#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Comparative transcriptome reveals the potential modulation mechanisms of estradiol affecting ovarian development of female Portunus trituberculatus


Autoři: Meimei Liu aff001;  Jie Pan aff001;  Zhiguo Dong aff002;  Yongxu Cheng aff001;  Jie Gong aff005;  Xugan Wu aff001
Působiště autorů: Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China aff001;  Key Laboratory of Marine Biotechnology of Jiangsu Province, Huaihai Institute of Technology, Lianyungang, China aff002;  National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, China aff003;  Centre for Research on Environmental Ecology and Fish Nutrition of Ministry of Agriculture, Shanghai Ocean University, Shanghai, China aff004;  School of Life Sciences, Nantong University, Nantong, China aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226698

Souhrn

Estradiol is an important sex steroid hormone that is involved in the regulation of crustacean ovarian development. However, the molecular regulatory mechanisms of estradiol on ovarian development are largely unknown. This study performed transcriptome sequencing of ovary, hepatopancreas, brain ganglion, eyestalk, and mandibular organ of crabs after estradiol treatment (0.1μg g-1 crab weight). A total of 23, 806 genes were annotated, and 316, 1300, 669, 142, 383 genes were expressed differently in ovary, hepatopancreas, brain ganglion, eyestalk, and mandibular organ respectively. Differentially expressed gene enrichment analysis revealed several crucial pathways including protein digestion and absorption, pancreatic secretion, insect hormone biosynthesis, drug metabolism-cytochrome P450 and signal transduction pathway. Through this study, some key genes in correlation with the ovarian development and nutrition metabolism were significantly affected by estradiol, such as vitelline membrane outer layer 1-like protein, heat shock protein 70, Wnt5, JHE-like carboxylesterase 1, cytochrome P302a1, crustacean hyperglycemic hormone, neuropeptide F2, trypsin, carboxypeptidase B, pancreatic triacylglycerol lipase-like, and lipid storage droplet protein. Moreover, RT-qPCR validation demonstrated that expression of transcripts related to ovarian development (vitelline membrane outer layer 1-like protein and cytochrome P302a1) and nutrition metabolism (trypsin, glucose dehydrogenase and lipid storage droplet protein) were significantly affected by estradiol treatment. This study not only has identified relevant genes and several pathways that are involved in estradiol regulation on ovarian development of P. trituberculatus, but also provided new insight into the understanding of the molecular function mechanisms of estradiol in crustacean.

Klíčová slova:

Crabs – Crustaceans – estradiol – Ganglia – Gene expression – Hormones – Ovaries – Transcriptome analysis


Zdroje

1. Meusy J, Payen G. Female reproduction in malacostracan crustacea. Zoological Science. 1988; 5: 217–265. doi: 10.1111/j.1096-3642.1988.tb01730.x

2. Zmora N, Trant J, Chan S, Chung J. Vitellogenin and its messenger RNA during ovarian development in the female blue crab, Callinectes sapidus: gene expression, synthesis, transport, and cleavage. Biology of Reproduction. 2007; 77(1): 138–146. doi: 10.1095/biolreprod.106.055483 17409377.

3. Nagaraju G. Reproductive regulators in decapod crustaceans: an overview. Journal of Experimental Biology. 2011; 214(1): 3–16. doi: 10.1242/jeb.047183 21147963.

4. Rodriguez E, Medesani D, Greco L, Fingerman M. Effects of some steroids and other compounds on ovarian growth of the red swamp crayfish, Procambarus clarkii, during early vitellogenesis. Journal of Experimental Zoology. 2002; 292(1): 82–87. doi: 10.1002/jez.1144 11754024.

5. Yano I, Hoshino R. Effects of 17 beta-estradiol on the vitellogenin synthesis and oocyte development in the ovary of kuruma prawn (Marsupenaeus japonicus). Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology. 2006; 144(1): 18–23. doi: 10.1016/j.cbpa.2006.01.026 16545975.

6. Shen B, Yang X, Wu X, Cheng Y, Tang B. The effects of exogenous 17β-estradiol on ovary development and on the level of endogenous 17β-estradiol in Eriocheir sinensis. Journal of Shanghai Ocean University. 2010;19: 289–95 (In Chinese with English abstract).

