Influence of the cholinergic system on the immune response of teleost fishes: Potential model in biomedical research

Clinical and Developmental Immunology

Volumn 2013, Issue , 2013, Pages

  Toledo Ibarra, G A ^a   Rojas Mayorquin A E ^b,c   Giron Perez M I ^a  

^a UNIVERSIDAD AUTÓNOMA DE NAYARIT   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c INSTITUTO NACIONAL DE GERIATRÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; BIOMEDICINE; CHOLINERGIC SYSTEM; EXPERIMENTAL MODEL; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; INNATE IMMUNITY; LYMPHOCYTE; LYMPHOID ORGAN; MEDICAL RESEARCH; NERVOUS SYSTEM; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TELEOST; ANIMAL; ANIMAL MODEL; CHOLINERGIC NERVE CELL; FISH; IMMUNITY; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE SUBPOPULATION; METABOLISM; PHYSIOLOGY;

ACETYLCHOLINE; CHOLINERGIC RECEPTOR;

ACETYLCHOLINE; ANIMALS; BIOMEDICAL RESEARCH; CHOLINERGIC NEURONS; FISHES; HUMANS; IMMUNE SYSTEM; IMMUNITY; LYMPHOCYTE SUBSETS; MODELS, ANIMAL; NEUROIMMUNOMODULATION; RECEPTORS, CHOLINERGIC;

EID: 84890045313     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2013/536534     Document Type: Review

References (81)

1. Hurley I. A., Mueller R. L., Dunn K. A., Schmidt E. J., Friedman M., Ho R. K., Prince V. E., Yang Z., Thomas M. G., Coates M. I., A new time-scale for ray-finned fish evolution. Proceedings of the Royal Society B 2007 274 1609 489 498 2-s2.0-34447305524 10.1098/rspb.2006.3749 (Pubitemid 47055521)
2. Volff J.-N., Genome evolution and biodiversity in teleost fish. Heredity 2005 94 3 280 294 2-s2.0-15544377813 10.1038/sj.hdy.6800635 (Pubitemid 40398786)
3. Litman G. W., Cannon J. P., Dishaw L. J., Reconstructing immune phylogeny: new perspectives. Nature Reviews Immunology 2005 5 11 866 879 2-s2.0-27744492083 10.1038/nri1712 (Pubitemid 41581668)
4. Rauta P. R., Nayak B., Das S., Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunology Letters 2012 148 1 23 33 10.1016/j.imlet.2012.08.003
5. Press C. M., Evensen Ø., The morphology of the immune system in teleost fishes. Fish & Shellfish Immunology 1999 9 4 309 318 2-s2.0-0000998941 10.1006/fsim.1998.0181 (Pubitemid 129595707)
6. Zwollo P., Cole S., Bromage E., Kaattari S., B cell heterogeneity in the teleost kidney: evidence for a maturation gradient from anterior to posterior kidney. Journal of Immunology 2005 174 11 6608 6616 2-s2.0-18944374347 (Pubitemid 40705621)
7. Zapata A., Diez B., Cejalvo T., Gutiérrez-De Frías C., Cortés A., Ontogeny of the immune system of fish. Fish & Shellfish Immunology 2006 20 2 126 136 2-s2.0-22844440000 10.1016/j.fsi.2004.09.005 (Pubitemid 41033795)
8. Davidson A. J., Zon L. I., The 'definitive' (and 'primitive') guide to zebrafish hematopoiesis. Oncogene 2004 23 43 7233 7246 2-s2.0-5444247906 10.1038/sj.onc.1207943 (Pubitemid 39382157)
9. Bowden T. J., Cook P., Rombout J. H. W. M., Development and function of the thymus in teleosts. Fish & Shellfish Immunology 2005 19 5 413 427 2-s2.0-19544388101 10.1016/j.fsi.2005.02.003 (Pubitemid 40727976)
10. Gao L., He C., Liu X., Su H., Gao X., Li Y., Liu W., The innate immune-related genes in catfish. International Journal of Molecular Science 2012 13 11 14172 14202 10.3390/ijms131114172
11. Chia T.-J., Wu Y.-C., Chen J.-Y., Chi S.-C., Antimicrobial peptides (AMP) with antiviral activity against fish nodavirus. Fish & Shellfish Immunology 2010 28 3 434 439 2-s2.0-76749160808 10.1016/j.fsi.2009.11.020
