Gene Silencing in Crustaceans: From Basic Research to Biotechnologies

Genes

Volumn 4, Issue 4, 2013, Pages 620-645

  Sagi, Amir ^a   Manor, Rivka ^a   Ventura, Tomer ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b UNIVERSITY OF THE SUNSHINE COAST   (Australia)

Author keywords

Androgenic gland; Biotechnology; Crustaceans; Gene function; Humoral defense mechanisms; Insulin like peptide; RNA interference

Indexed keywords

BETA INTEGRIN; CASPASE 3; OXIDOREDUCTASE; PROPHENOL OXIDASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AQUACULTURE; ARTEMIA FRANCISCANA; BIOMINERALIZATION; BIOTECHNOLOGY; CARCINUS MAENAS; CHERAX QUADRICARINATUS; CRUSTACEA; DAPHNIA MAGNA; DAPHNIA PULEX; DSX1 GENE; DSX2 GENE; FENNEROPENAEUS CHINENSIS; GENE; GENE FUNCTION; GENE SILENCING; IMMUNOPRECIPITATION; IN VIVO STUDY; INNATE IMMUNITY; LITOPENAEUS; LITOPENAEUS SCHMITTI; LITOPENAEUS VANNAMEI; MACROBRACHIUM ROSENBERGII; MARSUPENAEUS JAPONICUS; METAPENAEUS ENSIS; NONHUMAN; PARHYALE ULTRABITHORAX; PENAEUS MONODON; PROCAMBARUS; PROCAMBARUS CLARKIA; REVIEW; RNA INTERFERENCE; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL MATURITY; TAURA SYNDROME VIRUS; UCA PUGILATOR; WHITE SPOT SYNDROME VIRUS;

EID: 84973168537     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes4040620     Document Type: Review

References (128)

1. Fire, A.; Xu, S.; Montgomery, M. K.; Kostas, S. A.; Driver, S. E.; Mello, C. C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391, 806-811.
2. Dorsett, Y.; Tuschl, T. siRNAs: Applications in functional genomics and potential as therapeutics. Nat. Rev. Drug Discov. 2004, 3, 318-329.
3. Fire, A. Z.; Mello, C. C. The Nobel Prize in Physiology or Medicine 2006. Available online: http: //www. nobelprize. org/nobel_prizes/medicine/laureates/2006/ (accessed on 26 January 2013).
4. Agrawal, N.; Dasaradhi, P. V. N.; Mohmmed, A.; Malhotra, P.; Bhatnagar, R. K.; Mukherjee, S. K. RNA interference: Biology, mechanism, and applications. Microbiol. Mol. Biol. Rev. 2003, 67, 657-685.
5. Qi, Y. J.; Hannon, G. J. Uncovering RNAi mechanisms in plants: Biochemistry enters the foray. FEBS Lett. 2005, 579, 5899-5903.
6. Watson, J. M.; Fusaro, A. F.; Wang, M. B.; Waterhouse, P. M. RNA silencing platforms in plants. FEBS Lett. 2005, 579, 5982-5987.
7. Lu, Y.; Sun, P. S. Viral resistance in shrimp that express an antisense Taura syndrome virus coat protein gene. Antivir. Res. 2005, 67, 141-146.
8. Sun, P. S.; Venzon, N. C., Jr.; Calderon, F. R. O.; Esaki, D. M. Evaluation of methods for DNA delivery into shrimp zygotes of Penaeus (Litopenaeus) vannamei. Aquaculture 2005, 243, 19-26.
9. Söderhäll, I.; Kim, Y.-A.; Jiravanichpaisal, P.; Lee, S.-Y.; Söderhäll, K. An ancient role for a Prokineticin domain in invertebrate hematopoiesis. J. Immunol. 2005, 174, 6153-6160.
10. Robalino, J.; Browdy, C. L.; Prior, S.; Metz, A.; Parnell, P.; Gross, P.; Warr, G. Induction of antiviral immunity by double-stranded RNA in a marine invertebrate. J. Virol. 2004, 78, 10442-10448.
11. Robalino, J.; Bartlett, T.; Shepard, E.; Prior, S.; Jaramillo, G.; Scura, E.; Chapman, R. W.; Gross, P. S.; Browdy, C. L.; Warr, G. W. Double-stranded RNA induces sequence-specific antiviral silencing in addition to nonspecific immunity in a marine shrimp: Convergence of RNA interference and innate immunity in the invertebrate antiviral response? J. Virol. 2005, 79, 13561-13571.