7. Koskela R, Greenwood J, Rothlisberg P. The influence of prostaglandin estradiol and the steroid hormones, 17α-hydroxyprogesterone and 17β-estradiol on moulting and ovarian development in the tiger prawn, Penaeus esculentus Haswell, 1879 (Crustacea: Decapoda). Comparative Biochemistry and Physiology Part A: Physiology. 1992; 101: 295–299. doi: 10.1016/0300-9629(92)90535-X

8. Tsukimura B, Bender J, Linder C. Development of an anti-vitellin ELISA for the assessment of reproduction in the ridgeback shrimp, Sicyonia ingentis. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology. 2000; 127(2): 215–24. doi: 10.1016/s1095-6433(00)00255-5 11064288.

9. Tiu S, Hui J, He J, Tobe S, Chan S. Characterization of vitellogenin in the shrimp Metapenaeus ensis: expression studies and hormonal regulation of MeVg1 transcription in vitro. Molecular Reproduction and Development. 2006; 73(4): 424–36. doi: 10.1002/mrd.20433 16425293.

10. Liu M, Pan J, Liu Z, Cheng Y, Gong J, Wu X. Effect of estradiol on vitellogenesis and oocyte development of female swimming crab, Portunus trituberculatus. Aquaculture. 2018; 486: 240–5. doi: 10.1016/j.aquaculture.2017.12.034

11. Quinitio E, Hara A, Yamauchi K, Nakao S. Changes in the steroid hormone and vitellogenin levels during the gametogenic cycle of the giant tiger shrimp, Penaeus monodon. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology. 1994; 109: 21–6. doi: 10.1016/0742-8413(94)00044-B

12. Martins J, Ribeiro K, Rangel-Figueiredo T, Coimbra J. Reproductive cycle, ovarian development, and vertebrate-type steroids profile in the freshwater prawn Macrobrachium rosenbergii. Journal of Crustacean Biology. 2007; 27(2): 220–8. doi: 10.1651/c-2597.1

13. Huang H, Ye H, Han S, Wang G. Profiles of gonadotropins and steroid hormone-like substances in the hemolymph of mud crab Scylla paramamosain during the reproduction cycle. Marine and Freshwater Behaviour and Physiology. 2009; 42(4): 297–305. doi: 10.1080/10236240903174792

14. Mardis E. The impact of next-generation sequencing technology on genetics. Trends in Genetics. 2008; 24(3): 133–41. doi: 10.1016/j.tig.2007.12.007 18262675.

15. Subramoniam T. Crustacean ecdysteriods in reproduction and embryogenesis. Comparative Biochemistry and Physiology C-Pharmacology Toxicology & Endocrinology. 2000; 125(2): 135–56. doi: 10.1016/s0742-8413(99)00098-5 11790337.

16. Ye H, Ai C, Huang H, Li S. Advances on reproductive physiology of crabs. Journal of Xiamen University (Natural Science). 2006; 45: 170–175 (In Chinese with English abstract). doi: 10.3321/j.issn:0438–0479.2006.z2.024

17. De Kleijn D, Janssen K, Waddy S, Hegeman R, Lai W, Martens G, et al. Expression of the crustacean hyperglycaemic hormones and the gonad-inhibiting hormone during the reproductive cycle of the female American lobster Homarus americanus. Journal of Endocrinology. 1998; 156(2): 291–298. doi: 10.1677/joe.0.1560291 9518875.

18. Gu P, Tobe S, Chow B, Chu K, He J, Chan S. Characterization of an additional molt inhibiting hormone-like neuropeptide from the shrimp Metapenaeus ensis. Peptides. 2002; 23(11): 1875–83. doi: 10.1016/s0196-9781(02)00178-x 12431725.

19. Zmora N, Trant J, Zohar Y, Chung J. Molt-inhibiting hormone stimulates vitellogenesis at advanced ovarian developmental stages in the female blue crab, Callinectes sapidus 1: an ovarian stage dependent involvement. Saline Systems. 2009; 5(1): 7. doi: 10.1186/1746-1448-5-7 19583852

20. Chen Y, Fan H, Hsieh S, Kuo C. Physiological involvement of DA in ovarian development of the freshwater giant prawn, Macrobrachium rosenbergii. Aquaculture. 2003; 228(1–4): 383–395. doi: 10.1016/s0044-8486(03)00324-7

21. Laufer H, Albrecht K. Metabolism of methyl farnesoate in vitro by peripheral tissues of the spider crab, Libinia emarginata (Decapoda). Advances in Invertebrate Reproduction. 1990; 5: 217–222.

