Insight into the lymphoid organ of penaeid prawns: A review

Fish and Shellfish Immunology

Volumn 29, Issue 3, 2010, Pages 367-377

  Rusaini, ^a,b   Owens, L ^b  

^a TADULAKO UNIVERSITY   (Indonesia)

^b JAMES COOK UNIVERSITY   (Australia)

Author keywords

Crustacea; Haemocytes; Lymphoid organ; Spheroid cells; Viral diseases

Indexed keywords

ASTACOIDEA; CRUSTACEA; DECAPODA (CRUSTACEA); LOBSTER; PENAEIDAE;

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL STRUCTURES; CYTOLOGY; IMMUNOLOGY; PENAEIDAE; VIROLOGY; VIRUS;

ANIMAL STRUCTURES; ANIMALS; PENAEIDAE; VIRUSES;

EID: 77954533646     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2010.05.011     Document Type: Review

References (97)

1. Smith V.J., Brown J.H., Hauton C. Immunostimulation in crustaceans: does it really protect against infection?. Fish Shellfish Immunol 2003, 15:71-90.
2. Flegel T.W., Lightner D.V., Lo C.F., Owens L. Shrimp diseases control: past, present and future. Diseases in Asian aquaculture 2008, 355-378. Fish Health Section, Asian Fisheries Society, Manila. M.G. Bondad-Reantaso, C.V. Mohan, M. Crumlish, R.P. Subasinghe (Eds.).
3. Loker E.S., Adema C.M., Zhang S.-M., Kepler T.B. Invertebrate immune system - not homogeneous, not simple, not well understood. Immunol Rev 2004, 198:10-24.
4. Bachere E. Anti-infectious immune effectors in marine invertebrate: potential tools for disease control in larviculture. Aquaculture 2003, 237:427-438.
5. Roch P. Defense mechanism and disease prevention in farmed marine invertebrate. Aquaculture 1999, 172:125-145.
6. Rodriguez J., Le Moullac G. State of the art of immunological tools and health control of penaeid shrimp. Aquaculture 2000, 191:109-119.
7. Soderhall K., Cerenius L. Crustacean immunity. Ann Rev Fish Dis 1992, 3-23.
8. Anggraeni M.S., Owens L. The haemocytic origin of lymphoid organ spheroid cells in the penaeid prawn Penaeus monodon. Dis Aquat Org 2000, 40:85-92.
9. Hasson K.W., Lightner D.V., Mohney L.L., Redman R.M., White B.M. Role of lymphoid organ spheroids in chronic Taura syndrome virus (TSV) infections in Penaeus vannamei. Dis Aquat Org 1999, 38:93-105.
10. Kondo M., Itami T., Takahashi Y., Fujii R., Tomonaga S. Structure and function of the lymphoid organ in the kuruma prawn. Dev Comp Immunol 1994, 18(Suppl. 1):S109.
11. Martin G.G., Hose J.E., Minka G., Rosenberg S. Clearance of bacteria injected into the hemolymph of the ridgeback prawn, Sicyonia ingentis (Crustacea: Decapoda): role of hematopoietic tissue. J Morphol 1996, 227:227-233.
12. van de Braak C.B.T., Botterblom M.H.A., Taverne N., van Muiswinkel W.B., Rombout J.H.W.M., van der Knaap W.P.W. The roles of haemocytes and the lymphoid organ in the clearance of injected Vibrio bacteria in Penaeus monodon shrimp. Fish Shellfish Immunol 2002, 13:293-309.
13. Nakamura K. Lymphoid organ and its developmental property of larval prawn Penaeus japonicus. Mem Fac Fish, Kagoshima University 1987, 36:215-220.
14. Duangsuwan P., Phoungpetchara I., Tinikul Y., Poljaroen J., Wanichanon C., Sobhon P. Histological and three dimensional organizations of lymphoid tubules in normal lymphoid organ of Penaeus monodon. Fish Shellfish Immunol 2008, 24:426-435.
