Table of Contents Author Guidelines Submit a Manuscript
Clinical and Developmental Immunology
Volume 2013, Article ID 536534, 9 pages
http://dx.doi.org/10.1155/2013/536534
Review Article

Influence of the Cholinergic System on the Immune Response of Teleost Fishes: Potential Model in Biomedical Research

1Universidad Autónoma de Nayarit (UAN), Secretaría de Investigación y Posgrado, Laboratorio de Inmunotoxicología, Boulevard Tepic-Xalisco s/n, Cd de la Cultura Amado Nervo, 63190 Tepic, Nayarit, Mexico
2Departamento de Ciencias Ambientales, Instituto de Neurociencias, Centro Universitario de Ciencias Biológicas y Agropecuarias (CUCBA), Universidad de Guadalajara (UdeG), Francisco de Quevedo 180, Col. Arcos Vallarta, 45100 Guadalajara, Jal, Mexico
3Departamento de Investigación Básica, Instituto Nacional de Geriatría (INGER), Periférico Sur No. 2767, Col. San Jerónimo Lídice, Del. Magdalena Contreras, 10200 México, DF, Mexico

Received 26 July 2013; Revised 24 September 2013; Accepted 26 September 2013

Academic Editor: Marco Antonio Velasco-Velázquez

Copyright © 2013 G. A. Toledo-Ibarra et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. I. A. Hurley, R. L. Mueller, K. A. Dunn et al., “A new time-scale for ray-finned fish evolution,” Proceedings of the Royal Society B, vol. 274, no. 1609, pp. 489–498, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. J.-N. Volff, “Genome evolution and biodiversity in teleost fish,” Heredity, vol. 94, no. 3, pp. 280–294, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. G. W. Litman, J. P. Cannon, and L. J. Dishaw, “Reconstructing immune phylogeny: new perspectives,” Nature Reviews Immunology, vol. 5, no. 11, pp. 866–879, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. P. R. Rauta, B. Nayak, and S. Das, “Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms,” Immunology Letters, vol. 148, no. 1, pp. 23–33, 2012. View at Publisher · View at Google Scholar
  5. C. M. Press and Ø. Evensen, “The morphology of the immune system in teleost fishes,” Fish & Shellfish Immunology, vol. 9, no. 4, pp. 309–318, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Zwollo, S. Cole, E. Bromage, and S. Kaattari, “B cell heterogeneity in the teleost kidney: evidence for a maturation gradient from anterior to posterior kidney,” Journal of Immunology, vol. 174, no. 11, pp. 6608–6616, 2005. View at Google Scholar · View at Scopus
  7. A. Zapata, B. Diez, T. Cejalvo, C. Gutiérrez-De Frías, and A. Cortés, “Ontogeny of the immune system of fish,” Fish & Shellfish Immunology, vol. 20, no. 2, pp. 126–136, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. A. J. Davidson and L. I. Zon, “The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis,” Oncogene, vol. 23, no. 43, pp. 7233–7246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. T. J. Bowden, P. Cook, and J. H. W. M. Rombout, “Development and function of the thymus in teleosts,” Fish & Shellfish Immunology, vol. 19, no. 5, pp. 413–427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Gao, C. He, X. Liu et al., “The innate immune-related genes in catfish,” International Journal of Molecular Science, vol. 13, no. 11, pp. 14172–14202, 2012. View at Publisher · View at Google Scholar
  11. T.-J. Chia, Y.-C. Wu, J.-Y. Chen, and S.-C. Chi, “Antimicrobial peptides (AMP) with antiviral activity against fish nodavirus,” Fish & Shellfish Immunology, vol. 28, no. 3, pp. 434–439, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Saurabh and P. K. Sahoo, “Lysozyme: an important defence molecule of fish innate immune system,” Aquaculture Research, vol. 39, no. 3, pp. 223–239, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. C. S. F. Bah, E. F. Fang, T. B. Ng, S. Mros, M. McConnell, and A. El-Din Ahmed Bekhit, “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, vol. 59, no. 10, pp. 5720–5728, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Gisladottir, S. Gudmundsdottir, L. Brown, Z. O. Jonsson, and