsani G, Tonlorenzi R, Simmler MC, Dandolo L, Arnaud D, Capra V, Grompe M, Pizzuti A, Muzny D, Lawrence C, Willard HF, Avner P, Ballabio A (1991) Characterization of a murine gene expressed from the inactive X chromosome. Nature 351:325–329PubMedCrossRefGoogle Scholar
  7. Bu D, Yu K, Sun S, Xie C, Skogerbø G, Miao R, Xiao H, Liao Q, Luo H, Zhao G, Zhao H, Liu Z, Liu C, Chen R, Zhao Y (2012) NONCODE v3.0: integrative annotation of long noncoding RNAs. Nucleic Acids Res 40:D210-D215Google Scholar
  8. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927PubMedPubMedCentralCrossRefGoogle Scholar
  9. Carnevali MDC, Burighel P (2010) Regeneration in echinoderms and ascidians. eLS. doi: 10.1002/9780470015902.a0022102
  10. Carpenter S, Atianand M, Aiello D, Ricci E, Gandhi P, Hal LL, Byron M, Monks B, Henry-Bezy M, O’Neill LA, Lawrence JB, Moore MJ, Caffrey DR, Fitzgerald KA (2013) A long noncoding RNA mediates both activation and repression of immune response genes. Science 341:789–792PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147:358–369PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chen M, Zhang X, Liu J, Storey KB (2013) High-throughput sequencing reveals differential expression of miRNAs in intestine from sea cucumber during aestivation. PLoS One 8:e76120PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cho WJ, Shin JM, Kim JS, Lee MR, Hong KS, Lee JH, Koo KH, Park JW, Kim KS (2009) miR-372 regulates cell cycle and apoptosis of ags human gastric cancer cell line through direct regulation of LATS2. Mol Cell 28:521–527CrossRefGoogle Scholar
  14. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell 44:667–678PubMedPubMedCentralCrossRefGoogle Scholar
  15. Clarkson E (2009) Invertebrate palaeontology and evolution. Wiley-Blackwell, HobokenGoogle Scholar
  16. Collins LJ (2011) The RNA infrastructure: an introduction to ncRNA networks. In: RNA Infrastructure and Networks. Springer, New York, p 1–19Google Scholar
  17. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676PubMedCrossRefGoogle Scholar
  18. Dorn GW, Matkovich SJ (2014) Ménage à trois: intimate relationship among a microRNA, long noncoding RNA, and mRNA. Circ Res 114:1362–1365PubMedPubMedCentralCrossRefGoogle Scholar
  19. Eitan S, Schwartz M (1993) A transglutaminase that converts interleukin-2 into a factor cytotoxic to oligodendrocytes. Science 261:106–108PubMedCrossRefGoogle Scholar
  20. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2004) MicroRNA targets in Drosophila. Genome Biol 5:R1CrossRefGoogle Scholar
  21. Fan H (2001) Sea cucumber: research and development on the health care functioning of sea cucumber and its ingredients. Chinese Mar Med 4:37–42Google Scholar
  22. FAO (2012) Year Book. Fishery and aquaculture statistics. ftp://ftp.fao.org/FI/STAT/summary/b-1.pdf. Accessed 19 July 2015
  23. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37PubMedPubMedCentralCrossRefGoogle Scholar
  24. Fishery Administration, Ministry of Agriculture of the People’s Republic of China (2014) China Fishery Statistical Yearbook in 2014[M]. China Agriculture Press, Beijing (in Chinese)Google Scholar
  25. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037PubMedCrossRefGoogle Scholar
  26. García-Arrarás JE, Greenberg MJ (2001) Visceral regeneration in holothurians. Microsc Res Tech 55:438–451PubMedCrossRefGoogle Scholar
  27. Gong G, Sha Z, Chen S, Li C, Yan H, Chen Y, Wang T (2015) Expression profiling analysis of the microRNA response of Cynoglossus semilaevis to Vibrio anguillarum and other stimuli. Mar Biotechnol 17:338–352PubMedCrossRefGoogle Scholar