15. Burgents J.E., Burnett L.E., Stabb E.V., Burnett K.G. Localization and bacteriostasis of Vibrio introduced into the Pacific white shrimp, Litopenaeus vannamei. Dev Comp Immunol 2005, 29:681-691.
16. Oka M. Studies on Penaeus orientalis KISHINOUYE-VIII structure of the newly found lymphoid organ. Bull Jpn Soc Sci Fish 1969, 35:245-250.
17. Hose J.E., Martin G.G., Tiu S., McKrell N. Patterns of hemocyte production and release throughout the molt cycle in the penaeid shrimp Sicyonia ingentis. Biol Bull 1992, 183:185-199.
18. Martin G.G., Hose J.E., Kim J.J. Structure of hematopoietic nodules in the ridgeback prawn, Sicyonia ingentis: light and electron microscopic observations. J Morphol 1987, 192:193-204.
19. Lightner D.V., Hendrick R.P., Freyer J.L., Chen S.N., Liao I.C., Kou G.H. A survey of cultured penaeid shrimp in Taiwan for viral and other important diseases. Fish Pathol 1987, 22:127-140.
20. Lu Y., Tapay L.M., Loh P.C., Brock J.A., Gose R.B. Distribution of yellow-head virus in selected tissues and organs of penaeid shrimp Penaeus vannamei. Dis Aquat Org 1995, 23:67-70.
21. Nadala E.C.B., Lu Y., Loh P.C., Brock J.A. Infection of Penaeus stylirostris (Boone) with a rhabdovirus isolated from Penaeus spp. Gyobyo Kenkyu 1992, 27:143-147.
22. Lightner D.V., Brock J.A. A lymphoma-like neoplasm arising from hematopoietic tissue in the white shrimp, Penaeus vannamei Boone (Crustacea: Decapoda). J Invertebr Pathol 1987, 49:188-193.
23. Rusaini The lymphoid organ in penaeids and its interaction with moulting 2006, Microbiology and Immunology, JamesCook University, Townsville, pp. 193.
24. Bell T.A., Lightner D.V. A handbook of normal penaeid shrimp histology. Baton Rauge, La World Aquacult Soc 1988, 52-73.
25. Shao M.Y., Zhang Z.F., Kang K.H., Chen Z.T., Kim J.M. The study on the cytology and histochemistry of lymphoid organ spheroids in Penaeus chinensis. Aquaculture 2004, 240:463-471.
26. Cowley J.A., McCulloch R.J., Rajendran K.V., Cadogan L.C., Spann K.M., Walker P.J. RT-nested PCR detection of Mourilyan virus in Australian Penaeus monodon and its tissue distribution in healthy and moribund prawns. Dis Aquat Org 2005, 66:91-104.
27. Rajendran K.V., Cowley J.A., McCulloch R.J., Walker P.J. A TaqMan real-time RT-PCR for quantifying Mourilyan virus infection levels in penaeid shrimp tissues. J Virol Methods 2006, 137:265-271.
28. Pongsomboon S., Wongpanya R., Tang S., Chalorsrikul A., Tassanakajon A. Abundantly expressed transcripts in the lymphoid organ of the black tiger shrimp, Penaeus monodon, and their implication in immune function. Fish Shellfish Immunol 2008, 25:485-493.
29. van de Braak C.B.T., Botterblom M.H.A., Liu W., Taverne N., van der Knaap W.P.W., Rombout J.H.W.M. The role of the haematopoietic tissue in haemocyte production and maturation in the black tiger shrimp (Penaeus monodon). Fish Shellfish Immunol 2002, 12:253-272.
30. Fraser C.A., Owens L. Spawner-isolated mortality virus from Australian Penaeus monodon. Dis Aquat Org 1996, 27:141-148.
31. Owens L., Beer S.D., Smith J. Lymphoidal parvovirus-like particles in Australian penaeid prawns. Dis Aquat Org 1991, 11:129-134.
32. Turnbull J.F., Larkins P.E., McPadden C., Matondang R. A histopathological disease survey of cultured shrimp in North East Sumatera. Indonesia J Fish Dis 1994, 17:57-65.