12. Kim, S.-S.; Garg, H.; Joshi, A.; Manjunath, N. Strategies for targeted nonviral delivery of siRNAs in vivo. Trends Mol. Med. 2009, 15, 491-500.
13. Ahyong, S. T.; Lowry, J. K.; Alonso, M.; Bamber, R. N.; Boxshall, G. A.; Castro, P.; Gerken, S.; Karaman, G. S.; Goy, J. W.; Jones, D. S.; et al. Subphylum Crustacea Brünnich, 1772. In Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness; Zhang, Z. Q., Ed.; Magnolia Press: Auckland, New Zealand, 2011; pp. 165-191.
14. LeBlanc, G. A. Crustacean endocrine toxicology: A review. Ecotoxicology 2007, 16, 61-81.
15. Stillman, J. H. Acclimation capacity underlies susceptibility to climate change. Science 2003, 301, 65.
16. Ventura, T.; Sagi, A. The insulin-like androgenic gland hormone in crustaceans: From a single gene silencing to a wide array of sexual manipulation-based biotechnologies. Biotechnol. Adv. 2012, 30, 1543-1550.
17. Gherardi, F.; Aquiloni, L.; Diéguez-Uribeondo, J.; Tricarico, E. Managing invasive crayfish: Is there a hope? Aquat. Sci. 2011, 73, 185-200.
18. Glenner, H.; Thomsen, P. F.; Hebsgaard, M. B.; Sørensen, M. V.; Willerslev, E. The origin of insects. Science 2006, 314, 1883-1884.
19. Lukhtanov, V.; Kuznetsova, V. What genes and chromosomes say about the origin and evolution of insects and other arthropods. Russ. J. Genet. 2010, 46, 1115-1121.
20. Sorgeloos, P.; Dhert, P.; Candreva, P. Use of the brine shrimp, Artemia spp., in marine fish larviculture. Aquaculture 2001, 200, 147-159.
21. Colbourne, J. K.; Pfrender, M. E.; Gilbert, D.; Thomas, W. K.; Tucker, A.; Oakley, T. H.; Tokishita, S.; Aerts, A.; Arnold, G. J.; Basu, M. K.; et al. The ecoresponsive genome of Daphnia pulex. Science 2011, 331, 555-561.
22. Kamath, R. S.; Ahringer, J. Genome-Wide RNAi screening in Caenorhabditis elegans. Methods 2003, 30, 313-321.
23. Aigner, A. Delivery systems for the direct application of siRNAs to induce RNA interference (RNAi) in vivo. J. Biomed. Biotechnol. 2006, 2006, ArticleID 71659.
24. Luquet, G.; Marin, F. Biomineralisations in crustaceans: Storage strategies. C. R. Palevol. 2004, 3, 515-534.
25. Travis, D. F. The deposition of skeletal structures in the Crustacea. 1. The histology of the gastrolith skeletal tissue complex and the gastrolith in the crayfish, Orconectes (cambaus) verilis Hagen-Decapoda. Biol. Bull. 1960, 16, 137-149.
26. Travis, D. F.; Friberg, U. The deposition of skeletal structures in the crustacea. Vi. Microradiographic studies of the exoskeleton of the crayfish Orconectes virilis hagen. J. Ultrastruct. Res. 1963, 59, 285-301.
27. Shechter, A.; Glazer, L.; Cheled, S.; Mor, E.; Weil, S.; Berman, A.; Bentov, S.; Aflalo, E. D.; Khalaila, I.; Sagi, A. A gastrolith protein serving a dual role in the formation of an amorphous mineral containing extracellular matrix. Proc. Natl. Acad. Sci. USA 2008, 105, 7129-7134.
28. Glazer, L.; Shechter, A.; Tom, M.; Yudkovski, Y.; Weil, S.; Aflalo, E. D.; Pamuru, R. R.; Khalaila, I.; Bentov, S.; Berman, A.; et al. A protein involved in the assembly of an extracellular calcium storage matrix. J. Biol. Chem. 2010, 258, 12831-12839.
