Insights into eyestalk ablation mechanism to induce ovarian maturation in the black tiger shrimp

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Uawisetwathana, Umaporn ^a   Leelatanawit, Rungnapa ^a   Klanchui, Amornpan ^a   Prommoon, Juthatip ^a   Klinbunga, Sirawut ^a,b   Karoonuthaisiri, Nitsara ^a  

^a NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^b CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COMPLEMENTARY DNA; GONADORELIN; PROGESTERONE;

ANIMAL REPRODUCTIVE PROCEDURES; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; ELECTRON TRANSPORT; EYESTALK ABLATION; FEMALE; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MAPPING; GENETIC VARIABILITY; HORMONAL REGULATION; IMMUNE RESPONSE GENE; NONHUMAN; OVARY DEVELOPMENT; PENAEUS MONODON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHRIMP; TRANSCRIPTOMICS; UPREGULATION; VALIDATION PROCESS; VITELLOGENESIS; ANIMAL; ENDOCRINE GLAND; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHODOLOGY; OVARY; PENAEIDAE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CRUSTACEA; PENAEUS MONODON;

ANIMALS; ENDOCRINE GLANDS; FEMALE; GENE EXPRESSION PROFILING; GONADOTROPIN-RELEASING HORMONE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARY; PENAEIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 80052552082     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024427     Document Type: Article

References (72)

1. Bray WA, Lawrence AL, eds. (1992) Reproduction of Penaeus species in captivity Amsterdam, The Netherlands Elsevier pp. 93-170.
2. Browdy CL, Samocha TM, (1985) The effect of eyestalk ablation on spawning, molting and mating of Penaeus semisulcatus de Haan. Aquaculture 49: 19-29.
3. Benzie JAH, (1998) Penaeid genetics and biotechnology. Aquaculture 164: 23-47.
4. Quackenbush LS, (1991) Regulation of vitellogenesis in penaeid shrimp; In: DeLoach P, Dougherty WJ, Davidson MA, editors. Amsterdam Elsevier pp. 125-140.
5. Tan-Fermin JD, Pudadera RA, (1989) Ovarian maturation stages of the wild giant tiger prawn, Penaeus monodon Fabricius. Aquaculture 77: 229-242.
6. Rodrguez A, (1996) A comparative study of the ovarian development in wild and pond-reared shrimp, Penaeus kerathurus (Forskål, 1775). Aquaculture 148: 63-75.
7. Santiago J, Alfredo C, (1977) Successful spawning of cultured Penaeus monodon Fabricius after eyestalk ablation. Aquaculture 11: 185-196.
8. Beltz BS, (1988) Crustacean neurohormones. Endocrinology of Selected Invertebrate Types. Invertebrate Endocrinology 2: 235-258.
9. Chang ES, eds. (1992) Endocrinology Amsterdam Elsevier pp. 53-91.
10. Quackenbush LS, Herrnkind WF, (1981) Regulation of molt and gonadal development in the spiny lobster, Panulirus argus (Crustacea: Palinuridae): Effect of eyestalk ablation. Comparative Biochemistry and Physiology Part A: Physiology 69: 523-527.
11. Treerattrakool S, Panyim S, Chan SM, Withyachumnarnkul B, Udomkit A, (2008) Molecular characterization of gonad-inhibiting hormone of Penaeus monodon and elucidation of its inhibitory role in vitellogenin expression by RNA interference. FEBS J 275: 970-980.
12. Hoang T, Lee SY, Keenan CP, Marsden GE, (2002) Ovarian maturation of the banana prawn, Penaeus merguiensis de Man under different light intensities. Aquaculture 208: 159-168.
13. Karoonuthaisiri N, Sittikankeaw K, Preechaphol R, Kalachikov S, Wongsurawat T, et al. (2009) ReproArray(GTS): a cDNA microarray for identification of reproduction-related genes in the giant tiger shrimp Penaeus monodon and characterization of a novel nuclear autoantigenic sperm protein (NASP) gene. Comp Biochem Physiol Part D Genomics Proteomics 4: 90-99.
14. Wongsurawat T, Leelatanawit R, Thamniemdee N, Uawisetwathana U, Karoonuthaisiri N, et al. (2010) Identification of testis-relevant genes using in silico analysis from testis ESTs and cDNA microarray in the black tiger shrimp (Penaeus monodon). BMC Mol Biol 11: 55.