33. Bonami J.R., Lightner D.V., Redman R.M., Poulos B.T. Partial characterisation of a togavirus (LOVV) associated with histopathological changes of the lymphoid organ of penaeid shrimps. Dis Aquat Org 1992, 14:145-152.
34. Hasson K.W., Lightner D.V., Poulos B.T., Redman R.M., White B.L., Brock J.A., et al. Taura syndrome in Penaeus vannamei: demonstration of a viral etiology. Dis Aquat Org 1995, 23:115-126.
35. Anantasomboon G., Sriurairatana S., Flegel T.W., Withyachumnarnkul B. Unique lesions and viral-like particles found in growth retarded black tiger shrimp Penaeus monodon from East Africa. Aquaculture 2006, 253:197-203.
36. Anantasomboon G., Poonkhum R., Sittidilokratna N., Flegel T.W., Withyachumnarnkul B. Low viral loads and lymphoid organ spheroids are associated with yellow head virus (YHV) tolerance in whiteleg shrimp Penaeus vannamei. Dev Comp Immunol 2008, 32:613-626.
37. Rodríguez J., Bayot B., Amano Y., Panchana F., Blas Id, Alday V., et al. White spot syndrome virus infection in cultured Penaeus vannamei (Boone) in Ecuador with emphasis on histopathology and ultrastructure. J Fish Dis 2003, 26:439-450.
38. Alday-Sanz V., Roque A., Turnbull J.F. Clearing mechanisms of Vibrio vulnificus biotype I in the black tiger shrimp Penaeus monodon. Dis Aquat Org 2002, 48:91-99.
39. Anggraeni M.S. The origin and the role of lymphoid organ spheroid cells in the giant tiger prawn, Penaeus monodon 1998, Microbiology and Immunology, JamesCook University, Townsville, pp. 120.
40. Egusa S., Takahashi Y., Itami T., Momoyama K. Histopathology of vibriosis in the kuruma prawn Penaeus japonicus Bate. Fish Pathol 1988, 23:59-65.
41. Jiravanichpaisal P., Miyazaki T. Histopathology, biochemistry, and pathogenicity of Vibrio harveyi infecting black tiger prawn Penaeus monodon. J Aquat Anim Health 1994, 6:27-35.
42. de la Vega E., O'Leary N.A., Shockey J.E., Robalino J., Payne C., Browdy C.L., et al. 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.
43. Soowannayan C., Sithigorngul P., Flegel T.W. use of a specific monoclonal antibody to determine tissue tropism of yellow head virus (YHV) of Penaeus monodon by in situ immunocytochemistry. Fish Sci 2002, 68(Suppl. 1):805-809.
44. Bourchookarn A., Havanapan P.-O., Thongboonkerd V., Krittanai C. Proteomic analysis of altered proteins in lymphoid organ of yellow head virus infected Penaeus monodon. Biochim Biophys Acta 2008, 1784:504-511.
45. Spann K.M., Vickers J.E., Lester R.J.G. Lymphoid organ virus of Penaeus monodon from Australia. Dis Aquat Org 1995, 23:127-134.
46. Spann K.M., Cowley J.A., Walker P.J., Lester R.J.G. A yellow-head-like virus from Penaeus monodon cultured in Australia. Dis Aquat Org 1997, 31:169-179.
47. Wu J.L., Muroga K. Apoptosis does not play an important role in the resistance of 'immune' Penaeus japonicus against white spot syndrome virus. J Fish Dis 2004, 27:15-21.
48. Soowannayan C., Flegel T.W., Sithigorngul P., Slater J., Hyatt A., Cramerri S., et al. Detection and differentiation of yellow head complex viruses using monoclonal antibodies. Dis Aquat Org 2003, 57:193-200.
49. Chantanachookin C., Boonyaratpalin S., Kasornchandra J., Direkbusarakom S., Ekpanithanpong U., Supamataya K., et al. Histology and ultrastructure reveal a new granulosis-like virus in Penaeus monodon affected by yellow-head disease. Dis Aquat Org 1993, 17:145-157.