29. Hughes, C. L.; Kaufman, T. C. Hox genes and the evolution of the arthropod body plan. Evol. Dev. 2002, 4, 459-499.
30. Copf, T.; Rabet, N.; Averof, M. Knockdown of spalt function by RNAi causes de-repression of Hox genes and homeotic transformations in the crustacean Artemia franciscana. Dev. Biol. 2006, 298, 87-94.
31. Liubicich, D. M.; Serano, J. M.; Pavlopoulos, A.; Kontarakis, Z.; Protas, M. E.; Kwan, E.; Chatterjee, S.; Tran, K. D.; Averof, M.; Patel, N. H.; et al. Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proc. Natl. Acad. Sci. USA 2009, 106, 13892-13896.
32. Kato, Y.; Shiga, Y.; Kobayashi, K.; Tokishita, S.-I.; Yamagata, H.; Iguchi, T.; Watanabe, H. Development of an RNA interference method in the cladoceran crustacean Daphnia magna. Dev. Genes Evol. 2011, 220, 337-345.
33. Ventura, T.; Manor, R.; Aflalo, E. D.; Chalifa-Caspi, V.; Weil, S.; Sharabi, O.; Sagi, A. Post-Embryonic transcriptomes of the prawn Macrobrachium rosenbergii: Multigenic succession through metamorphosis. PLoS One 2013, 8, e55322.
34. Laufer, H.; Borst, D.; Baker, F. C.; Reuter, C. C.; Tsai, L. W.; Schooley, D. A.; Carrasco, C.; Sinkus, M. Identification of a juvenile hormone-like compound in a crustacean. Science 1987, 235, 202-205.
35. Hui, J. H. L.; Tobe, S. S.; Chan, S.-M. Characterization of the putative farnesoic acid O-methyltransferase (LvFAMeT) cDNA from white shrimp, Litopenaeus vannamei: Evidence for its role in molting. Peptides 2008, 29, 252-260.
36. Sonanez-Organis, J. G.; Peregrino-Uriarte, A. B.; Gomez-Jimenez, S.; Lopez-Zavala, A.; Forman, H. J.; Yepiz-Plascencia, G. Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp. Biochem. Phys. C 2009, 150, 395-405.
37. Soñanez-Organis, J. G.; Racotta, I. S.; Yepiz-Plascencia, G. Silencing of the hypoxia inducible factor 1-HIF-1-obliterates the effects of hypoxia on glucose and lactate concentrations in a tissue-specific manner in the shrimp Litopenaeus vannamei. J. Exp. Mar. Biol. Ecol. 2010, 393, 51-58.
38. De Santis, C.; Wade, N. M.; Jerry, D. R.; Preston, N. P.; Glencross, B. D.; Sellars, M. J. Growing backwards: An inverted role for the shrimp ortholog of vertebrate myostatin and GDF11. J. Exp. Biol. 2011, 214, 2671-2677.
39. Hermann, A.; Cox, J. A. Sarcoplasmic calcium-binding protein. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1995, 111, 337-345.
40. White, A. J.; Northcutt, M. J.; Rohrback, S. E.; Carpenter, R. O.; Niehaus-Sauter, M. M.; Gao, Y. P.; Wheatly, M. G.; Gillen, C. M. Characterization of sarcoplasmic calcium binding protein (SCP) variants from freshwater crayfish Procambarus clarkii. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2011, 160, 8-14.
41. Keller, R. Crustacean neuropeptides: Structures, functions and comparative aspects. Experientia 1992, 48, 439-448.
42. Webster, S. G. Measurement of crustacean hyperglycaemic hormone levels in the edible crab Cancer pagurus during emersion stress. J. Exp. Biol. 1996, 199, 1579-1585.
43. Lugo, J. M.; Morera, Y.; Rodríguez, T.; Huberman, A.; Ramos, L.; Estrada, M. P. Molecular cloning and characterization of the crustacean hyperglycemic hormone cDNA from Litopenaeus schmitti. FEBS J. 2006, 273, 5669-5677.
44. Tiu, S. H.-K.; Chan, S.-M. The use of recombinant protein and RNA interference approaches to study the reproductive functions of a gonad-stimulating hormone from the shrimp Metapenaeus ensis. FEBS J. 2007, 274, 4385-4395.
45. Webster, S. G.; Keller, R.; Dircksen, H. The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen. Comp. Endocrinol. 2012, 175, 217-233.