22. Gong J, Ye H, Xie Y, Yang Y, Huang H, Li S, et al. Ecdysone receptor in the mud crab Scylla paramamosain: a possible role in promoting ovarian development. Journal of Endocrinology. 2015; 224(3): 273–287. doi: 10.1530/JOE-14-0526 25563354.

23. Hamasaki K, Fukunaga K, Kitada S. Batch fecundity of the swimming crab Portunus trituberculatus (Brachyura: Portunidae). Aquaculture. 2006; 253(1–4): 359–365. doi: 10.1016/j.aquaculture.2005.08.002

24. Kim D, Kim S, Choi J, Kim B, Seo H, Jang I. The effects of manipulating water temperature, photoperiod, and eyestalk ablation on gonad maturation of the swimming crab, Portunus trituberculatus. Crustaceana. 2010; 83(2): 129–141. doi: 10.1163/001121609x12591347509248

25. Liu M, Wu X, Pan J, Cheng Y. Immunolocalization and changes in 17β-estradiol in Portunus trituberculatus during ovarian development. Journal of Fishery Sciences of China. 2017; 24: 239–47 (In Chinese with English abstract). doi: 10.3724/SP.J.1118.2017.16136

26. Lu Y, Liu M, Gong J, Cheng Y, Wu X. Effect of exogenous estrogen on the ovarian development and gene expression in the female swimming crab Portunus trituberculatus (Miers, 1876) (Decapoda: Brachyura: Portunidae). Journal of Crustacean Biology. 2018; 38(3): 367–373. doi: 10.1093/jcbol/ruy013

27. Pan G, Hou W, Wu X, Wu R, Zhang N, Long X, et al. Effects of water temperature and single crab basket culture on ovarian development and tissue proximate composition of female Portunus trituberculatus. Marine Fisheries. 2015; 37: 550–556. doi: 10.3969/j.issn.1004-2490.2015.06.010

28. Coccia E, De Lisa E, Di Cristo C, Di Cosmo A, Paolucci M. Effects of estradiol and progesterone on the reproduction of the freshwater crayfish Cherax albidus. Biological Bulletin. 2010; 218(1): 36–47. doi: 10.1086/BBLv218n1p36 20203252.

29. Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology. 2011; 29(7): 644–652. doi: 10.1038/nbt.1883 21572440.

30. Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J, et al. Gene Ontology: tool for the unification of biology. Nature Genetics. 2000; 25(1): 25–29. doi: 10.1038/75556 10802651.

31. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Research. 2004; 32: D277–D80. doi: 10.1093/nar/gkh063 14681412.

32. Powell S, Forslund K, Szklarczyk D, Trachana K, Roth A, Huerta-Cepas J, et al. eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Research. 2014; 42(D1): 231–239. doi: 10.1093/nar/gkt1253 24297252.

33. Li B, Dewey C. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12: 16. doi: 10.1186/1471-2105-12-16 21816040.

34. Yang F, Xu H, Dai Z, Yang W. Molecular characterization and expression analysis of vitellogenin in the marine crab Portunus trituberculatus. Comparative Biochemistry and Physiology Part B: Biochemistry & Molecular Biology. 2005; 142(4): 456–464. doi: 10.1016/j.cbpb.2005.09.011 16257250.

35. Livak K, Schmittgen T. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods. 2001; 25(4): 402–408. doi: 10.1006/meth.2001.1262 11846609.

36. Fingerman M. Crustacean endocrinology: A retrospective, prospective, and introspective analysis. Physiological Zoology. 1997; 70(3): 257–269. doi: 10.1086/639593 9231399.

37. Chang E, Chang S, Mulder E. Hormones in the lives of crustaceans: An overview. American Zoologist. 2001; 41(5):1090–1097. doi: 10.1668/0003-1569(2001)041[1090:Hitloc]2.0.Co;2 WOS:000174175500005.

38. Subramoniam T. Chapter 9—Endocrine Regulation of Vitellogenesis. In: Subramoniam T, editor. Sexual Biology and Reproduction in Crustaceans: Academic Press; 2017. p. 231–67.

