Enhanced Cellular Immunity in Shrimp (Litopenaeus Vannamei) After 'vaccination'

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2011 Jun 24

PMID 21698190

Citations 21

Authors

Edward C Pope

Adam Powell

Emily C Roberts

Robin J Shields

Robin Wardle

Andrew F Rowley

Affiliations

Soon will be listed here.

Abstract

It has long been viewed that invertebrates rely exclusively upon a wide variety of innate mechanisms for protection from disease and parasite invasion and lack any specific acquired immune mechanisms comparable to those of vertebrates. Recent findings, however, suggest certain invertebrates may be able to mount some form of specific immunity, termed 'specific immune priming', although the mechanism of this is not fully understood (see Textbox S1). In our initial experiments, either formalin-inactivated Vibrio harveyi or sterile saline were injected into the main body cavity (haemocoel) of juvenile shrimp (Litopenaeus vannamei). Haemocytes (blood cells) from V. harveyi-injected shrimp were collected 7 days later and incubated with a 1:1 mix of V. harveyi and an unrelated gram positive bacterium, Bacillus subtilis. Haemocytes from 'vaccinated' shrimp showed elevated levels of phagocytosis of V. harveyi, but not B. subtilis, compared with those from saline-injected (non-immunised) animals. The increased phagocytic activity was characterised by a significant increase in the percentage of phagocytic cells. When shrimp were injected with B. subtilis rather than vibrio, there was no significant increase in the phagocytic activity of haemocytes from these animals in comparison to the non-immunised (saline injected) controls. Whole haemolymph (blood) from either 'immunised' or non-immunised' shrimp was shown to display innate humoral antibacterial activity against V. harveyi that was absent against B. subtilis. However, there was no difference in the potency of antibacterial activity between V. harveyi-injected shrimp and control (saline injected) animals showing that 'vaccination' has no effect on this component of the shrimp's immune system. These results imply that the cellular immune system of shrimp, particularly phagocytosis, is capable of a degree of specificity and shows the phenomenon of 'immune priming' reported by other workers. However, in agreement with other studies, this phenomenon is not universal to all potential pathogens.

Citing Articles

Innate and germline immune memory: specificity and heritability of the ancient immune mechanisms for adaptation and survival.

Boraschi D, Toepfer E, Italiani P Front Immunol. 2024; 15:1386578.

PMID: 38903500 PMC: 11186993. DOI: 10.3389/fimmu.2024.1386578.

Morinda citrifolia fruit extract enhances the resistance of Penaeus vannamei to Vibrio parahaemolyticus infection.

Moh J, Okomoda V, Mohamad N, Waiho K, Noorbaiduri S, Sung Y Sci Rep. 2024; 14(1):5668.

PMID: 38454039 PMC: 10920830. DOI: 10.1038/s41598-024-56173-4.

Exploring the role and mechanism of potential probiotics in mitigating the shrimp pathogens.

Tamilselvan M, Raja S Saudi J Biol Sci. 2024; 31(3):103938.

PMID: 38327656 PMC: 10847377. DOI: 10.1016/j.sjbs.2024.103938.

Alternative splicing derived invertebrate variable lymphocyte receptor displays diversity and specificity in immune system of crab .

Xu Y, Yang Y, Zheng J, Cui Z Front Immunol. 2023; 13:1105318.

PMID: 36999166 PMC: 10045472. DOI: 10.3389/fimmu.2022.1105318.

Does the heterotrophic system influence the cellular immune response of shrimp? phagocytosis indices and superoxide anion production comparisons.

Iunes R, Branco P, Pressinotti L, de Carvalho R, da Silva J Fish Shellfish Immunol Rep. 2022; 2:100009.

PMID: 36420495 PMC: 9680045. DOI: 10.1016/j.fsirep.2021.100009.