12. Saurabh S., Sahoo P. K., Lysozyme: an important defence molecule of fish innate immune system. Aquaculture Research 2008 39 3 223 239 2-s2.0-38549117731 10.1111/j.1365-2109.2007.01883.x (Pubitemid 351160889)
13. Bah C. S. F., Fang E. F., Ng T. B., Mros S., McConnell M., El-Din Ahmed Bekhit A., Purification and characterization of a rhamnose-binding chinook salmon roe lectin with antiproliferative activity toward tumor cells and nitric oxide-inducing activity toward murine macrophages. Journal of Agricultural and Food Chemistry 2011 59 10 5720 5728 2-s2.0-79957930654 10.1021/jf2004578
14. Gisladottir B., Gudmundsdottir S., Brown L., Jonsson Z. O., Magnadottir B., Isolation of two C-reactive protein homologues from cod (Gadus morhua L.) serum. Fish & Shellfish Immunology 2009 26 2 210 219 2-s2.0-60649096261 10.1016/j.fsi.2008.03.015
15. Boshra H., Li J., Sunyer J. O., Recent advances on the complement system of teleost fish. Fish & Shellfish Immunology 2006 20 2 239 262 2-s2.0-22844451392 10.1016/j.fsi.2005.04.004 (Pubitemid 41033801)
16. Alvarez-Pellitero P., Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Veterinary Immunology and Immunopathology 2008 126 3-4 171 198 2-s2.0-56249092734 10.1016/j.vetimm.2008. 07.013
17. Sylvie M. A., Boudinot P., Bengtén E., Comprehensive survey and genomic characterization of Toll-Like Receptors (TLRs) in channel catfish, Ictalurus punctatus: identification of novel fish TLRs. Immunogenetics 2013 65 7 511 530 10.1007/s00251-013-0694-9
18. Rieger A. M., Barreda D. R., Antimicrobial mechanisms of fish leukocytes. Developmental and Comparative Immunology 2011 35 12 1238 1245 2-s2.0-83355169929 10.1016/j.dci.2011.03.009
19. Palić D., Ostojić J., Andreasen C. B., Roth J. A., Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Developmental and Comparative Immunology 2007 31 8 805 816 2-s2.0-34047255282 10.1016/j.dci.2006.11.010 (Pubitemid 46550690)
20. Pijanowski L., Golbach L., Kolaczkowska E., Scheer M., Verburg-van Kemenade B. M. L., Chadzinsk M., Carp neutrophilic granulocytes form extracellular traps via ROS-dependent and independent pathways. Fish & Shellfish Immunology 2013 34 5 1244 1252 10.1016/j.fsi.2013.02.010
21. Leknes I. L., Eosinophilic granule cells and endocytic cells in intestinal wall of pearl gouramy (Anabantidae: Teleostei). Fish & Shellfish Immunology 2007 23 4 897 900 2-s2.0-34547593444 10.1016/j.fsi.2007.02.007 (Pubitemid 47199061)
22. Ellis A. E., Innate host defense mechanisms of fish against viruses and bacteria. Developmental and Comparative Immunology 2001 25 8-9 827 839 2-s2.0-0034888523 10.1016/S0145-305X(01)00038-6 (Pubitemid 32780993)
23. Laing K. J., Hansen J. D., Fish T cells: recent advances through genomics. Developmental and Comparative Immunology 2011 35 12 1282 1295 2-s2.0-83355169836 10.1016/j.dci.2011.03.004
24. Zwollo P., Dissecting teleost B cell differentiation using transcription factors. Developmental and Comparative Immunology 2011 35 9 898 905 2-s2.0-79959567246 10.1016/j.dci.2011.01.009
25. Barr M., Mott K., Zwollo P., Defining terminally differentiating B cell populations in rainbow trout immune tissues using the transcription factor XbpI. Fish & Shellfish Immunology 2011 31 6 727 735 2-s2.0-81255127564 10.1016/j.fsi.2011.06.018
26. Sunyer J. O., Fishing for mammalian paradigms in the teleost immune system. Nature Immunology 2013 14 320 326 10.1038/ni.2549