15. Leelatanawit R, Uawisetwathana U, Klinbunga S, Karoonuthaisiri N, (2011) A cDNA microarray, UniShrimpChip, for identification of genes relevant to testicular development in the black tiger shrimp (Penaeus monodon). BMC Mol Biol 12: 15.
16. Brothers SP, Janovick JA, Conn PM, (2006) Calnexin regulated gonadotropin-releasing hormone receptor plasma membrane expression. J Mol Endocrinol 37: 479-488.
17. Subramoniam T, (2011) Mechanisms and control of vitellogenesis in crustaceans. Fisheries Science 77: 1-21.
18. Chu KH, Tam YK, Chung CK, Ng WL, (1993) Morphometric relationships and reproductive maturation of the shrimp, Metapenaeus ensis, from commercial catches in Hong Kong. Fisheries Research 18: 187-197.
19. King JE, (1948) A study of the reproductive organs of the common marine shrimp, Penaeus setiferus (Linnaeus). Biol Bull 94: 244-262.
20. Cummings WC, (1961) Maturation and Spawning of the Pink Shrimp, Penaeus duorarum Burkenroad. Transactions of the American Fisheries Society 90: 462-468.
21. Meusy JJ, Payen GG, (1988) Female reproduction in malacostracan Crustacea. Zool Sci 5: 217-265.
22. Okumura T, Kim YK, Kawazoe I, Yamano K, Tsutsui N, et al. (2006) Expression of vitellogenin and cortical rod proteins during induced ovarian development by eyestalk ablation in the kuruma prawn, Marsupenaeus japonicus. Comparative Biochemistry and Physiology- Part A: Molecular & Integrative Physiology 143: 246-253.
23. Sainz-Hernández JC, Racotta IS, Dumas S, Hernández-López J, (2008) Effect of unilateral and bilateral eyestalk ablation in Litopenaeus vannamei male and female on several metabolic and immunologic variables. Aquaculture 283: 188-193.
24. Rosas C, Fernandez I, Brito R, Diaz-Iglesia E, (1993) The effect of eyestalk ablation on the energy balance of the pink shrimp, Penaeus notialis. Comparative Biochemistry and Physiology Part A: Physiology 104: 183-187.
25. Yepiz-Plascencia G, Vargas-Albores F, Higuera-Ciapara I, (2000) Penaeid shrimp hemolymph lipoproteins. Aquaculture 191: 177-189.
26. Garrett R, Grisham CM, (2010) Biochemistry Boston, MA, USA Mary Finch.
27. Teshima S-I, Kanazawa A, Sasada H, (1983) Nutritional value of dietary cholesterol and other sterols to larval prawn, Penaeus japonicus Bate. Aquaculture 31: 159-167.
28. Lytle JS, Lytle TF, Ogle JT, (1990) Polyunsaturated fatty acid profiles as a comparative tool in assessing maturation diets of Penaeus vannamei. Aquaculture 89: 287-299.
29. Middleditch BS, Missler SR, Ward DG, McVey JB, Brown A, et al. (1979) MATURATION OF PENAEID SHRIMP: DIETARY FATTY ACIDS. Proceedings of the World Mariculture Society 10: 472-476.
30. Benzie JAH, (1997) A review of the effect of genetics and environment on the maturation and larval quality of the giant tiger prawn Penaeus monodon. pp. 69-85 Proceedings of the fish and shellfish Larviculture Symposium Aquaculture.
31. Meunpol O, Iam-Pai S, Suthikrai W, Piyatiratitivorakul S, (2007) Identification of progesterone and 17[alpha]-hydroxyprogesterone in polychaetes (Perinereis sp.) and the effects of hormone extracts on penaeid oocyte development in vitro. Aquaculture 270: 485-492.
32. Wouters R, Molina C, Lavens P, Calderón J, (2001) Lipid composition and vitamin content of wild female Litopenaeus vannamei in different stages of sexual maturation. Aquaculture 198: 307-323.
33. Harrison KE, (1990) The role of nutrition in maturation, reproduction and embryonic development of decapod crustaceans: a review. J Shellfish Res 9: 1-28.
34. Primavera JH, (1983) Broodstock of Surgo, Penaeus monodon Fabricius. Southeast Asian Fisheries Development Center, Extension Manual 7: Aquaculture Department SEAFDEC, Iloilo, Philippines.