50. Wang C.S., Tang K.F.J., Kou G.H., Chen S.N. Light and electron microscopic evidence of white spot disease in the giant tiger shrimp, Penaeus monodon (Fabricius), and the kuruma shrimp, Penaeus japonicus (Bate), cultured in Taiwan. J Fish Dis 1997, 20:323-331.
51. Park J.H., Lee Y.S., Lee S., Lee Y. An infectious viral disease of penaeid shrimp newly found in Korea. Dis Aquat Org 1998, 34:71-75.
52. Sritunyalucksana K., Apisawetakan S., Boon-nat A., Withyachumnarnkul B., Flegel T.W. A new RNA virus found in black tiger shrimp Penaeus monodon from Thailand. Virus Res 2006, 118:31-38.
53. Andrade T.P.D., Redman R.M., Lightner D.V. Evaluation of the preservation of shrimp samples with Davidson's AFA fixative for infectious myonecrosis virus (IMNV) in situ hybridization. Aquaculture 2008, 278:179-183.
54. Tang K.F.J., Pantoja C.J., Poulos B.T., Redman R.M., Lightner D.V. In situ hybridization demonstrates that Litopenaeus vannamei, L. stylirostris and Penaeus monodon are susceptible to experimental infection with infectious myonecrosis virus (IMNV). Dis Aquat Org 2005, 63:261-265.
55. Hasson K.W., Lightner D.V., Mohney L.L., Redman R.M., Poulos B.T., White B.M. Taura syndrome virus (TSV) lesion development and the disease cycle in the Pacific white shrimp Penaeus vannamei. Dis Aquat Org 1999, 36:81-93.
56. Spann K.M., McCulloch R.J., Cowley J.A., East I.J., Walker P.J. Detection of gill-associated virus (GAV) by in situ hybridization during acute and chronic infections of Penaeus monodon and P. esculentus. Dis Aquat Org 2003, 56:1-10.
57. Rusaini, Owens L. Effect of moulting and lunar rhythms on the lymphoid organ spheroid (LOS) cells of the black tiger prawn (Penaeus monodon). J Exp Mar Biol Ecol 2010, 389:6-12.
58. Duangsuwan P., Tinikul Y., Chotwiwatthanakun C., Vanichviriyakit R., Sobhon P. Changes in the histological organization and spheroid formation in lymphoid organ of Penaeus monodon infected with yellow head virus. Fish Shellfish Immunol 2008, 25:560-569.
59. Littik S.A.M. Quantitative histopathology and epidemiology of prawn viral diseases 2003, Microbiology and Immunology, JamesCook University, Townsville, pp. 187.
60. Verli F.D., Rossi-Schneider T.R., Schneider F.L., Yurgel L.S., de Souza M.A.L. Vascular corrosion casting technique steps. Scanning 2007, 29:128-132.
61. Hossler F.E. Vascular corrosion casting. Microsc Microanal 2003, 9:1578-1579.
62. Cheng W., Chen J.C. Effect of intrinsic and extrinsic factors on the haemocyte profile of the prawn, Macrobrachium rosenbergii. Fish Shellfish Immunol 2001, 11:53-63.
63. Le Moullac G., Le Groumellec M., Ansquer D., Froissard S., Levy P. Aquacop. Haematological and phenoloxidase activity changes in the shrimp Penaeus stylirostris in relation with the moult cycle: protection against vibriosis. Fish Shellfish Immunol 1997, 7:227-234.
64. Sequeira T., Vilanova M., Lobo-da-Cunha A., Baldaia L., Arala-Chaves M. Flow cytometric analysis of molt-related changes in hemocyte type in male and female Penaeus japonicus. Biol Bull 1995, 189:376-380.
65. Liu C.-H., Yeh S.-T., Cheng S.-Y., Chen J.-C. The immune response of the white shrimp Litopenaeus vannamei and its susceptibility to Vibrio infection in relation with the moult cycle. Fish Shellfish Immunol 2004, 16:151-161.