39. Wang Z, Sun L, Guan W, Zhou C, Tang B, Cheng Y, et al. De novo transcriptome sequencing and analysis of male and female swimming crab (Portunus trituberculatus) reproductive systems during mating embrace (stage II). Bmc Genetics. 2018; 19(1): 3. doi: 10.1186/s12863-017-0592-5 29298661.

40. Vogt G, Stöcker W, Storch V, Zwilling R. Biosynthesis of astacus, protease, a digestive enzyme from crayfish. Histochemistry. 1989; 91(5): 373–381. doi: 10.1007/bf00493824 2656593

41. Vogt G. Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda). Zoomorphology. 1994; 114: 83–101. doi: 10.1007/BF00396642

42. Cheng Y, Du N, Lai W. The lipid accumulation during the stages of the ovarian fast maturation and their effect on the spawning of Eriocheir sinensis. Journal of Fisheries of China. 2000; 24: 113–119 (In Chinese with English abstract). doi: 10.3321/j.issn:1000–0615.2000.02.004

43. Summavielle T, Monteiro P, Reis-Henriques M, Coimbra J. In vitro metabolism of steroid hormones by ovary and hepatopancreas of the crustacean Penaeid shrimp Marsupenaeus japonicus. Scientia Marina. 2003; 67(3): 299–306. doi: 10.3989/scimar.2003.67n3299

44. Suwansa-ard S, Thongbuakaew T, Wang T, Zhao M, Elizur A, Hanna P, et al. In silico neuropeptidome of female Macrobrachium rosenbergii based on transcriptome and peptide mining of eyestalk, central nervous system and ovary. Plos One. 2015; 10(5): e0123848. doi: 10.1371/journal.pone.0123848 26023789.

45. Sumpter J, Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental Health Perspectives. 1995; 103: 173–178. doi: 10.2307/3432529 8593867.

46. Marin M, Matozzo V. Vitellogenin induction as a biomarker of exposure to estrogenic compounds in aquatic environments. Marine Pollution Bulletin. 2004; 48(9–10): 835–839. doi: 10.1016/j.marpolbul.2004.02.037 15111030.

47. Porte C, Janer G, Lorusso L, Ortiz-Zarragoitia M, Cajaraville M, Fossi M, et al. Endocrine disruptors in marine organisms: Approaches and perspectives. Comparative Biochemistry and Physiology Part C-Toxicology & Pharmacology. 2006; 143(3): 303–315. doi: 10.1016/j.cbpc.2006.03.004 16723279.

48. Gong J, Huang C, Shu L, Bao C, Huang H, Ye H, et al. The retinoid X receptor from mud crab: new insights into its roles in ovarian development and related signaling pathway. Scientific Reports. 2016; 6: 23654. doi: 10.1038/srep23654 27009370.

49. Sricharoen S, Kim J, Tunkijjanukij S, Soderhall I. Exocytosis and proteomic analysis of the vesicle content of granular hemocytes from a crayfish. Developmental and Comparative Immunology. 2005; 29(12): 1017–1031. doi: 10.1016/j.dci.2005.03.010 15975654.

50. Mayer M, Bukau B. Hsp70 chaperones: Cellular functions and molecular mechanism. Cellular and Molecular Life Sciences. 2005; 62(6): 670–684. doi: 10.1007/s00018-004-4464-6 15770419.

51. Romani W, Russ D. Acute effects of sex-specific sex hormones on heat shock proteins in fast muscle of male and female rats. European Journal of Applied Physiology. 2013;113(10): 2503–2510. doi: 10.1007/s00421-013-2686-8 23821238.

52. Dhamad A, Zhou Z, Zhou J, Du Y. Systematic proteomic identification of the Heat Shock Proteins (Hsp) that interact with estrogen receptor alpha (ER alpha) and biochemical characterization of the ER alpha-Hsp70 interaction. Plos One. 2016; 11(8): e0160312. doi: 10.1371/journal.pone.0160312 27483141.

53. Chan S, He J, Chu K, Sun C. The shrimp heat shock cognate 70 functions as a negative regulator in vitellogenin gene expression. Biology of Reproduction. 2014; 91(1): 14. doi: 10.1095/biolreprod.113.117200 24790159.

