Células Granulares Eosinofílicas/Células Mast (CGE/MC) y su relación con los efectos de herbicidas: Caso del Glifosato y surfactantes acompañantes en peces

Eosinophlic granular cells/Mast cells and their relation with the effects of herbicides: Case of glyphosate and accompaning surfactants on fish

Contenido principal del artículo

Jeraldyn Argüello-Rangel
Pedro A. Triana-García
Pedro R. Eslava-Mocha

Resumen

Los Mastocitos, Células Granulares Eosinofílicas (CGE) o células Mast de los peces (MC) pertenecientes al sistema inmune, han sido relacionadas en diferentes tipos de respuestas fisiológicas y patológicas en peces. Recientemente, se ha incrementado el interés científico relacionado con su participación en reacciones ante contaminantes acuáticos, así mismo, frente a agentes infecciosos y últimamente como modelos de peces para estudiar enfermedades que involucran desordenes alérgicos y alteraciones neurodegenerativas en los seres humanos. Numerosos trabajos en varias especies de teleósteos han demostrado que los comportamientos de CGE/MC son relevantes para estudiar mecanismos anti-infecciosos. Así mismo, se ha estudiado su respuesta ante la exposición a contaminantes tales como los herbicidas, que pueden interferir con el sistema nervioso y el olfato de los peces. Se muestran datos de trabajos sobre mastocitos de peces y se sugiere la importancia de estudiarlas también como biomarcador ante contaminantes. En esta revisión se enfatiza su participación en las respuestas de diferentes órganos y tejidos ante la exposición a herbicidas como el glifosato y los surfactantes acompañantes en las mezclas asperjadas, su morfología, su papel fisiológico y patológico, y sobre algunas posibles formas de estudiarlas en el sistema nervioso, especialmente, frente a exposiciones subletales a pesticidas.

Palabras clave: Mastocitos; POEA; Roundup®; toxicidad; patología toxicológica de peces; inmunohistoquímica; telencéfalo.

Descargas

Los datos de descargas todavía no están disponibles.

Detalles del artículo

Biografía del autor/a (VER)

Jeraldyn Argüello-Rangel, Universidad de los Llanos Villavicencio Colombia

MVZ, Unillanos. Villavicencio, Colombia.

Pedro A. Triana-García, Ciencias Agrarias Universidad de los Llanos Colombia

MV, MSc, Estudiante de Doctorado en Ciencias Agrarias Unillanos. 

Pedro R. Eslava-Mocha, Universidad de los Llanos Colombia

PhD., Ciencias Agrarias Unillanos. 

[email protected]

Referencias (VER)

Acosta J, Montero V, Carpio Y, Velázquez J, Garay HE, Reyes O, Cabrales A, Masforrol Y, Morales A, Estrada MP. Cloning and functional characterization of three novel antimicrobial peptides from tilapia (Oreochromis niloticus). Aquaculture. 2013; (372-375): 9-18.


Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S. Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta. 2000; 1523: 37-48.


Albinati ACL, Moreira ELT, Albinati RCB, Carvalho JV, Santos GB, Lira AD. 2007. Toxicidade aguda do herbicida roundup® para piauçu ("Leporinus macrocephalus"). Rev Bras Saúde Prod An. 2007; 8(3): 184-192.


Alejo A, Tafalla C. Chemokines in teleost fish species. Dev Comp Immunol 2011; 35: 1215-1222.


Alvarez-Moya C, Silva MR, Arambula AR, Sandoval AI, Vasquez HC, Gonzalez-Montes RM. Evaluation of genetic damage induced by glyphosate isopropylamine salt using Tradescantia bioassays. Genet Mol Biol. 2011; 34: 127-130.


Alvarez-Moya C, Silva MR, Ramírez CV, Gallardo DG, Sánchez RL, Aguirre AC, Velasco AF. Comparison of the in vivo and in vitro genotoxicity of glyphosate isopropylamine salt in three different organisms. Genet Mol Biol. 2014; 37: 105-110.


Alvarez-Pellitero P. Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet Immunol Immunopathol. 2008; 126: 171-198.


Allen SL. Regulatory aspects of neurotoxicity assessment. In: Krieger RI, editor. Hayes' Handbook of Pesticide Toxicology. Elsevier; New York: 2010; 3(1): 587-602.