66. Griffith D.R.W., Wigglesworth J.M. Growth rhytms in the shrimp Penaeus vannamei and P. schimitti. Mar Biol 1993, 115:295-299.
67. Withers P.C. Comparative animal physiology 1992, Brooks/Cole - Thomson Learning, Pacific Grove, CA, pp. 80-5.
68. Andersen J.T., Baatrup E. Ultrastructural localization of mercury accumulations in the gills, hepatopancreas, midgut, and antennal glands of the brown shrimp, Crangon crangon. Aquat Toxicol 1988, 13:309-324.
69. Dall W., Smith D.M. Ionic regulation of four species of penaeid prawn. J Exp Mar Biol Ecol 1981, 55:219-232.
70. Doughtie D.G., Rao K.R. Histopathological and ultrastructural changes in the antennal gland, midgut, hepatopancreas, and gill of grass shrimp following exposure to hexavalent chromium. J Invertebr Pathol 1984, 43:89-108.
71. Lin S.-C., Liou C.-H., Cheng J.-H. The role of the antennal glands in ion and body volume regulation of cannulated Penaeus monodon reared in various salinity conditions. Comp Biochem Physiol A 2000, 127:121-129.
72. Doughtie D.G., Rao K.R. Ultrastructural and histological study of degenerative changes in the antennal glands, hepatopancreas, and midgut of grass shrimp exposed to two dithiocarbamate biocides. J Invertebr Pathol 1983, 41:281-300.
73. Boonyaratpalin S., Supamattaya K., Kasornchandra J., Direkbusarocom S., Aekpanithanpong U., Chantanachooklin C. Non-occluded baculo-like virus, the causative agent of yellow head disease in the black tiger shrimp (Penaeus monodon). Gyobyo Kenkyu 1993, 28:103-109.
74. Speel E.J.M., Hopman A.H.N., Komminoth P. Amplification methods to increase the sensitivity of in situ hybridization: play CARD(S). J Histochem Cytochem 1999, 47:281-288.
75. Labat-Moleur F., Guillermet C., Lorimier P., Robert C., Lantuejoul S., Brambilla E., et al. TUNEL apoptotic cell detection in tissue sections: critical evaluation and improvement. J Histochem Cytochem 1998, 46:327-334.
76. Rusaini, Owens L. Validation of quantitative analysis of the LOS cells in prawns. J Agroland 2007, 14:72-76.
77. Unajak S., Boonsaeng V., Jitrapakdee S. Isolation and characterization of cDNA encoding Argonaute, a component of RNA silencing in shrimp (Penaeus monodon). Comp Biochem Physiol B 2006, 145:179-187.
78. Burge E.J., Madigan D.J., Burnett L.E., Burnett K.G. Lysozyme gene expression by hemocytes of Pacific white shrimp, Litopenaeus vannamei, after injection with Vibrio. Fish Shellfish Immunol 2007, 22:327-339.
79. Yang C., Zhang J., Li F., Ma H., Zhang Q., Jose Priya T.A., et al. A Toll receptor from Chinese shrimp Fenneropenaeus chinensis is responsive to Vibrio anguillarum infection. Fish Shellfish Immunol 2008, 24:564-574.
80. Sangsuriya P., Rojtinnakorn J., Senapin S., Flegel T.W. Characterization and tissue expression of apoptosis-related ALG-2 interacting protein Alix/AIP1 from the black tiger shrimp Penaeus monodon. Fish Shellfish Immunol 2007, 23:485-492.
81. Sriphaijit T., Senapin S. High expression of a novel leucine-rich repeat protein in hemocytes and the lymphoid organ of the black tiger shrimp Penaeus monodon. Fish Shellfish Immunol 2007, 22:264-271.
82. 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.