54. Lasko P, Ashburner M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature. 1988; 335: 611–617. doi: 10.1038/335611a0 3140040

55. Hay B, Jan L, Jan Y. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell. 1988; 55: 577–587. doi: 10.1016/0092-8674(88)90216-4 3052853

56. Aflalo E, Bakhrat A, Raviv S, Harari D, Sagi A, Abdu U. Characterization of a Vasa-like gene from the Pacific white shrimp Litopenaeus vannamei and its expression during oogenesis. Molecular Reproduction and Development. 2007; 74(2): 172–177. doi: 10.1002/mrd.20622 16955407.

57. Zhou Q, Shao M, Qin Z, Kang Q, Zhang Z. Cloning, characterization, and expression analysis of the DEAD-box family genes, Fc-vasa and Fc-PL10a, in Chinese shrimp (Fenneropenaeus chinensis). Chinese Journal of Oceanology and Limnology. 2010; 28: 37–45 (In Chinese with English abstract). doi: 10.1007/s00343-010-9231-y

58. Nakkrasae L, Damrongphol P. A vasa-like gene in the giant freshwater prawn, Macrobrachium rosenbergii. Molecular Reproduction and Development. 2007; 74(7): 835–842. doi: 10.1002/mrd.20680 17186538.

59. Extavour C, Akam M. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development. 2003; 130(24): 5869–5884. doi: 10.1242/dev.00804 14597570.

60. Wang Y, Chen Y, Han K, Zou Z, Zhang Z. A vasa gene from green mud crab Scylla paramamosain and its expression during gonadal development and gametogenesis. Molecular Biology Reports. 2012; 39(4): 4327–4335. doi: 10.1007/s11033-011-1220-5 21842219.

61. Wang Q, Fang D, Sun J, Wang Y, Wang J, Liu L. Characterization of the vasa gene in the Chinese mitten crab Eriocheir sinensis: a germ line molecular marker. Journal of Insect Physiology. 2012;58(7):960–5. doi: 10.1016/j.jinsphys.2012.04.012 22562064.

62. Cardinali M, Gioacchini G, Candiani S, Pestarino M, Yoshizaki G, Carnevali O. Hormonal regulation of vasa-like messenger RNA expression in the ovary of the marine teleost Sparus aurata. Biology of Reproduction. 2004; 70(3): 737–743. doi: 10.1095/biolreprod.103.021428 14613903.

63. Gao J, Wang X, Zou Z, Jia X, Wang Y, Zhang Z. Transcriptome analysis of the differences in gene expression between testis and ovary in green mud crab (Scylla paramamosain). Bmc Genomics. 2014; 15(1): 585. doi: 10.1186/1471-2164-15-585 25015001.

64. Prathibha Y, Senthilkumaran B. Expression of wnt4/5 during reproductive cycle of catfish and wnt5 promoter analysis. Journal of Endocrinology. 2017; 232(1): 1–13. doi: 10.1530/JOE-16-0104 27875264.

65. Kim H, Schleiffarth J, Jessurun J, Sumanas S, Petryk A, Lin S, et al. Wnt5 signaling in vertebrate pancreas development. Bmc Biology. 2005; 3(1): 23. doi: 10.1186/1741-7007-3-23 16246260.

66. Huang L, Xiao A, Choi S, Kan Q, Zhou W, Chacon-Heszele M, et al. Wnt5a is necessary for normal kidney development in zebrafish and mice. Nephron Experimental Nephrology. 2014; 128(1–2): 80–88. doi: 10.1159/000368411 25412793.

67. Kilian B, Mansukoski H, Barbosa F, Ulrich F, Tada M, Heisenberg C. The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mechanisms of Development. 2003; 120(4): 467–476. doi: 10.1016/s0925-4773(03)00004-2 12676324

68. Naillat F, Prunskaite-Hyyrylainen R, Pietila I, Sormunen R, Jokela T, Shan J, et al. Wnt4/5a signalling coordinates cell adhesion and entry into meiosis during presumptive ovarian follicle development. Human Molecular Genetics. 2010; 19(8): 1539–1550. doi: 10.1093/hmg/ddq027 20106871.