46. Pamuru, R. R.; Rosen, O.; Manor, R.; Chung, J. S.; Zmora, N.; Glazer, L.; Aflalo, E. D.; Weil, S.; Tamone, S. L.; Sagi, A. Stimulation of molt by RNA interference of the molt-inhibiting hormone in the crayfish Cherax quadricarinatus. Gen. Comp. Endocrinol. 2012, 178, 227-236.
47. Tiu, S. H. K.; He, J.-G.; Chan, S.-M. The LvCHH-ITP gene of the shrimp (Litopenaeus vannamei) produces a widely expressed putative ion transport peptide (LvITP) for osmo-regulation. Gene 2007, 396, 226-235.
48. Treerattrakool, S.; Panyim, S.; Chan, S.-M.; Withyachumnarnkul, B.; Udomkit, A. Molecular characterization of gonad-inhibiting hormone of Penaeus monodon and elucidation of its inhibitory role in vitellogenin expression by RNA interference. FEBS J. 2008, 275, 970-980.
49. Treerattrakool, S.; Panyim, S.; Udomkit, A. Induction of ovarian maturation and spawning in Penaeus monodon broodstock by double-stranded RNA. Mar. Biotechnol. 2011, 13, 163-169.
50. Treerattrakool, S.; Chartthai, C.; Phrommain, N.; Panyim, S.; Udomkit, A. Silencing of gonad-inhibiting hormone gene expression in Penaeus monodon by feeding with GIH dsRNA enriched Artemia. Aquaculture 2013, 404, 116-121.
51. Sathapondecha, P.; Treerattrakool, S.; Panyim, S.; Udomkit, A. Potential roles of transglutaminase and thioredoxin in the release of gonad-stimulating factor in Penaeus monodon: Implication from differential expression in the brain during ovarian maturation cycle. Mar. Genom. 2011, 4, 279-285.
52. Sharabi, O.; Ventura, T.; Manor, R.; Aflalo, E. D.; Sagi, A. Epidermal growth factor receptor in the prawn Macrobrachium rosenbergii: Function and putative signaling cascade. Endocrinology 2013, 154, 3188-3196.
53. Tiu, S. H. K.; Benzie, J.; Chan, S.-M. From hepatopancreas to ovary: Molecular characterization of a shrimp vitellogenin receptor involved in the processing of vitellogenin. Biol. Reprod. 2008, 79, 66-74.
54. Das, S.; Durica, D. S. Ecdysteroid receptor signaling disruption obstructs blastemal cell proliferation during limb regeneration in the fiddler crab, Uca pugilator. Mol. Cell. Endocrinol. 2013, 365, 249-259.
55. Priya, T. A. J.; Li, F.; Zhang, J.; Wang, B.; Zhao, C.; Xiang, J. Molecular characterization and effect of RNA interference of retinoid X receptor (RXR) on E75 and chitinase gene expression in Chinese shrimp Fenneropenaeus chinensis. Comp. Biochem. Physiol. Part. B Biochem. Mol. Biol. 2009, 153, 121-129.
56. Freeman, M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 1996, 87, 651-660.
57. Kono, M.; Wilder, M. N.; Matsui, T.; Furukawa, K.; Koga, D.; Aida, K. Chitinolytic enzyme activities in the hepatopancreas, tail fan and hemolymph of kuruma prawn Penaeus Japonicus during the molt cycle. Fish. Sci. 1995, 61, 727-728.
58. Priya, T. A. J.; Li, F.; Zhang, J.; Yang, C.; Xiang, J. Molecular characterization of an ecdysone inducible gene E75 of Chinese shrimp Fenneropenaeus chinensis and elucidation of its role in molting by RNA interference. Comp. Biochem. Physiol. Part. B Biochem. Mol. Biol. 2010, 156, 149-157.
59. Nagaraju, G. P. C.; Rajitha, B.; Borst, D. W. Molecular cloning and sequence of retinoid X receptor in the green crab Carcinus maenas: A possible role in female reproduction. J. Endocrinol. 2011, 210, 379-390.
60. Kato, Y.; Kobayashi, K.; Watanabe, H.; Iguchi, T. Environmental sex determination in the branchiopod crustacean Daphnia magna: Deep conservation of a Doublesex gene in the sex-determining pathway. PLoS Genet. 2011, 7, e1001345.