  28. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652PubMedPubMedCentralCrossRefGoogle Scholar
  29. Grillo G, Turi A, Licciulli F, Mignone F, Liuni S, Banfi S, Gennarino VA, Horner DS, Pavesi G, Picardi E, Pesole G (2010) UTRdb and UTRsite (RELEASE 2010): a collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res 38:D75–D80PubMedCrossRefGoogle Scholar
  30. Guo H, Ye C-X, Wang A-L, Xian J-A, Liao S-A, Miao Y-T, Zhang S-P (2013) Trascriptome analysis of the Pacific white shrimp Litopenaeus vannamei exposed to nitrite by RNA-seq. Fish Shellfish Immunol 35:2008–2016PubMedCrossRefGoogle Scholar
  31. Guttman M, Rinn JL (2012) Modular regulatory principles of large non-coding RNAs. Nature 482:339–346PubMedPubMedCentralCrossRefGoogle Scholar
  32. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28:503–510PubMedPubMedCentralCrossRefGoogle Scholar
  33. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300PubMedPubMedCentralCrossRefGoogle Scholar
  34. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512PubMedCrossRefGoogle Scholar
  35. Huang W, Long N, Khatib H (2012) Genome-wide identification and initial characterization of bovine long non-coding RNAs from EST data. Anim Genet 43:674–682PubMedCrossRefGoogle Scholar
  36. Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P, Wang Y, Kong B, Langerød A, Børresen-Dale AL, Kim SK, Van de Vijver M, Sukumar S, Whitfield ML, Kellis M, Xiong Y, Wong DJ, Chang HY (2011) Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet 43:621–629PubMedPubMedCentralCrossRefGoogle Scholar
  37. Iyengar BR, Choudhary A, Sarangdhar MA, Venkatesh K, Gadgil CJ, Pillai B (2014) Non-coding RNA interact to regulate neuronal development and function. Front Cell Neurosci 8:47PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jalali S, Bhartiya D, Lalwani MK, Sivasubbu S, Scaria V (2013) Systematic transcriptome wide analysis of lncRNA-miRNA interactions. PLoS One 8:e53823PubMedPubMedCentralCrossRefGoogle Scholar
  39. Jiao Y, Zheng Z, Du X, Wang Q, Huang R, Deng Y, Shi S, Zhao X (2014) Identification and characterization of microRNAs in pearl oyster Pinctada martensii by Solexa deep sequencing. Mar Biotechnol 16:54–62PubMedCrossRefGoogle Scholar
  40. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS (2004) Human microRNA targets. PLoS Biol 2:e363PubMedPubMedCentralCrossRefGoogle Scholar
  41. Johnsson P, Lipovich L, Grandér D, Morris KV (2014) Evolutionary conservation of long non-coding RNAs; sequence, structure, function. Biochim Biophys Acta Gen Subj 1840:1063–1071CrossRefGoogle Scholar
  42. Kaur S, Spillane C (2015) Reduction in carotenoid levels in the marine diatom Phaeodactylum tricornutum by artificial microRNAs targeted against the endogenous phytoene synthase gene. Mar Biotechnol 17:1–7PubMedCrossRefGoogle Scholar
  43. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39:D152–D157PubMedCrossRefGoogle Scholar
  44. Kretz M et al (2012) Suppression of progenitor differentiation requires the long noncoding RNA ANCR. Genes Dev 26:338–343PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kung JT, Colognori D, Lee JT (2013) Long noncoding RNAs: past, present, and future. Genetics 193:651–669PubMedPubMedCentralCrossRefGoogle Scholar
  46. Lee JT (2011) Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat Rev Mol Cell Biol 12:815–826PubMedCrossRefGoogle Scholar
  47. Lee C, Kikyo N (2012) Strategies to identify long noncoding RNAs involved in gene regulation. Cell Biosci 2:1–6CrossRefGoogle Scholar
  48. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:1Google Scholar