83. O'Leary N.A., Trent H.F., Robalino J., Peck M.E.T., McKillen D.J., Gross P.S. Analysis of multiple tissue-specific cDNA libraries from the Pacific whiteleg shrimp, Litopenaeus vannamei. Integr Comp Biol 2006, 46:931-939.
84. Supungul P., Klinbunga S., Pichyangkura R., Hirono I., Aoki T., Tassanakajon A. Antimicrobial peptides discovered in the black tiger shrimp Penaeus monodon using the EST approach. Dis Aquat Org 2004, 61:123-135.
85. Chen D., He N., Xu X. Mj-DWD, a double WAP domain-containing protein with antiviral relevance in Marsupenaeus japonicus. Fish Shellfish Immunol 2008, 25:775-781.
86. Dong B., Xiang J.-H. Discovery of genes involved in defense/immunity functions in a haemocytes cDNA library from Fenneropenaeus chinensis by ESTs annotation. Aquaculture 2007, 272:208-215.
87. Gross P.S., Bartlett T.C., Browdy C.L., Chapman R.W., Warr G.W. Immune gene discovery by expressed sequence tag analysis of hemocytes and hepatopancreas in the Pacific white shrimp, Litopenaeus vannamei, and the Atlantic white shrimp, L. setiferus. Dev Comp Immunol 2001, 25:565-577.
88. Rojtinnakorn J., Hirono I., Itami T., Takahashi Y., Aoki T. Gene expression in haemocytes of kuruma prawn, Penaeus japonicus, in response to infection with WSSV by EST approach. Fish Shellfish Immunol 2002, 13:69-83.
89. Supungul P., Klibunga S., Pichangkura R., Jitrapakdee S., Hirono I., Aoki T., et al. Identification of immune-related genes in haemocytes of black tiger shrimp (Penaeus monodon). Mar Biotechnol 2002, 4:487-494.
90. Costa A.M., Buglione C.C., Bezerra F.L., Martins P.C.C., Barracco M.A. Immune assessment of farm-reared Penaeus vannamei shrimp naturally infected by IMNV in NE Brazil. Aquaculture 2009, 291:141-146.
91. Liu Y., Li F., Wang B., Dong B., Zhang X., Xiang J. A serpin from Chinese shrimp Fenneropenaeus chinensis is responsive to bacteria and WSSV challenge. Fish Shellfish Immunol 2009, 26:345-351.
92. Maningas M.B.B., Koyama T., Kondo H., Hirono I., Aoki T. A peroxiredoxin from kuruma shrimp, Marsupenaeus japonicus, inhibited by peptidoglycan. Dev Comp Immunol 2008, 32:198-203.
93. Somboonwiwat K., Bachère E., Rimphanitchayakit V., Tassanakajon A. Localization of anti-lipopolysaccharide factor (ALFPm3) in tissues of the black tiger shrimp, Penaeus monodon, and characterization of its binding properties. Dev Comp Immunol 2008, 32:1170-1176.
94. Vatanavicharn T., Supungul P., Puanglarp N., Yingvilasprasert W., Tassanakajon A. Genomic structure, expression pattern and functional characterization of crustinPm5, a unique isoform of crustin from Penaeus monodon. Comp Biochem Physiol B 2009, 153:244-252.
95. Yeh M.-S., Lai C.-Y., Liu C.-H., Kuo C.-M., Cheng W. A second proPO present in white shrimp Litopenaeus vannamei and expression of the proPOs during a Vibrio alginolyticus injection, molt stage, and oral sodium alginate ingestion. Fish Shellfish Immunol 2009, 26:49-55.
96. Chang C.-C., Yeh M.-S., Lin H.-K., Cheng W. The effect of Vibrio alginolyticus infection on caspase-3 expression and activity in white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 2008, 25:672-678.
97. Wang Y.-C., Chang P.-S., Chen H.-Y. Tissue expressions of nine genes important to immune defence of the Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 2007, 23:1161-1177.