61. Charniaux-Cotton, H. Androgenic gland of crustaceans. Gen. Comp. Endocrinol. 1962, 1, 241-247.
62. Rosen, O.; Manor, R.; Weil, S.; Gafni, O.; Linial, A.; Aflalo, E. D.; Ventura, T.; Sagi, A. A sexual shift induced by silencing of a single insulin-like gene in crayfish: Ovarian upregulation and testicular degeneration. PLoS One 2010, 5, e15281.
63. Ventura, T.; Manor, R.; Aflalo, E. D.; Weil, S.; Raviv, S.; Glazer, L.; Sagi, A. Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 2009, 150, 1278-1286.
64. Ventura, T.; Manor, R.; Aflalo, E. D.; Weil, S.; Rosen, O.; Sagi, A. Timing sexual differentiation: Full functional sex reversal achieved through silencing of a single insulin-like gene in the prawn, Macrobrachium rosenbergii. Biol. Reprod. 2012, 86, 90-96.
65. Chen, Y. H.; Jia, X. T.; Zhao, L.; Li, C. Z.; Zhang, S. A.; Chen, Y. G.; Weng, S. P.; He, J. G. Identification and functional characterization of Dicer2 and five single VWC domain proteins of Litopenaeus vannamei. Dev. Comp. Immunol. 2011, 35, 661-671.
66. Dechklar, M.; Udomkit, A.; Panyim, S. Characterization of Argonaute cDNA from Penaeus monodon and implication of its role in RNA interference. Biochem. Biophys. Res. Commun. 2008, 367, 768-774.
67. Labreuche, Y.; Veloso, A.; de la Vega, E.; Gross, P. S.; Chapman, R. W.; Browdy, C. L.; Warr, G. W. Non-Specific activation of antiviral immunity and induction of RNA interference may engage the same pathway in the Pacific white leg shrimp Litopenaeus vannamei. Dev. Comp. Immunol. 2010, 34, 1209-1218.
68. Su, J. S.; Oanh, D. T. H.; Lyons, R. E.; Leeton, L.; van Hulten, M. C. W.; Tan, S. H.; Song, L.; Rajendran, K. V.; Walker, P. J. A key gene of the RNA interference pathway in the black tiger shrimp, Penaeus monodon: Identification and functional characterisation of Dicer-1. Fish. Shellfish Immunol. 2008, 24, 223-233.
69. Wang, S.; Chen, A. J.; Shi, L. J.; Zhao, X. F.; Wang, J. X. TRBP and eIF6 homologue in Marsupenaeus japonicus play crucial roles in antiviral response. PLoS One 2012, 7, e30057.
70. Yao, X. M.; Wang, L. L.; Song, L. S.; Zhang, H. A.; Dong, C. H.; Zhang, Y.; Qiu, L. M.; Shi, Y. H.; Jianmin, Z. M.; Bi, Y. K. A Dicer-1 gene from white shrimp Litopenaeus vannamei: Expression pattern in the processes of immune response and larval development. Fish. Shellfish Immunol. 2010, 29, 565-570.
71. Shabalina S. A.; Koonin E. V. Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 2008, 23, 578-587.
72. Stentiford, G. D.; Bonami, J. R.; Alday-Sanz, V. A critical review of susceptibility of crustaceans to Taura syndrome, Yellowhead disease and White Spot Disease and implications of inclusion of these diseases in European legislation. Aquaculture 2009, 291, 1-17.
73. Hirono, I.; Fagutao, F. F.; Kondo, H.; Aoki, T. Uncovering the mechanisms of shrimp innate immune response by RNA interference. Mar. Biotechnol. 2011, 13, 622-628.
74. La Fauce, K.; Owens, L. RNA interference with special reference to combating viruses of crustacea. Indian J. Virol. 2012, 23, 226-243.
75. Heinrichs, A. RISC assessment. Nat. Rev. Mol. Cell. Biol. 2004, 5, 334.
76. De la Vega, E.; O'Leary, N. A.; Shockey, J. E.; Robalino, J.; Payne, C.; Browdy, C. L.; Warr, G. W.; Gross, P. S. Anti-Lipopolysaccharide factor in Litopenaeus vannamei (LvALF): A broad spectrum antimicrobial peptide essential for shrimp immunity against bacterial and fungal infection. Mol. Immunol. 2008, 45, 1916-1925.