Amarante Junior OPD, Santos TCRD, Brito NM, Ribeiro ML. Glifosato: propriedades, toxicidade, usos e legislação. Química Nova. 2002; 25: 589-593.


Antón FA, Laborda E, De Ariz M. Acute toxicity of the herbicide glyphosate to fish. Chemosphere. 1994; 28: 745-753.


Baccari GC, Pinelli C, Santillo A, Minucci S, Rastogi RK. Mast cells in nonmammalian vertebrates: an overview. Int Rev Cell Mol Biol. 2011; 290: 1-53.


Bao B, Peatman E, Xu P, Li P, Zeng H, He C, Liu Z. The catfish liver-expressed antimicrobial peptide 2 (LEAP-2) gene is expressed in a wide range of tissues and developmentally regulated. Mol Immunol. 2006; 43: 367-77.

Ben Ameur W, De Lapuente J, El Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-Lopez D, Gonzalez-Linares J, Driss MR, Borras M. Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull. 2012; 64: 241-51.


Blackstock N, Pickering AD. Acidophilic granular cells in the epidermis of the brown trout, Salmo trutta L. Cell Tissue Res. 1980; 210: 359-69.


Bolognesi C, Carrasquilla G, Volpi S, Solomon KR, Marshall EJ. Biomonitoring of genotoxic risk in agricultural workers from five colombian regions: association to occupational exposure to glyphosate. J Toxicol Environ Health A. 2009; 72: 986-997.


Borggaard OK, Gimsing AL. Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: a review. Pest Manag Sci. 2008; 64: 441-56.


Buonocore F, Randelli E, Casani D, Picchietti S, Belardinelli MC, De Pascale D, De Santi C, Scapigliati G. A piscidin-like antimicrobial peptide from the icefish Chionodraco hamatus (Perciformes: Channichthyidae): molecular characterization, localization and bactericidal activity. Fish Shellfish Immunol. 2012; 33: 1183-1191.


Buss RR, Sun W, Oppenheim RW. Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci. 2006; 29: 1-35.


Cammarata M, Vazzana M, Cervello M, Arizza V, Parrinello N. Spontaneous cytotoxic activity of eosinophilic granule cells separated from the normal peritoneal cavity of Dicentrarchus labrax. Fish Shellfish Immunol. 2000; 10: 143-154.


Castañeda CD. 2012. Descripción de las vías olfativas (roseta - bulbo olfativo) y evaluación de los efectos histopatológicos causados por el Roundup® activo sobre el sistema olfativo de alevinos de cachama blanca (Piaractus brachypomus). Biologo, Universidad Militar Nueva Granada.


Cavalcante DG, Martinez CB, Sofia SH. Genotoxic effects of Roundup on the fish Prochilodus lineatus. Mutat Res. 2008; 655: 41-46.


Cavas T, Konen S. Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis. 2007; 22: 263-268.


Cazenave J, Bacchetta C, Parma MJ, Scarabotti PA, Wunderlin DA. Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the water quality of Salado River basin (Santa Fe, Argentina). Environ Pollut. 2009; 157: 3025-3033.


Coimbra AM, Figueiredo-Fernandes A, Reis-Henriques MA. Nile tilapia (Oreochromis niloticus), liver morphology, CYP1A activity and thyroid hormones after Endosulfan dietary exposure. Pestic Biochem Physiol. 2007; 89: 230-236.


Corrales J, Mulero I, Mulero V, Noga EJ. Detection of antimicrobial peptides related to piscidin 4 in important aquacultured fish. Dev Comp Immunol. 2010; 34: 331-43.


Cuesta A, Meseguer J, Esteban MA. Molecular and functional characterization of the gilthead seabream beta-defensin demonstrate its chemotactic and antimicrobial activity. Mol Immunol. 2011; 48: 1432-1438.


Chang CI, Zhang YA, Zou J, Nie P, Secombes CJ. Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and atlantic salmon (Salmo salar). Antimicrob Agents Chemother. 2006; 50: 185-195.