B. Magnadottir, “Isolation of two C-reactive protein homologues from cod (Gadus morhua L.) serum,” Fish & Shellfish Immunology, vol. 26, no. 2, pp. 210–219, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Boshra, J. Li, and J. O. Sunyer, “Recent advances on the complement system of teleost fish,” Fish & Shellfish Immunology, vol. 20, no. 2, pp. 239–262, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Alvarez-Pellitero, “Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects,” Veterinary Immunology and Immunopathology, vol. 126, no. 3-4, pp. 171–198, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. A. Sylvie, P. Boudinot, and E. Bengtén, “Comprehensive survey and genomic characterization of Toll-Like Receptors (TLRs) in channel catfish, Ictalurus punctatus: identification of novel fish TLRs,” Immunogenetics, vol. 65, no. 7, pp. 511–530, 2013. View at Publisher · View at Google Scholar
  18. A. M. Rieger and D. R. Barreda, “Antimicrobial mechanisms of fish leukocytes,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1238–1245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Palić, J. Ostojić, C. B. Andreasen, and J. A. Roth, “Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils,” Developmental and Comparative Immunology, vol. 31, no. 8, pp. 805–816, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Pijanowski, L. Golbach, E. Kolaczkowska, M. Scheer, B. M. L. Verburg-van Kemenade, and M. Chadzinsk, “Carp neutrophilic granulocytes form extracellular traps via ROS-dependent and independent pathways,” Fish & Shellfish Immunology, vol. 34, no. 5, pp. 1244–1252, 2013. View at Publisher · View at Google Scholar
  21. I. L. Leknes, “Eosinophilic granule cells and endocytic cells in intestinal wall of pearl gouramy (Anabantidae: Teleostei),” Fish & Shellfish Immunology, vol. 23, no. 4, pp. 897–900, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. A. E. Ellis, “Innate host defense mechanisms of fish against viruses and bacteria,” Developmental and Comparative Immunology, vol. 25, no. 8-9, pp. 827–839, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. K. J. Laing and J. D. Hansen, “Fish T cells: recent advances through genomics,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1282–1295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Zwollo, “Dissecting teleost B cell differentiation using transcription factors,” Developmental and Comparative Immunology, vol. 35, no. 9, pp. 898–905, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Barr, K. Mott, and P. Zwollo, “Defining terminally differentiating B cell populations in rainbow trout immune tissues using the transcription factor XbpI,” Fish & Shellfish Immunology, vol. 31, no. 6, pp. 727–735, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. J. O. Sunyer, “Fishing for mammalian paradigms in the teleost immune system,” Nature Immunology, vol. 14, pp. 320–326, 2013. View at Publisher · View at Google Scholar
  27. H. Dooley and M. F. Flajnik, “Antibody repertoire development in cartilaginous fish,” Developmental and Comparative Immunology, vol. 30, no. 1-2, pp. 43–56, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Tort, J. C. Balasch, and S. Mackenzie, “Fish immune system. A crossroads between innate and adaptive responses,” Inmunologia, vol. 22, no. 3, pp. 277–286, 2003. View at Google Scholar · View at Scopus
  29. R. Castro, D. Bernard, M. P. Lefranc, A. Six, A. Benmansour, and P. Boudinot, “T cell diversity and TcR repertoires in teleost fish,” Fish & Shellfish Immunology, vol. 31, no. 5, pp. 644–654, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Wang, B. Gorgoglione, T. Maehr et al., “Fish Suppressors of Cytokine Signaling (SOCS): gene discovery, modulation of expression and function,” Journal of Signal Transduction, vol. 2011, Article ID 905813, 20 pages, 2011. View at Publisher · View at Google Scholar