27. Dooley H., Flajnik M. F., Antibody repertoire development in cartilaginous fish. Developmental and Comparative Immunology 2006 30 1-2 43 56 2-s2.0-26044449608 10.1016/j.dci.2005.06.022 (Pubitemid 41405787)
28. Tort L., Balasch J. C., Mackenzie S., Fish immune system. A crossroads between innate and adaptive responses. Inmunologia 2003 22 3 277 286 2-s2.0-0242364218 (Pubitemid 37339230)
29. Castro R., Bernard D., Lefranc M. P., Six A., Benmansour A., Boudinot P., T cell diversity and TcR repertoires in teleost fish. Fish & Shellfish Immunology 2011 31 5 644 654 2-s2.0-80053248217 10.1016/j.fsi.2010.08.016
30. Wang T., Gorgoglione B., Maehr T., Holland J. W., González-Vecino J. L., Wadsworth S., Secombes C. J., Fish Suppressors of Cytokine Signaling (SOCS): gene discovery, modulation of expression and function. Journal of Signal Transduction 2011 2011 20 10.1155/2011/905813 905813
31. Verburg-van Kemenade B. M. L., Ribeiro C. M. S., Chadzinska M., Neuroendocrine-immune interaction in fish: differential regulation of phagocyte activity by neuroendocrine factors. General and Comparative Endocrinology 2011 172 1 31 38 2-s2.0-79955739827 10.1016/j.ygcen.2011.01.004
32. Arenzana F. J., Clemente D., Sánchez-González R., Porteros A., Aijón J., Arévalo R., Development of the cholinergic system in the brain and retina of the zebrafish. Brain Research Bulletin 2005 66 4-6 421 425 10.1016/j.brainresbull.2005.03.006 (Pubitemid 41247688)
33. Bols N. C., Brubacher J. L., Ganassin R. C., Lee L. E. J., Ecotoxicology and innate immunity in fish. Developmental and Comparative Immunology 2001 25 8-9 853 873 2-s2.0-0034883225 10.1016/S0145-305X(01)00040-4 (Pubitemid 32780995)
34. Galloway T., Handy R., Immunotoxicity of organophosphorous pesticides. Ecotoxicology 2003 12 1-4 345 363 2-s2.0-0037306140 10.1023/A:1022579416322 (Pubitemid 36398842)
35. Abreu-Villaça Y., Filgueiras C. C., Manhães A. C., Developmental aspects of the cholinergic system. Behavioural Brain Research 2011 221 2 367 378 2-s2.0-77955248113 10.1016/j.bbr.2009.12.049
36. Wessler I., Kirkpatrick C. J., Racké K., The cholinergic 'pitfall': acetylcholine, a universal cell molecule in biological systems, including humans. Clinical and Experimental Pharmacology and Physiology 1999 26 3 198 205 2-s2.0-0033033206 10.1046/j.1440-1681.1999.03016.x (Pubitemid 29128015)
37. Clemente D., Porteros Á., Weruaga E., Alonso J. R., Arenzana F. J., Aijón J., Arévalo R., Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis. Journal of Comparative Neurology 2004 474 1 75 107 2-s2.0-2542418147 10.1002/cne.20111 (Pubitemid 38685715)
38. Funakoshi K., Nakano M., The sympathetic nervous system of anamniotes. Brain, Behavior and Evolution 2007 69 2 105 113 2-s2.0-33846406898 10.1159/000095199 (Pubitemid 46140911)
39. Phelps P. E., Barber R. P., Vaughn J. E., Embryonic development of choline acetyltransferase in thoracic spinal motor neurons: somatic and autonomic neurons may be derived from a common cellular group. Journal of Comparative Neurology 1991 307 1 77 86 2-s2.0-0025911545
40. Funakoshi K., Atobe Y., Hisajima T., Nakano M., Kadota T., Goris R. C., Kishida R., Choline acetyltransferase immunoreactive sympathetic ganglion cells in a teleost, Stephanolepis cirrhifer. Autonomic Neuroscience: Basic and Clinical 2002 99 1 31 39 2-s2.0-0037205797 10.1016/S1566-0702(02)00061-9 (Pubitemid 34667264)
