High-Throughput Sequencing Reveals Circulating miRNAs as Potential Biomarkers for Measuring Puberty Onset in Chicken (Gallus gallus)

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Han, Wei ^a   Zhu, Yunfen ^a   Su, Yijun ^a   Li, Guohui ^a   Qu, Liang ^a   Zhang, Huiyong ^a   Wang, Kehua ^a   Zou, Jianmin ^a   Liu, Honglin ^b  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; MICRORNA;

ANIMAL; BLOOD; CHICKEN; DOWN REGULATION; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; PROCEDURES; PUBERTY; SEXUAL MATURATION; UPREGULATION;

ANIMALS; BIOMARKERS; CHICKENS; DOWN-REGULATION; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; PUBERTY; SEXUAL MATURATION; UP-REGULATION;

EID: 84988363408     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0154958     Document Type: Article

References (47)

1. Lakshman R FN, Luben R, Bingham S, Khaw K, Wareham N, Ong KK. (2008) Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia 51: 781–786. doi: 10.1007/s00125-008-0948-5 PMID: 18320165
2. Lomniczi A, Wright H, Castellano JM, Sonmez K, Ojeda SR (2013) A system biology approach to identify regulatory pathways underlying the neuroendocrine control of female puberty in rats and nonhuman primates. Horm Behav 64: 175–186. doi: 10.1016/j.yhbeh.2012.09.013 PMID: 23998662
3. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JSJ, et al. (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349: 1614–1627. PMID: 14573733
4. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, et al. (2009) TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet 41: 354–358. doi: 10.1038/ng.306 PMID: 19079066
5. Ong KK, Elks CE, Li S, Zhao JH, Luan J, et al. (2009) Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet 41: 729–733. doi: 10.1038/ng.382 PMID: 19448623
6. Gajdos ZK, Butler JL, Henderson KD, He C, Supelak PJ, et al. (2008) Association studies of common variants in 10 hypogonadotropic hypogonadism genes with age at menarche. J Clin Endocrinol Metab 93: 4290–4298. doi: 10.1210/jc.2008-0981 PMID: 18728166
7. Elks CE PJ, Sulem P, Chasman DI, Franceschini N, He C (2010) Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet 42: 1077–1085. doi: 10. 1038/ng.714 PMID: 21102462
8. Lorah DD, Frank MB (2011) Puberty and its measurement: a decade in review. Journal of research on adolescence 21: 180–195.
9. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, et al. (2003) The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24: 668–693. PMID: 14570750
10. Yingling VR, Khaneja A (2006) Short-term delay of puberty causes a transient reduction in bone strength in growing female rats. Bone 38: 67–73. PMID: 16112636
11. Dorn LD, Dahl RE, Woodward HR, Biro F (2006) Defining the Boundaries of Early Adolescence: A User's Guide to Assessing Pubertal Status and Pubertal Timing in Research With Adolescents. Applied Developmental Science 10: 30–56.
12. Shirtcliff EA, Dahl RE, Pollak SD (2009) Pubertal development: Correspondence between hormonal and physical development. Child Development 80: 327–337. doi: 10.1111/j.1467-8624.2009.01263.x PMID: 19466995
13. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215–233. doi: 10. 1016/j.cell.2009.01.002 PMID: 19167326
14. Squadrito ML, Baer C, Burdet F, Maderna C, Gilfillan GD, et al. (2014) Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep 8: 1432–1446. doi: 10.1016/j. celrep.2014.07.035 PMID: 25159140
15. Villarroya-Beltri C G- VC, Sánchez-Cabo F, Pérez-Hernández D, Vázquez J, Martin-Cofreces N, Martinez-Herrera DJ, et al. (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4.
16. Qin H, Chen GX, Liang MY, Rong J, Yao JP, et al. (2013) The altered expression profile of microRNAs in cardiopulmonary bypass canine models and the effects of mir-499 on myocardial ischemic reperfusion injury. J Transl Med 11: 154. doi: 10.1186/1479-5876-11-154 PMID: 23800236
17. Botta-Orfila T, Morato X, Compta Y, Lozano JJ, Falgas N, et al. (2014) Identification of blood serum micro-RNAs associated with idiopathic and LRRK2 Parkinson's disease. J Neurosci Res 92: 1071–1077. doi: 10.1002/jnr.23377 PMID: 24648008
18. Akat K M MMD, Morozov P (2014) Comparative RNA-sequencing analysis of myocardial and circulating small RNAs in human heart failure and their utility as biomarkers. PNAS 111(30): 11151–11156. doi: 10.1073/pnas.1401724111 PMID: 25012294
19. Yang C, Wang C, Chen X, Chen SD, Zhang YN, Zhi F, et al. (2013) Identification of seven serum microRNAs from a genome-wide serum microRNA expression profile as potential noninvasive biomarkers for malignant astrocytomas. Int J Cancer 132(1): 116–127. doi: 10.1002/ijc.27657 PMID: 22674182
20. Liu H, Zhu L, Liu B, Yang L, Meng X, et al. (2012) Genome-wide microRNA profiles identify miR-378 as a serum biomarker for early detection of gastric cancer. Cancer Lett 316(2): 196–203. doi: 10.1016/j. canlet.2011.10.034 PMID: 22169097
21. Chen X, Gao C, Li H, Huang L, Sun Q, et al. (2010) Identification and characterization of microRNAs in raw milk during different periods of lactation, commercial fluid, and powdered milk products. Cell Res 20: 1128–1137. doi: 10.1038/cr.2010.80 PMID: 20548333