77. Shockey, J. E.; O'Leary, N. A.; de la Vega, E.; Browdy, C. L.; Baatz, J. E.; Gross, P. S. The role of crustins in Litopenaeus vannamei in response to infection with shrimp pathogens: An in vivo approach. Dev. Comp. Immunol. 2009, 33, 668-673.
78. Woramongkolchai, N.; Supungul, P.; Tassanakajon, A. The possible role of penaeidin5 from the black tiger shrimp, Penaeus monodon, in protection against viral infection. Dev. Comp. Immunol. 2011, 35, 530-536.
79. Vazquez, L.; Alpuche, J.; Maldonado, G.; Agundis, C.; Pereyra-Morales, A.; Zenteno, E. Review: Immunity mechanisms in crustaceans. Innate Immun. 2009, 15, 179-188.
80. Maningas, M. B. B.; Kondo, H.; Hirono, I.; Saito-Taki, T.; Aoki, T. Essential function of transglutaminase and clotting protein in shrimp immunity. Mol. Immunol. 2008, 45, 1269-1275.
81. Portera, A. G.; Jänicke, R. U. Emerging roles of caspase-3 in apoptosis. Cell. Death Differ. 1999, 6, 99-104.
82. Wang, L.; Zhi, B.; Wu, W.; Zhang, X. Requirement for shrimp caspase in apoptosis against virus infection. Dev. Comp. Immunol. 2008, 32, 706-715.
83. Rijiravanich, A.; Browdy, C. L.; Withyachumnarnkul, B. Knocking down caspase-3 by RNAi reduces mortality in Pacific white shrimp Penaeus (Litopenaeus) vannamei challenged with a low dose of white-spot syndrome virus. Fish. Shellfish Immunol. 2008, 24, 308-313.
84. Lin, Y.-C.; Chen, J.-C.; Chen, Y.-Y.; Liu, C.-H.; Cheng, W.; Hsu, C.-H.; Tsui, W.-C. Characterization of white shrimp Litopenaeus vannamei integrin β and its role in immunomodulation by dsRNA-mediated gene silencing. Dev. Comp. Immunol. 2013, 40, 167-179.
85. Zong, R.; Wu, W.; Xu, J.; Zhang, X. Regulation of phagocytosis against bacterium by Rab GTPase in shrimp Marsupenaeus japonicus. Fish. Shellfish Immunol. 2008, 25, 258-263.
86. Wu, W.; Zong, R.; Xu, J.; Zhang, X. Antiviral phagocytosis is regulated by a novel Rab-dependent complex in shrimp Penaeus japonicus. J. Proteome Res. 2007, 7, 424-431.
87. Ongvarrasopone, C.; Chanasakulniyom, M.; Sritunyalucksana, K.; Panyim, S. Suppression of PmRab7 by dsRNA inhibits WSSV or YHV infection in shrimp. Mar. Biotechnol. 2008, 10, 374-381.
88. Assavalapsakul, W.; Smith, D. R.; Panyim, S. Identification and characterization of a Penaeus monodon lymphoid cell-expressed receptor for the yellow head virus. J. Virol. 2006, 80, 262-269.
89. Johansson, M. W.; Soderhall, K. Cellular immunity in crustaceans and the proPO system. Parasitol. Today 1989, 5, 171-176.
90. Fagutao, F. F.; Koyama, T.; Kaizu, A.; Saito-Taki, T.; Kondo, H.; Aoki, T.; Hirono, I. Increased bacterial load in shrimp hemolymph in the absence of prophenoloxidase. FEBS J. 2009, 276, 5298-5306.
91. Amparyup, P.; Charoensapsri, W.; Tassanakajon, A. Two prophenoloxidases are important for the survival of Vibrio harveyi challenged shrimp Penaeus monodon. Dev. Comp. Immunol. 2009, 33, 247-256.
92. Liu, H.; Jiravanichpaisal, P.; Cerenius, L.; Lee, B. L.; Söderhäll, I.; Söderhäll, K. Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. J. Biol. Chem. 2007, 282, 33593-33598.
93. Xu, J.; Wu, S.; Zhang, X. Novel function of QM protein of shrimp (Penaeus japonicus) in regulation of phenol oxidase activity by interaction with hemocyanin. Cell. Physiol. Biochem. 2008, 21, 473-480.
94. Li, D.-F.; Zhang, M.-C.; Yang, H.-J.; Zhu, Y.-B.; Xu, X. β-Integrin mediates WSSV infection. Virology 2007, 368, 122-132.