41. Rodríguez-Moldes I., Molist P., Adrio F., Pombal M. A., Pérez S. E., Yáñez J., Mandado M., Marín O., López J. M., González A., Anadon R., Organization of cholinergic systems in the brain of different fish groups: a comparative analysis. Brain Research Bulletin 2002 57 3-4 331 334 10.1016/S0361-9230(01)00700-6 (Pubitemid 34234881)
42. Clemente D., Arenzana F. J., Sánchez-González R., Porteros Á., Aijón J., Arévalo R., Comparative analysis of the distribution of choline acetyltransferase in the central nervous system of cyprinids. Brain Research Bulletin 2005 66 4-6 546 549 2-s2.0-24344486350 10.1016/j.brainresbull.2005.02.017 (Pubitemid 41247711)
43. Mueller T., Vernier P., Wullimann M. F., The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Research 2004 1011 2 156 169 2-s2.0-2442444842 10.1016/j.brainres.2004.02. 073 (Pubitemid 38638682)
44. Rico E. P., Rosemberg D. B., Seibt K. J., Capiotti K. M., Da Silva R. S., Bonan C. D., Zebrafish neurotransmitter systems as potential pharmacological and toxicological targets. Neurotoxicology and Teratology 2011 33 6 608 617 2-s2.0-84855943743 10.1016/j.ntt.2011.07.007
45. Steele S., Li V., Lo A., Cheng H., Perry S., The role of the M2 muscarinic receptor in the development of hypoxic bradycardia in zebrafish (Danio rerio) larvae. Comparative Biochemistry and Physiology A 2007 146 supplement 4 S182 10.1016/j.cbpa.2007.01.393
46. Levin E. D., Bencan Z., Cerutti D. T., Anxiolytic effects of nicotine in zebrafish. Physiology & Behavior 2007 90 1 54 58 2-s2.0-33845485067 10.1016/j.physbeh.2006.08.026 (Pubitemid 44918005)
47. Bencan Z., Levin E. D., The role of α 7 and α 4 β 2 nicotinic receptors in the nicotine-induced anxiolytic effect in zebrafish. Physiology & Behavior 2008 95 3 408 412 2-s2.0-52949104082 10.1016/j.physbeh.2008.07.009
48. Dias Assis C. R., Guedes Linhares A., Oliveira V. M., Penha França R. C., Maciel Carvalho E. V. M., Souza Bezerra R., Bezerra de Carvalho L. Jr., Comparative effect of pesticides on brain acetylcholinesterase in tropical fish. Science of the Total Environment 2012 441 141 150 10.1016/j.scitotenv.2012.09. 058
49. Verburg-Van Kemenade B. M. L., Stolte E. H., Metz J. R., Chadzinska M., McCormick S. D., Farrell A. P., Brauner C. J., Neuroendocrine-immune interactions in teleost fish. Fish Physiology 2009 28 chapter 7 313 364 10.1016/S1546-5098(09)28007-1
50. Balasubramanian A. S., Bhanumathy C. D., Noncholinergic functions of cholinesterases. FASEB Journal 1993 7 14 1354 1358 2-s2.0-0027435432 (Pubitemid 23336163)
51. Weitnauer E., Robitzki A., Layer P. G., Aryl acylamidase activity exhibited by butyrylcholinesterase is higher in chick than in horse, but much lower than in fetal calf serum. Neuroscience Letters 1998 254 3 153 156 2-s2.0-0032476123 10.1016/S0304-3940(98)00689-2 (Pubitemid 28459404)
52. Pezzementi L., Chatonnet A., Evolution of cholinesterases in the animal kingdom. Chemico-Biological Interactions 2010 187 1-3 27 33 2-s2.0-77955515328 10.1016/j.cbi.2010.03.043
53. Ferriere F., Khan N. A., Meyniel J.-P., Deschaux P., Characterisation of serotonin transport mechanisms in rainbow trout peripheral blood lymphocytes: role in PHA-induced lymphoproliferation. Developmental and Comparative Immunology 1999 23 1 37 50 2-s2.0-0033062310 10.1016/S0145-305X(98)00041-X (Pubitemid 29131636)