22. Zheng Y, Chen KL, Zheng XM, Li HX, Wang GL (2014) Identification and bioinformatics analysis of microRNAs associated with stress and immune response in serum of heat-stressed and normal Holstein cows. Cell Stress Chaperones 19: 973–981. doi: 10.1007/s12192-014-0521-8 PMID: 24917036
23. Paczoska-Eliasiewicz HE, Proszkowiec-Weglarz M, Proudman J, Jacek T, Mika M, et al. (2006) Exogenous leptin advances puberty in domestic hen. Domest Anim Endocrinol 31: 211–226. PMID: 16303278
24. Han W Z, Wang K, Su Y, Zhu Y, Song C, Li G, et al. (2015) High-throughput sequencing reveals hypothalamic microRNAs as novel partners involved in timing the rapid development of chicken (Gallus gallus) gonads. PLoS One 10(6):e0129738. doi: 10.1371/journal.pone.0129738 PMID: 26061962
25. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, et al. (2009) A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 10(6): 1–10.
26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. PMID: 11846609
27. Carletti MZ, Christenson LK (2009) MicroRNA in the ovary and female reproductive tract. J Anim Sci 87: E29–38. doi: 10.2527/jas.2008-1331 PMID: 18791135
28. 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. doi: 10. 1371/journal.pone.0011744 PMID: 20805883
29. Kang L, Cui X, Zhang Y, Yang C, Jiang Y (2013) Identification of miRNAs associated with sexual maturity in chicken ovary by Illumina small RNA deep sequencing. BMC Genomics 14: 352. doi: 10.1186/ 1471-2164-14-352 PMID: 23705682
30. Wu J, Zhu H, Song W, Li M, Liu C, et al. (2014) Identification of conservative microRNAs in Saanen dairy goat testis through deep sequencing. Reprod Domest Anim 49: 32–40. doi: 10.1111/rda.12217 PMID: 23981187
31. Zhu H, Shah S, Shyh-Chang N, Shinoda G, Einhorn WS, et al. (2010) Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat Genet 42: 626–630. doi: 10.1038/ng.593 PMID: 20512147
32. Wu G, Park MY, Conway SR, Wang JW, Weigel D, et al. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750–759. doi: 10.1016/j.cell.2009. 06.031 PMID: 19703400
33. Sangiao-Alvarellos S, Manfredi-Lozano M, Ruiz-Pino F, Navarro VM, Sanchez-Garrido MA, et al. (2013) Changes in hypothalamic expression of the Lin28/let-7 system and related microRNAs during postnatal maturation and after experimental manipulations of puberty. Endocrinology 154: 942–955. doi: 10.1210/en.2012-2006 PMID: 23291449
34. Boulan L, Martin D, Milan M (2013) bantam miRNA promotes systemic growth by connecting insulin signaling and ecdysone production. Curr Biol 23: 473–478. doi: 10.1016/j.cub.2013.01.072 PMID: 23477723
35. Li J ZY, Li D, Liu Y, Chu D, Jiang X, Hou D, et al. (2015) Small non-coding RNAs transfer through mammalian placenta and directly regulate fetal gene expression. Protein Cell 6(6): 391–396. doi: 10.1007/ s13238-015-0156-2 PMID: 25963995
36. Rom S DH, Zuluaga-Ramirez V, Reichenbach N L, Persidsky Y (2015) miR-98 and let-7g* protect the blood-brain barrier under neuroinflammatory conditions. J Cereb Blood Flow Metab doi: 10.1038/jcbfm. 2015.154
37. Kolesarova A, Sirotkin AV, Mellen M, Roychoudhury S (2015) Possible intracellular regulators of female sexual maturation. Physiol Res 64: 379–386. PMID: 25536325
38. Hernandez Gifford JA (2011) The role of WNT signaling in adult ovarian folliculogenesis. Reproduction 150: R137–148.
39. Roa J, Tena-Sempere M (2012) Energy balance and puberty onset: emerging role of central mTOR signaling. Trends Endocrinol Metab 21: 519–528.
40. Fortes MR, Reverter A, Nagaraj SH, Zhang Y, Jonsson NN, et al. (2011) A single nucleotide polymorphism-derived regulatory gene network underlying puberty in 2 tropical breeds of beef cattle. J Anim Sci 89: 1669–1683. doi: 10.2527/jas.2010-3681 PMID: 21357453
41. Frost RJ, Olson EN (2009) Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc Natl Acad Sci U S A 108: 21075–21080.
42. Zhu H, Shyh-Chang N, Segre AV, Shinoda G, Shah SP, et al. (2011) The Lin28/let-7 axis regulates glucose metabolism. Cell 147: 81–94. doi: 10.1016/j.cell.2011.08.033 PMID: 21962509
43. Lovis P, Gattesco S, Regazzi R (2008) Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs. Biol Chem 389: 305–312. doi: 10.1515/BC.2008. 026 PMID: 18177263
44. Ling YH, Ren CH, Guo XF, Xu LN, Huang YF, et al. (2014) Identification and characterization of microRNAs in the ovaries of multiple and uniparous goats (Capra hircus) during follicular phase. BMC Genomics 15: 339. doi: 10.1186/1471-2164-15-339 PMID: 24886377
45. Becker C, Riedmaier I, Reiter M, Tichopad A, Pfaffl MW, et al. (2011) Changes in the miRNA profile under the influence of anabolic steroids in bovine liver. Analyst 136: 1204–1209. doi: 10.1039/ c0an00703j PMID: 21212882
46. Chen Y, Siegel F, Kipschull S, Haas B, Frohlich H, et al. (2013) miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nat Commun 4: 1769. doi: 10.1038/ncomms2742 PMID: 23612310
47. Pirola CJ, Fernandez Gianotti T, Castano GO, Mallardi P, San Martino J, et al. (2014) Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut 64: 800–812. doi: 10.1136/gutjnl-2014-306996 PMID: 24973316