Chekmenev EY, Vollmar BS, Forseth KT, Manion MN, Jones SM, Wagner TJ, Endicott RM, Kyriss BP, Homem LM, Pate M, He J, Raines J, Gor'kov PL, Brey WW, Mitchell DJ, Auman AJ, Ellard-Ivey MJ, Blazyk J, Cotten M. Investigating molecular recognition and biological function at interfaces using piscidins, antimicrobial peptides from fish. Biochim Biophys Acta. 2006; 1758: 1359-1372.


Da'as S, Teh EM, Dobson JT, Nasrallah GK, Mcbride ER, Wang H, Neuberg DS, Marshall JS, Lin TJ, Berman JN. Zebrafish mast cells possess an FcvareRI-like receptor and participate in innate and adaptive immune responses. Dev Comp Immunol. 2011; 35: 125-134.


Da'as SI, Coombs AJ, Balci TB, Grondin CA, Ferrando A A, Berman JN. The zebrafish reveals dependence of the mast cell lineage on Notch signaling in vivo. Blood. 2012; 119: 3585-94.

De Roos AJ, Blair A, Rusiecki JA, Hoppin JA, Svec M, Dosemeci M, Sandler DP, Alavanja MC. Cancer incidence among glyphosate-exposed pesticide applicators in the Agricultural Health Study. Environ Health Perspect. 2005; 113: 49-54.

Dezfuli BS, Giari L, Lui A, Lorenzoni M, Noga EJ. Mast cell responses to Ergasilus (Copepoda), a gill ectoparasite of sea bream. Fish Shellfish Immunol. 2011; 30: 1087-94.

Dezfuli BS, Giovinazzo G, Lui A, Giari L. Inflammatory response to Dentitruncus truttae (Acanthocephala) in the intestine of brown trout. Fish Shellfish Immun. 2013; 36: 577-585.

Dezfuli BS, Lui A, Pironi F, Manera M, Shinn AP, Lorenzoni M. Cell types and structures involved in tench, Tinca tinca (L.), defence mechanisms against a systemic digenean infection. J Fish Dis. 2013; 36: 577-85.

Dimitrov BD, Gadeva PG, Benova DK, Bineva MV. Comparative genotoxicity of the herbicides Roundup, Stomp and Reglone in plant and mammalian test systems. Mutagenesis. 2006; 21: 375-382.

Dobson JT, Seibert J, Teh EM, Da'as S, Fraser RB, Paw BH, Lin TJ, Berman JN. Carboxypeptidase A5 identifies a novel mast cell lineage in the zebrafish providing new insight into mast cell fate determination. Blood. 2008; 112: 2969-72.

Douglas SE, Gallant JW, Gong Z, Hew C. Cloning and developmental expression of a family of pleurocidin-like antimicrobial peptides from winter flounder, Pleuronectes americanus (Walbaum). Dev Comp Immunol. 2001; 25: 137-47.

Douglas SE, Gallant JW, Liebscher RS, Dacanay A, Tsoi SCM. Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev Comp Immunol. 2003; 27: 589-601.

Duke SO, Powles SB. Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 2008; 64: 319-325.

Elie-Caille C, Heu C, Guyon C, Nicod L. Morphological damages of a glyphosate-treated human keratinocyte cell line revealed by a micro- to nanoscale microscopic investigation. Cell Biology and Toxicology. 2010; 26: 331-339.

Ellis AE. Eosinophilic granular cells (EGC) and histamine responses to Aeromonas salmonicida toxins in rainbow trout. Dev Comp Immunol. 1985; 9: 251-260.

EPA. 2012. Herbicides [Online]. US. Available: http://www.epa.gov/caddis/ssr_herb_int.html [Accessed 09/02/2015]
.

Evrard E, Marchand J, Theron M, Pichavant-Rafini K, Durand G, Quiniou L, Laroche J. Impacts of mixtures of herbicides on molecular and physiological responses of the European flounder Platichthys flesus. Comp Biochem Physiol C Toxicol Pharmacol. 2010; 152: 321-331.

Ferreira D, Da Motta AC, Kreutz LC, Toni C, Loro VL, Barcellos LJ. Assessment of oxidative stress in Rhamdia quelen exposed to agrichemicals. Chemosphere. 2010; 79: 914-921.