54. Flory C. M., Phylogeny of neuroimmunoregulation: effects of adrenergic and cholinergic agents on the in vitro antibody response of the rainbow trout, Onchorynchus mykiss. Developmental and Comparative Immunology 1990 14 3 283 294 2-s2.0-0025071444 10.1016/0145-305X(90)90019-B (Pubitemid 20277482)
55. Flory C. M., Bayne C. J., The influence of adrenergic and cholinergic agents on the chemiluminescent and mitogenic responses of leukocytes from the rainbow trout, Oncorhynchus mykiss. Developmental and Comparative Immunology 1991 15 3 135 142 2-s2.0-0025736113 10.1016/0145-305X(91)90004-I
56. Nilsson S., Grove D. J., Adrenergic and cholinergic innervation of the spleen of the cod: Gadus morhua. European Journal of Pharmacology 1974 28 1 135 143 2-s2.0-0016201899
57. Fange R., Nilsson S., The fish spleen: structure and function. Experientia 1985 41 2 152 158 2-s2.0-0022005282 (Pubitemid 15170560)
58. Dunier M., Siwicki A. K., Demael A., Effects of organophosphorus insecticides: effects of trichlorfon and dichlorvos on the immune response of carp (Cyprinus carpio). III. In vitro effects on lymphocyte proliferation and phagocytosis and in vivo effects on humoral response. Ecotoxicology and Environmental Safety 1991 22 1 79 87 2-s2.0-0025738328
59. Girón-Pérez M. I., Santerre A., Gonzalez-Jaime F., Casas-Solis J., Hernández-Coronado M., Peregrina-Sandoval J., Takemura A., Zaitseva G., Immunotoxicity and hepatic function evaluation in Nile tilapia (Oreochromis niloticus) exposed to diazinon. Fish & Shellfish Immunology 2007 23 4 760 769 2-s2.0-34547670504 10.1016/j.fsi.2007.02.004 (Pubitemid 47214567)
60. Girón-Pérez M. I., Zaitseva G., Casas-Solis J., Santerre A., Effects of diazinon and diazoxon on the lymphoproliferation rate of splenocytes from Nile tilapia (Oreochromis niloticus): the immunosuppresive effect could involve an increase in acetylcholine levels. Fish & Shellfish Immunology 2008 25 5 517 521 2-s2.0-54849433349 10.1016/j.fsi.2008.07.002
61. Horiuchi Y., Kimura R., Kato N., Fujii T., Seki M., Endo T., Kato T., Kawashima K., Evolutional study on acetylcholine expression. Life Sciences 2003 72 15 1745 1756 2-s2.0-0037469910 10.1016/S0024-3205(02)02478-5 (Pubitemid 36136078)
62. Fujii T., Kawashima K., An independent non-neuronal cholinergic system in lymphocytes. Japanese Journal of Pharmacology 2001 85 1 11 15 2-s2.0-0035134690 10.1254/jjp.85.11 (Pubitemid 32149385)
63. Kawashima K., Fujii T., The lymphocytic cholinergic system and its contribution to the regulation of immune activity. Life Sciences 2003 74 6 675 696 2-s2.0-0344255794 10.1016/j.lfs.2003.09.037 (Pubitemid 37494897)
64. Kawashima K., Fujii T., Moriwaki Y., Misawa H., Horiguchi K., Reconciling neuronally and nonneuronally derived acetylcholine in the regulation of immune function. Annals of the New York Aacademy of Sciences 2012 1261 7 17 10.1111/j.1749-6632.2012.06516.x
65. Reardon C., Duncan G. S., Brüstle A., Brenner D., Tusche M. W., Olofsson P. S., Rosas-Ballina M., Tracey K. J., Mak T. W., Lymphocyte-derived ACh regulates local innate but not adaptive immunity. Annals of the New York Academy of Sciences 2013 110 4 1410 1415
66. Neumann S., Razen M., Habermehl P., Meyer C. U., Zepp F., Kirkpatrick C. J., Wessler I., The non-neuronal cholinergic system in peripheral blood cells: effects of nicotinic and muscarinic receptor antagonists on phagocytosis, respiratory burst and migration. Life Sciences 2007 80 24-25 2361 2364 2-s2.0-34249285850 10.1016/j.lfs.2007.01.010 (Pubitemid 46818263)