  31. B. M. L. Verburg-van Kemenade, C. M. S. Ribeiro, and M. Chadzinska, “Neuroendocrine-immune interaction in fish: differential regulation of phagocyte activity by neuroendocrine factors,” General and Comparative Endocrinology, vol. 172, no. 1, pp. 31–38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. F. J. Arenzana, D. Clemente, R. Sánchez-González, A. Porteros, J. Aijón, and R. Arévalo, “Development of the cholinergic system in the brain and retina of the zebrafish,” Brain Research Bulletin, vol. 66, no. 4–6, pp. 421–425, 2005. View at Publisher · View at Google Scholar
  33. N. C. Bols, J. L. Brubacher, R. C. Ganassin, and L. E. J. Lee, “Ecotoxicology and innate immunity in fish,” Developmental and Comparative Immunology, vol. 25, no. 8-9, pp. 853–873, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Galloway and R. Handy, “Immunotoxicity of organophosphorous pesticides,” Ecotoxicology, vol. 12, no. 1–4, pp. 345–363, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Abreu-Villaça, C. C. Filgueiras, and A. C. Manhães, “Developmental aspects of the cholinergic system,” Behavioural Brain Research, vol. 221, no. 2, pp. 367–378, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. I. Wessler, C. J. Kirkpatrick, and K. Racké, “The cholinergic ‘pitfall’: acetylcholine, a universal cell molecule in biological systems, including humans,” Clinical and Experimental Pharmacology and Physiology, vol. 26, no. 3, pp. 198–205, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Clemente, Á. Porteros, E. Weruaga et al., “Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis,” Journal of Comparative Neurology, vol. 474, no. 1, pp. 75–107, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Funakoshi and M. Nakano, “The sympathetic nervous system of anamniotes,” Brain, Behavior and Evolution, vol. 69, no. 2, pp. 105–113, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. P. E. Phelps, R. P. Barber, and J. E. Vaughn, “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, vol. 307, no. 1, pp. 77–86, 1991. View at Google Scholar · View at Scopus
  40. K. Funakoshi, Y. Atobe, T. Hisajima et al., “Choline acetyltransferase immunoreactive sympathetic ganglion cells in a teleost, Stephanolepis cirrhifer,” Autonomic Neuroscience: Basic and Clinical, vol. 99, no. 1, pp. 31–39, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Rodríguez-Moldes, P. Molist, F. Adrio et al., “Organization of cholinergic systems in the brain of different fish groups: a comparative analysis,” Brain Research Bulletin, vol. 57, no. 3-4, pp. 331–334, 2002. View at Publisher · View at Google Scholar
  42. D. Clemente, F. J. Arenzana, R. Sánchez-González, Á. Porteros, J. Aijón, and R. Arévalo, “Comparative analysis of the distribution of choline acetyltransferase in the central nervous system of cyprinids,” Brain Research Bulletin, vol. 66, no. 4–6, pp. 546–549, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Mueller, P. Vernier, and M. F. Wullimann, “The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio,” Brain Research, vol. 1011, no. 2, pp. 156–169, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. E. P. Rico, D. B. Rosemberg, K. J. Seibt, K. M. Capiotti, R. S. Da Silva, and C. D. Bonan, “Zebrafish neurotransmitter systems as potential pharmacological and toxicological targets,” Neurotoxicology and Teratology, vol. 33, no. 6, pp. 608–617, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Steele, V. Li, A. Lo, H. Cheng, and S. Perry, “The role of the M2 muscarinic receptor in the development of hypoxic bradycardia in zebrafish (Danio rerio) larvae,” Comparative Biochemistry and Physiology A, vol. 146, supplement 4, p. S182, 2007. View at Publisher · View at Google Scholar
  46. E. D. Levin, Z. Bencan, and D. T. Cerutti, “Anxiolytic effects of nicotine in zebrafish,” Physiology & Behavior, vol. 90, no. 1, pp. 54–58, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Bencan and E. D. Levin, “The role of α7 and α4β2 nicotinic receptors in the nicotine-induced anxiolytic effect in zebrafish,” Physiology & Behavior, vol. 95, no. 3, pp. 408–412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. C. R. Dias Assis, A. Guedes Linhares, V. M. Oliveira et al., “Comparative effect of pesticides on brain acetylcholinesterase in tropical fish,” Science of the Total Environment, vol. 441, pp. 141–150, 2012. View at Publisher · View at Google Scholar