References

Mori K, Stewart J . Immunogen-dependent quantitative and qualitative differences in phagocytic responses of the circulating hemocytes of the lobster Homarus americanus. Dis Aquat Organ. 2006; 69(2-3):197-203. DOI: 10.3354/dao069197. View

Cabello F . Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol. 2006; 8(7):1137-44. DOI: 10.1111/j.1462-2920.2006.01054.x. View

Munoz M, Vandenbulcke F, Gueguen Y, Bachere E . Expression of penaeidin antimicrobial peptides in early larval stages of the shrimp Penaeus vannamei. Dev Comp Immunol. 2003; 27(4):283-9. DOI: 10.1016/s0145-305x(02)00102-7. View

Chou P, Chang H, Chen I, Lee C, Hung H, Wang K . Penaeus monodon Dscam (PmDscam) has a highly diverse cytoplasmic tail and is the first membrane-bound shrimp Dscam to be reported. Fish Shellfish Immunol. 2011; 30(4-5):1109-23. DOI: 10.1016/j.fsi.2011.02.009. View

Soderhall K, Smith V . Separation of the haemocyte populations of Carcinus maenas and other marine decapods, and prophenoloxidase distribution. Dev Comp Immunol. 1983; 7(2):229-39. DOI: 10.1016/0145-305x(83)90004-6. View

Schmid-Hempel P . Evolutionary ecology of insect immune defenses. Annu Rev Entomol. 2004; 50:529-51. DOI: 10.1146/annurev.ento.50.071803.130420. View

Rowley A, Powell A . Invertebrate immune systems specific, quasi-specific, or nonspecific?. J Immunol. 2007; 179(11):7209-14. DOI: 10.4049/jimmunol.179.11.7209. View

Fitzgerald S, Ratcliffe N . Evidence for the presence of subpopulations of Arenicola marina coelomocytes identified by their selective response towards Gram+ve and Gram-ve bacteria. Dev Comp Immunol. 1982; 6(1):23-34. DOI: 10.1016/0145-305x(82)90004-0. View

Mone Y, Gourbal B, Duval D, Du Pasquier L, Kieffer-Jaquinod S, Mitta G . A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis. 2010; 4(9). PMC: 2935394. DOI: 10.1371/journal.pntd.0000813. View

10.

Powell A, Pope E, Eddy F, Roberts E, Shields R, Francis M . Enhanced immune defences in Pacific white shrimp (Litopenaeus vannamei) post-exposure to a vibrio vaccine. J Invertebr Pathol. 2011; 107(2):95-9. DOI: 10.1016/j.jip.2011.02.006. View

11.

Sadd B, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P . Trans-generational immune priming in a social insect. Biol Lett. 2006; 1(4):386-8. PMC: 1626361. DOI: 10.1098/rsbl.2005.0369. View

12.

Garcia S, Grainger R . Gloom and doom? The future of marine capture fisheries. Philos Trans R Soc Lond B Biol Sci. 2005; 360(1453):21-46. PMC: 1636098. DOI: 10.1098/rstb.2004.1580. View

13.

Hauton C, Smith V . Adaptive immunity in invertebrates: a straw house without a mechanistic foundation. Bioessays. 2007; 29(11):1138-46. DOI: 10.1002/bies.20650. View

14.

Jiravanichpaisal P, Puanglarp N, Petkon S, Donnuea S, Soderhall I, Soderhall K . Expression of immune-related genes in larval stages of the giant tiger shrimp, Penaeus monodon. Fish Shellfish Immunol. 2007; 23(4):815-24. DOI: 10.1016/j.fsi.2007.03.003. View

15.

Munoz M, Vandenbulcke F, Saulnier D, Bachere E . Expression and distribution of penaeidin antimicrobial peptides are regulated by haemocyte reactions in microbial challenged shrimp. Eur J Biochem. 2002; 269(11):2678-89. DOI: 10.1046/j.1432-1033.2002.02934.x. View

16.

Little T, OConnor B, Colegrave N, Watt K, Read A . Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol. 2003; 13(6):489-92. DOI: 10.1016/s0960-9822(03)00163-5. View

17.

Moret Y . "Trans-generational immune priming": specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc Biol Sci. 2006; 273(1592):1399-405. PMC: 1560290. DOI: 10.1098/rspb.2006.3465. View

18.

Zhang X, Xu W, Wang X, Mu Y, Zhao X, Yu X . A novel C-type lectin with two CRD domains from Chinese shrimp Fenneropenaeus chinensis functions as a pattern recognition protein. Mol Immunol. 2009; 46(8-9):1626-37. DOI: 10.1016/j.molimm.2009.02.029. View

19.

Brites D, McTaggart S, Morris K, Anderson J, Thomas K, Colson I . The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. Mol Biol Evol. 2008; 25(7):1429-39. DOI: 10.1093/molbev/msn087. View

20.

Roth O, Kurtz J . Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev Comp Immunol. 2009; 33(11):1151-5. DOI: 10.1016/j.dci.2009.04.005. View