  49. Li T, Wang S, Wu R, Zhou X, Zhu D, Zhang Y (2012) Identification of long non-protein coding RNAs in chicken skeletal muscle using next generation sequencing. Genomics 99:292–298PubMedCrossRefGoogle Scholar
  50. Li J-H, Liu S, Zhou H, Qu L-H, Yang J-H (2013) starBase v2. 0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res 42:D92-97Google Scholar
  51. Liao Q, Liu C, Yuan X, Kang S, Miao R, Xiao H, Zhao G, Luo H, Bu D, Zhao H, Skogerbø G, Wu Z, Zhao Y (2011) Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res 39:3864–3878PubMedPubMedCentralCrossRefGoogle Scholar
  52. Luo F, Yang Y, Zhong J, Gao H, Khan L, Thompson DK, Zhou J (2007) Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory. BMC Bioinformatics 8:299PubMedPubMedCentralCrossRefGoogle Scholar
  53. Ma N, Zhou L, Zhang Y, Jiang Y, Gao X (2014) Intragenic microRNA and long non-coding RNA: novel potential regulator of IGF2-H19 imprinting region. Evol Dev 16:1–2PubMedCrossRefGoogle Scholar
  54. Martens JA, Laprade L, Winston F (2004) Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 429:571–574PubMedCrossRefGoogle Scholar
  55. Mashanov VS, García-Arrarás JE (2011) Gut regeneration in holothurians: a snapshot of recent developments. Biol Bull 221:93–109PubMedGoogle Scholar
  56. Mashanov VS, Zueva OR, García-Arrarás JE (2014) Transcriptomic changes during regeneration of the central nervous system in an echinoderm. BMC Genomics 15:357PubMedPubMedCentralCrossRefGoogle Scholar
  57. Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15:R17–R29PubMedCrossRefGoogle Scholar
  58. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159PubMedCrossRefGoogle Scholar
  59. Nagase H, Kitazato K, Sasaki E, Hattori M, Kitazato K, Saito H (1997) Antithrombin III-independent effect of depolymerized holothurian glycosaminoglycan (DHG) on acute thromboembolism in mice. Thromb Haemost 77:399–402PubMedGoogle Scholar
  60. Nam J-W, Bartel DP (2012) Long noncoding RNAs in C. elegans. Genome Res 22:2529–2540PubMedPubMedCentralCrossRefGoogle Scholar
  61. Nguyen T et al (2001) Discovery of a novel member of the histamine receptor family. Mol Pharmacol 59:427–433PubMedGoogle Scholar
  62. Pan B, Ren Y, Gao J, Gao H (2015) De novo RNA-Seq analysis of the Venus clam, Cyclina sinensis, and the identification of immune-related genes. PLoS One 10:e0123296PubMedPubMedCentralCrossRefGoogle Scholar
  63. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22:577–591PubMedPubMedCentralCrossRefGoogle Scholar
  64. Petruk S, Sedkov Y, Riley KM, Hodgson J, Schweisguth F, Hirose S, Jaynes JB, Brock HW, Mazo A (2006) Transcription of bxd Noncoding RNAs Promoted by Trithorax Represses Ubx in cis by Transcriptional Interference. Cell 127:1209–1221PubMedPubMedCentralCrossRefGoogle Scholar
  65. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465:1033–1038PubMedPubMedCentralCrossRefGoogle Scholar
  66. Pontier DB, Gribnau J (2011) Xist regulation and function explored. Hum Genet 130:223–236PubMedPubMedCentralCrossRefGoogle Scholar
  67. Quiñones JL, Rosa R, Ruiz DL, Garcı́ JE (2002) Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol 250:181–197PubMedCrossRefGoogle Scholar
  68. Rao R, Zhu YB, Alinejad T, Tiruvayipati S, Thong KL, Wang J, Bhassu S (2015) RNA-seq analysis of Macrobrachium rosenbergii hepatopancreas in response to Vibrio parahaemolyticus infection. Gut Pathog 7:1CrossRefGoogle Scholar
  69. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277PubMedCrossRefGoogle Scholar
  70. Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81Google Scholar