35. O'Leary CD, Matthews AD, (1990) Lipid class distribution and fatty acid composition of wild and farmed prawn, Penaeus monodon (Fabricius). Aquaculture 89: 65-81.
36. Cahu C, Guillaume JC, Stéphan G, Chim L, (1994) Influence of phospholipid and highly unsaturated fatty acids on spawning rate and egg and tissue composition in Penaeus vannamei fed semi-purified diets. Aquaculture 126: 159-170.
37. Yano I, (1995) Final oocyte maturation, spawning and maturration in penaeid shrimp. J Exp Mar Biol Ecol 193: 113-118.
38. Ngernsoungnern P, Ngernsoungnern A, Kavanaugh S, Sobhon P, Sower SA, et al. (2008) The presence and distribution of gonadotropin-releasing hormone-liked factor in the central nervous system of the black tiger shrimp, Penaeus monodon. General and Comparative Endocrinology 155: 613-622.
39. Subramaniam T, Keller R, (1993) A new look at the endocrine regulation of egg maturation in the decapod crustacean. Curr Sci 65: 619-623.
40. Seachord CL, VandeVoort CA, Duffy DM, (2005) Adipose differentiation-related protein: a gonadotropin- and prostaglandin-regulated protein in primate periovulatory follicles. Biol Reprod 72: 1305-1314.
41. Schmitt A, Nebreda AR, (2002) Signalling pathways in oocyte meiotic maturation. J Cell Sci 115: 2457-2459.
42. Ngernsoungnern A, Ngernsoungnern P, Weerachatyanukul W, Chavadej J, Sobhon P, et al. (2008) The existence of gonadotropin-releasing hormone (GnRH) immunoreactivity in the ovary and the effects of GnRHs on the ovarian maturation in the black tiger shrimp Penaeus monodon. Aquaculture 279: 197-203.
43. Amano M, Okumura T, Okubo K, Amiya N, Takahashi A, et al. (2009) Biochemical Analysis and lmmunohistochemical Examination of a GnRH-like Immunoreactive Peptide in the Central Nervous System of a Decapod Crustacean, the Kuruma Prawn (Marsupenaeus japonicus). Zoolog Sci 26: 840.
44. Ngernsoungnern P, Ngernsoungnern A, Sobhon P, Sretarugsa P, (2009) Gonadotropin-releasing hormone (GnRH) and a GnRH analog induce ovarian maturation in the giant freshwater prawn, Macrobrachium rosenbergii. Invertebrate Reproduction & Development 53: 125-135.
45. Corbett EF, Michalak M, (2000) Calcium, a signaling molecule in the endoplasmic reticulum? Trends in Biochemical Sciences 25: 307-311.
46. Okazaki Y, Ohno H, Takase K, Ochiai T, Saito T, (2000) Cell surface expression of calnexin, a molecular chaperone in the endoplasmic reticulum. J Biol Chem 275: 35751-35758.
47. Carnegie JA, Tsang BK, (1984) The calcium-calmodulin system: participation in the regulation of steroidogenesis at different stages of granulosa cell differentiation. Biol Reprod 30: 515-522.
48. Cicirelli MF, Smith LD, (1987) Do calcium and calmodulin trigger maturation in amphibian oocytes? Developmental Biology 121: 48-57.
49. Francisco SK-S, Schuetz AW, (1987) Sources of calcium and the involvement of calmodulin during steroidogenesis and oocyte maturation in follicles of Rana pipiens. J Exp Zool 244: 133-143.
50. Benninghoff AD, Thomas P, (2005) Involvement of calcium and calmodulin in the regulation of ovarian steroidogenesis in Atlantic croaker (Micropogonias undulatus) and modulation by Aroclor 1254. Gen Comp Endocrinol 144: 211-223.
51. Nakatsuji T, Lee CY, Watson RD, (2009) Crustacean molt-inhibiting hormone: structure, function, and cellular mode of action. Comp Biochem Physiol A Mol Integr Physiol 152: 139-148.
52. Kugu K, Dharmarajan AM, Preutthipan S, Wallach EE, (1995) Role of calcium/calmodulin-dependent protein kinase II in gonadotrophin-induced ovulation in in vitro perfused rabbit ovaries. J Reprod Fertil 103: 273-278.