69. Scott Q. Yolk synthesis in the marine shrimp, Penaeus vannamei. American Zoologist. 2001; 41: 458–464. doi: 10.2307/3884476

70. Ye H, Song P, Ma J, Huang H, Wang G. Changes in progesterone levels and distribution of progesterone receptor during vitellogenesis in the female mud crab (Scylla paramamosain). Marine and Freshwater Behaviour and Physiology. 2010; 43(1): 25–35. doi: 10.1080/10236241003654113

71. Yano I. Induced ovarian maturation and spawning in greasyback shrimp, Metapenaeus ensis, by progesterone. Aquaculture. 1985; 47: 223–229. doi: 10.1016/0044-8486(85)90068-7

72. Uawisetwathana U, Leelatanawit R, Klanchui A, Prommoon J, Klinbunga S, Karoonuthaisiri N. Insights into eyestalk ablation mechanism to induce ovarian maturation in the Black Tiger Shrimp. Plos One. 2011; 6(9): e24427. doi: 10.1371/journal.pone.0024427 21915325.

73. Wainwright G, Prescott M, Rees H, Webster S. Mass spectrometric determination of methyl farnesoate profiles and correlation with ovarian development in the edible crab, Cancer pagurus. Journal of Mass Spectrometry. 1996; 31(12): 1338–1344. doi: 10.1002/(sici)1096-9888(199612)31:12<1338::Aid-jms428>3.0.Co;2-a

74. Nagaraju G. Is methyl farnesoate a crustacean hormone? Aquaculture. 2007; 272(1–4): 39–54. doi: 10.1016/j.aquacutture.2007.05.014

75. Borst D, Ogan J, Tsukimura B, Claerhout T, Holford K. Regulation of the crustacean mandibular organ. American Zoologist. 2001; 41(3): 430–441. doi: 10.1668/0003-1569(2001)041[0430:Rotcmo]2.0.Co;2

76. Goldstein J, Brown M. Regulation of the mevalonate pathway. Nature. 1990; 343: 425–430. doi: 10.1038/343425a0 1967820

77. Holford K, Edwards K, Bendena W, Tobe S, Wang Z, Borst D. Purification and characterization of a mandibular organ protein from the American lobster, Homarus americanus: a putative farnesoic acid O-methyltransferase. Insect Biochemistry and Molecular Biology. 2004; 34(8): 785–798. doi: 10.1016/j.ibmb.2004.04.003 15262283.

78. Kontogiannatos D, Swevers L, Maenaka K, Park E, Iatrou K, Kourti A. Functional characterization of a juvenile hormone esterase related gene in the moth Sesamia nonagrioides through RNA Interference. Plos One. 2013; 8(9): e73834. doi: 10.1371/journal.pone.0073834 24040087.

79. Tobe S, Young D, Khoo H, Baker F. Farnesoic acid as a major product of release from crustacean mandibular organs in vitro. Journal of Experimental Zoology.1989; 249(2): 165–171. doi: 10.1002/jez.1402490208

80. Niwa R, Sakudoh T, Namiki T, Saida K, Fujimoto Y, Kataoka H. The ecdysteroidogenic P450 Cyp302a1/disembodied from the silkworm, Bombyx mori, is transcriptionally regulated by prothoracicotropic hormone. Insect Molecular Biology. 2005; 14(5): 563–571. doi: 10.1111/j.1365-2583.2005.00587.x 16164612.

81. Gao J, He J, Shi X, Stefanovic-Racic M, Xu M, O'Doherty R, et al. Sex-specific effect of estrogen sulfotransferase on mouse models of Type 2 diabetes. Diabetes. 2012; 61(6): 1543–1551. doi: 10.2337/db11-1152 22438574.

82. Swevers L, Lambert J, Loof A. Metabolism of vertebrate-type steroids by tissues of three crustacean species. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry. 1991; 99: 35–41. doi: 10.1016/0305-0491(91)90004-W

83. Webster S, Keller R, Dircksen H. The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. General and Comparative Endocrinology. 2012;175(2):217–33. doi: 10.1016/j.ygcen.2011.11.035 22146796.

84. Bao C, Yang Y, Huang H, Ye H. Neuropeptides in the cerebral ganglia of the mud crab, Scylla paramamosain: transcriptomic analysis and expression profiles during vitellogenesis. Scientific Reports. 2015; 5: 17055. doi: 10.1038/srep17055 26592767.