  71. Rivas E, Klein RJ, Jones TA, Eddy SR (2001) Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 11:1369–1373PubMedCrossRefGoogle Scholar
  72. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25PubMedPubMedCentralCrossRefGoogle Scholar
  73. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140PubMedCrossRefGoogle Scholar
  74. Salem M, Xiao C, Womack J, Rexroad CE III, Yao J (2010) A microRNA repertoire for functional genome research in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 12:410–429PubMedCrossRefGoogle Scholar
  75. Schwab ME, Caroni P (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J Neurosci 8:2381–2393PubMedGoogle Scholar
  76. Sharan R, Ulitsky I, Shamir R (2007) Network-based prediction of protein function. Mol Syst Biol 3:88PubMedPubMedCentralCrossRefGoogle Scholar
  77. Signor III PW, Brett CE (1984) The mid-Paleozoic precursor to the Mesozoic marine revolution. Paleobiology 229–245Google Scholar
  78. Škugor A, Slanchev K, Torgersen JS, Tveiten H, Andersen Ø (2014) Conserved mechanisms for germ cell-specific localization of nanos3 transcripts in teleost species with aquaculture significance. Mar Biotechnol 16:256–264PubMedCrossRefGoogle Scholar
  79. Sloan N (1985) Echinoderm fisheries of the world: a review. AA Balkema, Rotterdam, pp 109–124Google Scholar
  80. Sprinkle J (1992) Radiation of echinodermata. In: Lipps JH et al (eds) Origin and early evolution of the Metazoa. Plenum Press, New York, p 375–398Google Scholar
  81. Steinfeld I, Navon R, Creech ML, Yakhini Z, Tsalenko A (2015) ENViz: a Cytoscape App for integrated statistical analysis and visualization of sample-matched data with multiple data types. Bioinformatics 31:1683–1685Google Scholar
  82. Sugitani K, Matsukawa T, Koriyama Y, Shintani T, Nakamura T, Noda M, Kato S (2006) Upregulation of retinal transglutaminase during the axonal elongation stage of goldfish optic nerve regeneration. Neuroscience 142:1081–1092PubMedCrossRefGoogle Scholar
  83. Takeda K, Akira S (2004) TLR signaling pathways. Semin Immunol 16(1):3–9PubMedCrossRefGoogle Scholar
  84. Tetzlaff W, Gilad VH, Leonard C, Bisby MA, Gilad GM (1988) Retrograde changes in transglutaminase activity after peripheral nerve injuries. Brain Res 445:142–146PubMedCrossRefGoogle Scholar
  85. Tossas K, Qi-Huang S, Cuyar E, García-Arrarás JE (2014) Temporal and spatial analysis of enteric nervous system regeneration in the sea cucumber Holothuria glaberrima. Regeneration 1:10–26PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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 28:511–515PubMedPubMedCentralCrossRefGoogle Scholar
  87. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329:689–693PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147:1537–1550PubMedPubMedCentralCrossRefGoogle Scholar
  89. Wang J, Liu X, Wu H, Ni P, Gu Z, Qiao Y, Chen N, Sun F, Fan Q (2010) CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res 38:5366–5383PubMedPubMedCentralCrossRefGoogle Scholar
  90. Wang L, Park HJ, Dasari S, Wang S, Kocher J-P, Li W (2013) CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model. Nucleic Acids Res 41:e74PubMedPubMedCentralCrossRefGoogle Scholar
  91. Wang H, Liu S, Cui J, Li C, Qiu X, Chang Y, Liu Z, Wang X (2014a) Characterization and expression analysis of microRNAs in the tube foot of sea cucumber Apostichopus japonicus. PLoS One 9:e111820PubMedPubMedCentralCrossRefGoogle Scholar
  92. Wang Y, Li Y, Wang Q, Lv Y, Wang S, Chen X, Yu X, Jiang W, Li X (2014b) Computational identification of human long intergenic non-coding RNAs using a GA-SVM algorithm. Gene 533:94–99PubMedCrossRefGoogle Scholar