67. Okuma Y., Nomura Y., Roles of muscarinic acetylcholine receptors in interleukin-2 synthesis in lymphocytes. Japanese Journal of Pharmacology 2001 85 1 16 19 2-s2.0-0035131536 10.1254/jjp.85.16 (Pubitemid 32149386)
68. Behra M., Cousin X., Bertrand C., Vonesch J.-L., Biellmann D., Chatonnet A., Strähle U., Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nature Neuroscience 2002 5 2 111 118 2-s2.0-0036164239 10.1038/nn788 (Pubitemid 34121577)
69. Hightower L. E., Renfro J. L., Recent applications of fish cell culture to biomedical research. Journal of Experimental Zoology 1988 248 3 290 302 2-s2.0-0024204480 (Pubitemid 19016512)
70. Winn R. N., Transgenic fish as models in environmental toxicology. ILAR Journal 2001 42 4 322 329 2-s2.0-0035233097 (Pubitemid 33708717)
71. Cossins A. R., Crawford D. L., Fish as models for environmental genomics. Nature Reviews Genetics 2005 6 4 324 333 2-s2.0-15944388958 10.1038/nrg1590 (Pubitemid 40469051)
72. Keesey J., How electric fish became sources of acetylcholine receptor. Journal of the History of the Neurosciences 2005 14 2 149 164 2-s2.0-21244483066 10.1080/096470490512599 (Pubitemid 40896515)
73. Zouridakis M., Zisimopoulou P., Poulas K., Tzartos S. J., Recent advances in understanding the structure of nicotinic acetylcholine receptors. IUBMB Life 2009 61 4 407 423 2-s2.0-67549116445 10.1002/iub.170
74. Santana S., Rico E. P., Burgos J. S., Can zebrafish be used as animal model to study Alzheimer's disease? American Journal of Neurodegenerative Diseases 2012 1 1 32 48
75. Levin E. D., Chen E., Nicotinic involvement in memory function in zebrafish. Neurotoxicology and Teratology 2004 26 6 731 735 2-s2.0-4644227971 10.1016/j.ntt.2004.06.010 (Pubitemid 39296757)
76. Osswald J., Carvalho A. P., Guimarães L., Guilhermino L., Toxic effects of pure anatoxin-a on biomarkers of rainbow trout, Oncorhynchus mykiss. Toxicon 2013 70 162 169 10.1016/j.toxicon.2013.04.014
77. Pawar K. R., Toxic of teratogenic effect of fenitrothion, BHC and carbofuran on the embryonic development of Cyprinus carpio communis. Environment and Ecology 1994 12 2 284 287
78. Ram R. N., Singh S. K., Carbofuran-induced histopathological and biochemical changes in liver of the teleost fish, Channa punctatus (Bloch). Ecotoxicology and Environmental Safety 1988 16 3 194 201 2-s2.0-0024210569 10.1016/0147-6513(88)90050-4 (Pubitemid 19028564)
79. Zelikoff J. T., Biomarkers of immunotoxicity in fish and other non-mammalian sentinel species: predictive value for mammals? Toxicology 1998 129 1 63 71 2-s2.0-0032464820 10.1016/S0300-483X(98)00064-X (Pubitemid 29084432)
80. Girón-Pérez M. I., Velázquez-Fernández J., Díaz-Resendiz K., Díaz-Salas F., Canto-Montero C., Medina-Díaz I., Robledo-Marenco M., Rojas-García A., Zaitseva G., Immunologic parameters evaluations in Nile tilapia (Oreochromis niloticus) exposed to sublethal concentrations of diazinon. Fish & Shellfish Immunology 2009 27 2 383 385 2-s2.0-67650456518 10.1016/j.fsi.2009.06.004
81. Girón-Pérez M. I., Barcelós-García R., Vidal-Chavez Z. G., Romero-Bañuelos C. A., Robledo-Marenco M. L., Effect of chlorpyrifos on the hematology and phagocytic activity of Nile tilapia cells (Oreochromis niloticus). Toxicology Mechanisms and Methods 2006 16 9 495 499 2-s2.0-33750045182 10.1080/15376510600751988 (Pubitemid 44582038)