95. Musthaq, S. S.; Kwang, J. Oral vaccination of baculovirus-expressed VP28 displays enhanced protection against white spot syndrome virus in Penaeus monodon. PLoS One 2011, 6, e26428.
96. Rajeshkumar, S.; Venkatesan, C.; Sarathi, M.; Sarathbabu, V.; Thomas, J.; Anver Basha, K.; Sahul Hameed, A. S. Oral delivery of DNA construct using chitosan nanoparticles to protect the shrimp from white spot syndrome virus (WSSV). Fish. Shellfish Immunol. 2009, 26, 429-437.
97. Sarathi, M.; Simon, M. C.; Venkatesan, C.; Hameed, A. S. S. Oral administration of bacterially expressed VP28dsRNA to protect Penaeus monodon from white spot syndrome virus. Mar. Biotechnol. 2008, 10, 242-249.
98. Anas, A.; Philip, R.; Singh, I. S. B. Chitosan as a wall material for a microencapsulated delivery system for Macrobrachium rosenbergii (de Man) larvae. Aquac. Res. 2008, 39, 885-890.
99. Sellars, M. J.; Rao, M.; Arnold, S. J.; Wade, N. M.; Cowley, J. A. Penaeus monodon is protected against gill-associated virus by muscle injection but not oral delivery of bacterially expressed dsRNAs. Dis. Aquat. Org. 2011, 95, 19-30.
100. Xu, J.; Han, F.; Zhang, X. Silencing shrimp white spot syndrome virus (WSSV) genes by siRNA. Antivir. Res. 2007, 73, 126-131.
101. Westenberg, M.; Heinhuis, B.; Zuidema, D.; Vlak, J. M. siRNA injection induces sequence-independent protection in Penaeus monodon against white spot syndrome virus. Virus Res. 2005, 114, 133-139.
102. Hartnoll, R. G. Growth. The Biology of Crustacea; Bliss, D. E., Ed.; Academic Press: New York, NY, USA, 1982; pp. 111-197.
103. Botsford, L. W. Models of Growth. In Crustacean Issues: Factors in Adult Growth; Wenner, A. M., Balkema, A. A., Eds.; A. A. Balkema Publishers: Boston, MA, USA, 1985; Volume 3, pp. 171-188.
104. Aiken, D. E.; Waddy, S. L. The growth-process in crayfish. Rev. Aquat. Sci. 1992, 6, 335-381.
105. Curtis, M. C.; Jones, C. M. Observations on monosex culture of redclaw crayfish Cherax quadricarinatus von Martens (Decapoda: Parastacidae) in earthen ponds. J. World Aquac. Soc. 1995, 26, 154-159.
106. Sagi, A.; Milstein, A.; Eran, Y.; Joseph, D.; Khalaila, I.; Abdu, U.; Harpaz, S.; Karplus, I. Culture of the Australian redclaw crayfish (Cherax quadricarinatus) in Israel, II. second growout season of overwintered populations. Isr. J. Aquac. Bamidgeh 1997, 49, 222-229.
107. Kuris, A. M.; Ra'anan, Z.; Sagi, A.; Cohen, D. Morphotypic differentiation of male Malaysian giant prawn, Macrobrachium rosenbergii. J. Crustac. Biol. 1987, 7, 219-237.
108. Sagi, A.; Ra'anan, Z.; Cohen, D.; Wax, Y. Production of Macrobrachium rosenbergii in monosex population: Yield characteristics under intensive monoculture conditions in cages. Aquaculture 1986, 51, 265-275.
109. Nair, C. M.; Salin, K. R.; Raju, M. S.; Sebastian, M. Economic analysis of monosex culture of giant freshwater prawn (Macrobrachium rosenbergii de Man): A case study. Aquac. Res. 2006, 37, 949-954.
110. Sagi, A.; Aflalo, E. D. The androgenic gland and monosex culture in prawns-A biotechnological perspective. Aquac. Res. 2005, 36, 231-237.
111. Charniaux-Cotton, H. Decouverte chez un Crustace Amphipode (Orchestia gammarella) d'une glande endocrine responsible de la differenciation des caracteres sexuels primaires et secondaires males. C. R. Acad. Sci. Paris 1954, 239, 780-782.