  93. Wang J, Fu L, Koganti PP, Wang L, Hand JM, Ma H, Yao J (2016) Identification and Functional Prediction of Large Intergenic Noncoding RNAs (lincRNAs) in Rainbow Trout (Oncorhynchus mykiss). Mar Biotechnol 18:271–282PubMedCrossRefGoogle Scholar
  94. Wapinski O, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21:354–361PubMedCrossRefGoogle Scholar
  95. Wilusz JE, Sharp PA (2013) A Circuitous Route to Noncoding RNA. Science 340:440–441PubMedPubMedCentralCrossRefGoogle Scholar
  96. Wren JD (2009) A global meta-analysis of microarray expression data to predict unknown gene functions and estimate the literature-data divide. Bioinformatics 25:1694–1701PubMedPubMedCentralCrossRefGoogle Scholar
  97. Xie X, Lu J, Kulbokas EJ, Golub TR, Mootha V, Lindblad-Toh K, Lander ES, Kellis M (2005) Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals. Nature 434:338–345PubMedPubMedCentralCrossRefGoogle Scholar
  98. Xu J, Li CX, Li YS, Lv JY, Ma Y, Shao TT, Xu LD, Wang YY, Du L, Zhang YP, Jiang W, Li CQ, Xiao Y, Li X (2011) MiRNA-miRNA synergistic network: construction via co-regulating functional modules and disease miRNA topological features. Nucleic Acids Res 39:825–836PubMedCrossRefGoogle Scholar
  99. Yabuta N, Fujii T, Copeland NG, Gilbert DJ, Jenkins NA, Nishiguchi H, Endo Y, Toji S, Tanaka H, Nishimune Y, Nojima H (2000) Structure, expression, and chromosome mapping of LATS2, a mammalian homologue of the Drosophila tumor suppressor gene lats/warts. Genomics 63:263–270PubMedCrossRefGoogle Scholar
  100. Yan H, Chen Y, Zhou S, Li C, Gong G, Chen X, Wang T, Chen S, Sha Z (2016) Expression Profile Analysis of miR-221 and miR-222 in Different Tissues and Head Kidney Cells of Cynoglossus semilaevis, Following Pathogen Infection. Mar Biotechnol 18:37–48PubMedCrossRefGoogle Scholar
  101. Yang Z, Zhu Q, Luo K, Zhou Q (2001) The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414:317–322PubMedCrossRefGoogle Scholar
  102. Yoon S, De Micheli G (2005) Prediction of regulatory modules comprising microRNAs and target genes. Bioinformatics 21:ii93–ii100PubMedCrossRefGoogle Scholar
  103. Yoon J-H, Abdelmohsen K, Gorospe M (2014) Functional interactions among microRNAs and long noncoding RNAs. Semin Cell Dev Biol 34:9–14PubMedCrossRefGoogle Scholar
  104. Zhang P, Li C, Zhu L, Su X, Li Y, Jin C, Li T (2013) De novo assembly of the sea cucumber Apostichopus japonicus hemocytes transcriptome to identify miRNA targets associated with skin ulceration syndrome. PLoS One 8:e73506PubMedPubMedCentralCrossRefGoogle Scholar
  105. Zhou Z, Dong Y, Sun H, Yang A, Chen Z, Gao S, Jiang J, Guan X, Jiang B, Wang B (2014) Transcriptome sequencing of sea cucumber (Apostichopus japonicus) and the identification of gene-associated markers. Mol Ecol Resour 14:127–138PubMedCrossRefGoogle Scholar
  106. Zhu X, Chen D, Hu Y, Wu P, Wang K, Zhang J, Chu W, Zhang J (2015) The microRNA signature in response to nutrient restriction and refeeding in skeletal muscle of Chinese Perch (Siniperca chuatsi). Mar Biotechnol 17:180–189PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Chuang Mu
    • 1
  • Ruijia Wang
    • 1
    Email author
  • Tianqi Li
    • 1
  • Yuqiang Li
    • 1
  • Meilin Tian
    • 1
  • Wenqian Jiao
    • 1
  • Xiaoting Huang
    • 1
  • Lingling Zhang
    • 1
  • Xiaoli Hu
    • 1
  • Shi Wang
    • 1
  • Zhenmin Bao
    • 1
    Email author
  1. 1.Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life SciencesOcean University of ChinaQingdaoChina

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