  49. B. M. L. Verburg-Van Kemenade, E. H. Stolte, J. R. Metz, and M. Chadzinska, “Neuroendocrine-immune interactions in teleost fish,” in Fish Physiology, S. D. McCormick, A. P. Farrell, and C. J. Brauner, Eds., vol. 28, chapter 7, pp. 313–364, 2009. View at Publisher · View at Google Scholar
  50. A. S. Balasubramanian and C. D. Bhanumathy, “Noncholinergic functions of cholinesterases,” FASEB Journal, vol. 7, no. 14, pp. 1354–1358, 1993. View at Google Scholar · View at Scopus
  51. E. Weitnauer, A. Robitzki, and P. G. Layer, “Aryl acylamidase activity exhibited by butyrylcholinesterase is higher in chick than in horse, but much lower than in fetal calf serum,” Neuroscience Letters, vol. 254, no. 3, pp. 153–156, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Pezzementi and A. Chatonnet, “Evolution of cholinesterases in the animal kingdom,” Chemico-Biological Interactions, vol. 187, no. 1–3, pp. 27–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. F. Ferriere, N. A. Khan, J.-P. Meyniel, and P. Deschaux, “Characterisation of serotonin transport mechanisms in rainbow trout peripheral blood lymphocytes: role in PHA-induced lymphoproliferation,” Developmental and Comparative Immunology, vol. 23, no. 1, pp. 37–50, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. C. M. Flory, “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, vol. 14, no. 3, pp. 283–294, 1990. View at Publisher · View at Google Scholar · View at Scopus
  55. C. M. Flory and C. J. Bayne, “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, vol. 15, no. 3, pp. 135–142, 1991. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Nilsson and D. J. Grove, “Adrenergic and cholinergic innervation of the spleen of the cod: Gadus morhua,” European Journal of Pharmacology, vol. 28, no. 1, pp. 135–143, 1974. View at Google Scholar · View at Scopus
  57. R. Fange and S. Nilsson, “The fish spleen: structure and function,” Experientia, vol. 41, no. 2, pp. 152–158, 1985. View at Google Scholar · View at Scopus
  58. M. Dunier, A. K. Siwicki, and A. Demael, “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, vol. 22, no. 1, pp. 79–87, 1991. View at Google Scholar · View at Scopus
  59. M. I. Girón-Pérez, A. Santerre, F. Gonzalez-Jaime et al., “Immunotoxicity and hepatic function evaluation in Nile tilapia (Oreochromis niloticus) exposed to diazinon,” Fish & Shellfish Immunology, vol. 23, no. 4, pp. 760–769, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. M. I. Girón-Pérez, G. Zaitseva, J. Casas-Solis, and A. Santerre, “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, vol. 25, no. 5, pp. 517–521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. Horiuchi, R. Kimura, N. Kato et al., “Evolutional study on acetylcholine expression,” Life Sciences, vol. 72, no. 15, pp. 1745–1756, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Fujii and K. Kawashima, “An independent non-neuronal cholinergic system in lymphocytes,” Japanese Journal of Pharmacology, vol. 85, no. 1, pp. 11–15, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Kawashima and T. Fujii, “The lymphocytic cholinergic system and its contribution to the regulation of immune activity,” Life Sciences, vol. 74, no. 6, pp. 675–696, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Kawashima, T. Fujii, Y. Moriwaki, H. Misawa, and K. Horiguchi, “Reconciling neuronally and nonneuronally derived acetylcholine in the regulation of immune function,” Annals of the New York Aacademy of Sciences, vol. 1261, pp. 7–17, 2012. View at Publisher · View at Google Scholar