53. Kruevaisayawan H, Vanichviriyakit R, Weerachatyanukul W, Withyachumnarnkul B, Chavadej J, et al. (2010) Oogenesis and formation of cortical rods in the black tiger shrimp, Penaeus monodon. Aquaculture 301: 91-98.
54. Preechaphol R, Klinbunga S, Yamano K, Menasveta P, (2010) Molecular cloning and expression of progestin membrane receptor component 1 (Pgmrc1) of the giant tiger shrimp Penaeus monodon. Gen Comp Endocrinol 168: 440-449.
55. Tsutsui N, Kawazoe I, Ohira T, Jasmani S, Yang WJ, et al. (2000) Molecular Characterization of a cDNA Encoding Vitellogenin and Its Expression in the Hepatopancreas and Ovary during Vitellogenesis in the Kuruma Prawn, Penaeus japonicus. Zool Sci 17: 651-660.
56. Ravid T, Tietz A, Khayat M, Boehm E, Michelis R, et al. (1999) Lipid Accumulation in the Ovaries of a Marine Shrimp Penaeus Semisulcatus (DE HAAN). J Exp Biol 202: 1819-1829.
57. Qiu G-F, Yamano K, Unuma T, (2005) Cathepsin C transcripts are differentially expressed in the final stages of oocyte maturation in kuruma prawn Marsupenaeus japonicus. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 140: 171-181.
58. Yamano K, Qiu GF, Unuma T, (2004) Molecular cloning and ovarian expression profiles of thrombospondin, a major component of cortical rods in mature oocytes of penaeid shrimp, Marsupenaeus japonicus. Biol Reprod 70: 1670-1678.
59. Khayat M, Babin PJ, Funkenstein B, Sammar M, Nagasawa H, et al. (2001) Molecular characterization and high expression during oocyte development of a shrimp ovarian cortical rod protein homologous to insect intestinal peritrophins. Biol Reprod 64: 1090-1099.
60. Bauer R, Lehmann C, Martini J, Eckardt F, Hoch M, (2004) Gap junction channel protein innexin 2 is essential for epithelial morphogenesis in the Drosophila embryo. Mol Biol Cell 15: 2992-3004.
61. Bohrmann J, Zimmermann J, (2008) Gap junctions in the ovary of Drosophila melanogaster: localization of innexins 1, 2, 3 and 4 and evidence for intercellular communication via innexin-2 containing channels. BMC Dev Biol 8: 111.
62. Ito M, Yuan CX, Malik S, Gu W, Fondell JD, et al. (1999) Identity between TRAP and SMCC complexes indicates novel pathways for the function of nuclear receptors and diverse mammalian activators. Mol Cell 3: 361-370.
63. Yuan CX, Ito M, Fondell JD, Fu ZY, Roeder RG, (1998) The TRAP220 component of a thyroid hormone receptor- associated protein (TRAP) coactivator complex interacts directly with nuclear receptors in a ligand-dependent fashion. Proc Natl Acad Sci USA 95: 7939-7944.
64. Zhu X, Cheng SY, (2010) New insights into regulation of lipid metabolism by thyroid hormone. Curr Opin Endocrinol Diabetes Obes 17: 408-413.
65. Ito M, Yuan CX, Okano HJ, Darnell RB, Roeder RG, (2000) Involvement of the TRAP220 component of the TRAP/SMCC coactivator complex in embryonic development and thyroid hormone action. Mol Cell 5: 683-693.
66. Verghese B, Radhakrishnan EV, Padhi A, (2008) Effect of moulting, eyestalk ablation, starvation and transportation on the immune response of the Indian spiny lobster, Panulirus homarus. Aquaculture Research 39: 1009-1013.
67. Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, et al. (2007) Mating and immunity in invertebrates. Trends in Ecology & Evolution 22: 48-55.
68. Bengtsson H, eds. (2004) {aroma}- {A}n {R} {O}bject-oriented {M}icroarray {A}nalysis environment}: Mathematical Statistics, Centre for Mathematical Sciences, Lund University, Sweden.
69. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
70. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
71. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M, (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182-185.
72. Salomonis N, Hanspers K, Zambon AC, Vranizan K, Lawlor SC, et al. (2007) GenMAPP 2: new features and resources for pathway analysis. BMC Bioinformatics 8: 217.