112. Okumura, T.; Hara, M. Androgenic gland cell structure and spermatogenesis during the molt cycle and correlation to morphotypic differentiation in the giant freshwater prawn, Macrobrachium rosenbergii. Zool. Sci. 2004, 21, 621-628.
113. Sagi, A.; Cohen, D. Growth, maturation and progeny of sex-reversed Macrobrachium rosenbergii males. World Aquac. 1990, 21, 87-90.
114. Sagi, A.; Snir, E.; Khalaila, I. Sexual differentiation in decapod crustaceans: Role of the androgenic gland. Invertebr. Reprod. Dev. 1997, 31, 55-61.
115. Touir, A. Donnees nouvelles concernant l'endocrinologie sexuelle des Crustaces Decapodes Natantia hermaphrodites et gonochoriques. II. Maintien des gonies et evolution des gametogeneses in vivo et in vitro. C. R. Acad. Sci. 1977, 284, 2515-2518.
116. Taketomi, Y.; Murata, M.; Miyawaki, M. Androgenic gland and secondary sexual characters in the crayfish Procambarus clarkii. J. Crustac. Biol. 1990, 10, 492-497.
117. Manor, R.; Aflalo, E. D.; Segall, C.; Weil, S.; Azulay, D.; Ventura, T.; Sagi, A. Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebr. Reprod. Dev. 2004, 45, 151-159.
118. Cui, Z. X.; Liu, H.; Lo, T. S.; Chu, K. H. Inhibitory effects of the androgenic gland on ovarian development in the mud crab Scylla paramamosain. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2005, 140, 343-348.
119. King, D. S. Fine structure of the androgenic gland of the crab, Pachygrapsus crassipes. Gen. Comp. Endocrinol. 1964, 4, 533-544.
120. Awari, S. A.; Kiran, D. Histological and histochemical study of androgenic gland of Macrobrachium rosenbergii (de Man). J. Aquac. Trop. 1999, 14, 101-112.
121. Sun, P. S.; Weatherby, T. M.; Dunlap, M. F.; Arakaki, K. L.; Zacarias, D. T.; Malecha, S. R. Developmental changes in structure and polypeptide profile of the androgenic gland of the freshwater prawn Macrobrachium rosenbergii. Aquac. Int. 2000, 8, 327-334.
122. Martin, G.; Sorokine, O.; Moniatte, M.; Bulet, P.; Hetru, C.; van Dorsselaer, A. The structure of a glycosylated protein hormone responsible for sex determination in the isopod, Armadillidium vulgare. Eur. J. Biochem. 1999, 262, 727-736.
123. Okuno, A.; Hasegawa, Y.; Ohira, T.; Katakura, Y.; Nagasawa, H. Characterization and cDNA cloning of androgenic gland hormone of the terrestrial isopod Armadillidium vulgare. Biochem. Biophys. Res. Commun. 1999, 264, 419-423.
124. Manor, R.; Weil, S.; Oren, S.; Glazer, L.; Aflalo, E. D.; Ventura, T.; Chalifa-Caspi, V.; Lapidot, M.; Sagi, A. Insulin and gender: An insulin-like gene expressed exclusively in the androgenic gland of the male crayfish. Gen. Comp. Endocrinol. 2007, 150, 326-336.
125. Chung, J. S.; Manor, R.; Sagi, A. Cloning of an insulin-like androgenic gland factor (IAG) from the blue crab, Callinectes sapidus: Implications for eyestalk regulation of IAG expression. Gen. Comp. Endocrinol. 2011, 173, 4-10.
126. Mareddy, V. R.; Rosen, O.; Thaggard, H. B.; Manor, R.; Kuballa, A. V.; Aflalo, E. D.; Sagi, A.; Paterson, B.; Elizur, A. Isolation and characterization of the complete cDNA sequence encoding a putative insulin-like peptide from the androgenic gland of Penaeus monodon. Aquaculture 2011, 318, 364-370.
127. Ventura, T.; Aflalo, E. D.; Weil, S.; Kashkush, K.; Sagi, A. Isolation and characterization of a female-specific DNA marker in the giant freshwater prawn Macrobrachium rosenbergii. Heredity 2011, 107, 456-461.
128. Stein, A. J.; Rodriguez-Cerezo, E. International trade and the global pipeline of new GM crops. Nat. Biotechnol. 2010, 28, 23-25.