  65. C. Reardon, G. S. Duncan, A. Brüstle et al., “Lymphocyte-derived ACh regulates local innate but not adaptive immunity,” Annals of the New York Academy of Sciences, vol. 110, no. 4, pp. 1410–1415, 2013. View at Google Scholar
  66. S. Neumann, M. Razen, P. Habermehl et al., “The non-neuronal cholinergic system in peripheral blood cells: effects of nicotinic and muscarinic receptor antagonists on phagocytosis, respiratory burst and migration,” Life Sciences, vol. 80, no. 24-25, pp. 2361–2364, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. Y. Okuma and Y. Nomura, “Roles of muscarinic acetylcholine receptors in interleukin-2 synthesis in lymphocytes,” Japanese Journal of Pharmacology, vol. 85, no. 1, pp. 16–19, 2001. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Behra, X. Cousin, C. Bertrand et al., “Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo,” Nature Neuroscience, vol. 5, no. 2, pp. 111–118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. L. E. Hightower and J. L. Renfro, “Recent applications of fish cell culture to biomedical research,” Journal of Experimental Zoology, vol. 248, no. 3, pp. 290–302, 1988. View at Google Scholar · View at Scopus
  70. R. N. Winn, “Transgenic fish as models in environmental toxicology,” ILAR Journal, vol. 42, no. 4, pp. 322–329, 2001. View at Google Scholar · View at Scopus
  71. A. R. Cossins and D. L. Crawford, “Fish as models for environmental genomics,” Nature Reviews Genetics, vol. 6, no. 4, pp. 324–333, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. J. Keesey, “How electric fish became sources of acetylcholine receptor,” Journal of the History of the Neurosciences, vol. 14, no. 2, pp. 149–164, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Zouridakis, P. Zisimopoulou, K. Poulas, and S. J. Tzartos, “Recent advances in understanding the structure of nicotinic acetylcholine receptors,” IUBMB Life, vol. 61, no. 4, pp. 407–423, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Santana, E. P. Rico, and J. S. Burgos, “Can zebrafish be used as animal model to study Alzheimer's disease?” American Journal of Neurodegenerative Diseases, vol. 1, no. 1, pp. 32–48, 2012. View at Google Scholar
  75. E. D. Levin and E. Chen, “Nicotinic involvement in memory function in zebrafish,” Neurotoxicology and Teratology, vol. 26, no. 6, pp. 731–735, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Osswald, A. P. Carvalho, L. Guimarães, and L. Guilhermino, “Toxic effects of pure anatoxin-a on biomarkers of rainbow trout, Oncorhynchus mykiss,” Toxicon, vol. 70, pp. 162–169, 2013. View at Publisher · View at Google Scholar
  77. K. R. Pawar, “Toxic of teratogenic effect of fenitrothion, BHC and carbofuran on the embryonic development of Cyprinus carpio communis,” Environment and Ecology, vol. 12, no. 2, pp. 284–287, 1994. View at Google Scholar
  78. R. N. Ram and S. K. Singh, “Carbofuran-induced histopathological and biochemical changes in liver of the teleost fish, Channa punctatus (Bloch),” Ecotoxicology and Environmental Safety, vol. 16, no. 3, pp. 194–201, 1988. View at Publisher · View at Google Scholar · View at Scopus
  79. J. T. Zelikoff, “Biomarkers of immunotoxicity in fish and other non-mammalian sentinel species: predictive value for mammals?” Toxicology, vol. 129, no. 1, pp. 63–71, 1998. View at Publisher · View at Google Scholar · View at Scopus
  80. M. I. Girón-Pérez, J. Velázquez-Fernández, K. Díaz-Resendiz et al., “Immunologic parameters evaluations in Nile tilapia (Oreochromis niloticus) exposed to sublethal concentrations of diazinon,” Fish & Shellfish Immunology, vol. 27, no. 2, pp. 383–385, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. M. I. Girón-Pérez, R. Barcelós-García, Z. G. Vidal-Chavez, C. A. Romero-Bañuelos, and M. L. Robledo-Marenco, “Effect of chlorpyrifos on the hematology and phagocytic activity of Nile tilapia cells (Oreochromis niloticus),” Toxicology Mechanisms and Methods, vol. 16, no. 9, pp. 495–499, 2006. View at Publisher · View at Google Scholar · View at Scopus