85. Hussain Y, Ding Q, Connelly P, Brunt J, Ban M, McIntyre A, et al. G-Protein estrogen receptor as a regulator of low-density lipoprotein cholesterol metabolism cellular and population genetic studies. Arteriosclerosis Thrombosis and Vascular Biology. 2015; 35(1): 213–221. doi: 10.1161/atvbaha.114.304326 25395619.

86. Oosthuyse T, Bosch A. Oestrogen's regulation of fat metabolism during exercise and gender specific effects. Current Opinion in Pharmacology. 2012; 12(3): 363–371. doi: 10.1016/j.coph.2012.02.008 22398320.

87. Skern-Mauritzen R, Frost P, Dalvin S, Kvamme B, Sommerset I, Nilsen F. A trypsin-like protease with apparent dual function in early Lepeophtheirus salmonis (Kroyer)development. Bmc Molecular Biology. 2009; 10(1): 1–11. doi: 10.1186/1471-2199-10-44 19439101.

88. Wu J, Min R, Wu M, Chen W. Research progresses on the carboxypeptidase. Journal of Food Science and Biotechnology. 2012; 31: 793–801 (In Chinese with English abstract). doi: 10.3969/j.issn.1673-1689.2012.08.002

89. Chen L, Jiang H, Zhou Z, Li K, Li K, Deng G, et al. Purification of vitellin from the ovary of Chinese mitten-handed crab (Eriocheir sinensis) and development of an antivitellin ELISA. Comparative Biochemistry and Physiology Part B: Biochemistry & Molecular Biology. 2004; 138(3): 305–311. doi: 10.1016/j.cbpc.2004.04.012 15253879.

90. Harrison K. The role of nutrition in maturation, reproduction and embryonic development of decapod crustaceans: a review. Journal of Shellfish Research. 1990; 9: 1–28.

91. Murphy D. The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Progress in Lipid Research. 2001; 40(5): 325–438. doi: 10.1016/s0163-7827(01)00013-3 11470496.

92. Sittikankaew K, Hiransuchalert R, Yocawibun P, Yamano K, Klinbunga S. Identification, characterization and expression of adipose differentiation-related protein (ADRP) gene and protein in ovaries of the giant tiger shrimp Penaeus monodon. Aquaculture. 2010; 308: S91–S9. doi: 10.1016/j.aquaculture.2010.06.039

93. Brady P, Elizur A, Cummins S, Ngyuen N, Williams R, Knibb W. Differential expression microarrays reveal candidate genes potentially associated with reproductive dysfunction of captive-reared prawn Penaeus monodon. Aquaculture. 2013; 400: 14–28. doi: 10.1016/j.aquaculture.2013.02.038

94. Merlin J, Mohanlal D, Balasubramanian C, Sherly T, Subramoniam T, Syamadayal J, et al. Induction of vitellogenesis and reproductive maturation in tiger shrimp, Penaeus monodon by 17ß-estradiol and 17α-hydroxyprogesterone: in vivo and in vitro studies. Invertebrate Reproduction & Development. 2015; 59(3): 166–175. doi: 10.1080/07924259.2015.1051192

95. Qiu S, Vazquez J, Boulger E, Liu H, Xue P, Hussain M, et al. Hepatic estrogen receptor α is critical for regulation of gluconeogenesis and lipid metabolism in males. Scientific Reports. 2017; 7(1): 1661. doi: 10.1038/s41598-017-01937-4 28490809.

96. Thornton J, Need E, Crews D. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science. 2003; 301(5640): 1714–1717. doi: 10.1126/science.1086185 14500980.

97. Lu Y, Wu X, Pan G, Wang W, Hou W, Cheng Y. Expression analysis of PtERR during the molting cycle in Portunus trituberculatus. Journal of Shanghai Ocean University. 2016; 25(3): 321–328 (In Chinese with English abstract). doi: 10.12024/jsou.20150801528

98. Giguère V. Orphan nuclear receptors: from gene to function. Endocrine Reviews. 1999; 20(5): 689–725. doi: 10.1210/edrv.20.5.0378 10529899

99. Tarrant A, Greytak S, Callard G, Hahn M. Estrogen receptor-related receptors in the killifish Fundulus heteroclitus: diversity, expression, and estrogen responsiveness. Journal of Molecular Endocrinology. 2006; 37(1): 105–120. doi: 10.1677/jme.1.01976 16901928.


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#