Figueiredo-Fernandes A, Fontaínhas-Fernandes A, Rocha E, Reis-Henriques MA. The Effect of Paraquat on Hepatic EROD Activity, Liver, and Gonadal Histology in Males and Females of Nile Tilapia, Oreochromis niloticus, Exposed at Different Temperatures. Arch Environ Contam Toxicol. 2006; 51: 626-632.

Figueiredo-Fernandes AM, Fontainhas-Fernandes AA, Monteiro RA, Reis-Henriques MA, Rocha E. Spatial relationships of the intrahepatic vascular-biliary tracts and associated pancreatic acini of Nile tilapia, Oreochromis niloticus (Teleostei, Cichlidae): a serial section study by light microscopy. Ann Anat. 2007; 189: 17-30.

Folmar LC, Sanders HO, Julin AM. Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Arch Environ Contam Toxicol. 1979; 8: 269-278.

Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, Tsai M. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu Rev Immunol. 2005; 23: 749-786.

Garg TK, Domingos FXV, Almeida-Val VMF, Val AL. Histochemistry and functional organization of the dorsal skin of Ancistrus dolichopterus (Siluriformes: Loricariidae). Neotrop Ichthyol. 2010; 8: 877-884.

Giesy JP, Dobson S, Solomon KR. Ecotoxicological Risk Assessment for Roundup Herbicide. Rev Environ Contam Toxicol. 2000; 167: 35-120.

Glusczak L, Miron Ddos S, Moraes BS, Simoes RR, Schetinger MR, Morsch VM, Loro VL. Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comp Biochem Physiol C Toxicol Pharmacol. 2007; 146: 519-524.

Gomez D, Sunyer JO, Salinas I. The mucosal immune system of fish: The evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol. 2013; 35: 1729-1739.

Guilherme S, Gaivao I, Santos MA, Pacheco M. DNA damage in fish (Anguilla anguilla) exposed to a glyphosate-based herbicide - elucidation of organ-specificity and the role of oxidative stress. Mutat Res. 2012; 743: 1-9.

Hellberg H, Bjerkas I, Vagnes OB, Noga EJ. Mast cells in common wolffish Anarhichas lupus L.: ontogeny, distribution and association with lymphatic vessels. Fish Shellfish Immunol. 2013; 35: 1769-1778.

Hildebrand LD, Sullivan DS, Sullivan TP. Experimental studies of rainbow trout populations exposed to field applications of Roundup herbicide. Arch Environ Contam Toxicol. 1982; 11: 93-98.

Holland JW, Rowley AF. Studies on the eosinophilic granule cells in the gills of the rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1998; 120: 321-328.

Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N. Toxicity of glyphosate-based pesticides to four North American frog species. Environ Toxicol Chem. 2004; 23: 1928-1938.

Jackson AJ, Kerr AK, Cowey CB. Fish silage as a dietary ingredient for salmon. I. Nutritional and storage characteristics. Aquaculture. 1984; 38: 211-220.

Jarrard HE, Delaney KR, Kennedy CJ. Impacts of carbamate pesticides on olfactory neurophysiology and cholinesterase activity in coho salmon (Oncorhynchus kisutch). Aquat Toxicol. 2004; 69: 133-148.

Jiraungkoorskul W, Upatham ES, Kruatrachue M, Sahaphong S, Vichasri-Grams S, Pokethitiyook P. Biochemical and histopathological effects of glyphosate herbicide on Nile tilapia (Oreochromis niloticus). Environ Toxicol. 2003; 18: 260-267.

Jiraungkoorskula W, Upathama ES, Kruatrachuea M, Sahaphongc S, Vichasri-Gramsa S, Pokethitiyooka P. Histophatological effects of Roundup, a glyphosate herbicide, on Nile tilapia (Oreochromis niloticus). Sci Asia. 2002; 28: 121-127.

Jordanova M, Miteva N, Rocha E. A quantitative study of the hepatic eosinophilic granule cells and rodlet cells during the breeding cycle of Ohrid trout, Salmo letnica Kar. (Teloestei, Salmonidae). Fish Shellfish Immunol. 2007; 23: 473-478.

Kelly DW, Poulin R, Tompkins DM, Townsend CR. Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. J Appl Ecol. 2010; 47: 498-504.

Kolpin DW, Thurman EM, Lee EA, Meyer MT, Furlong ET, Glassmeyer ST. Urban contributions of glyphosate and its degradate AMPA to streams in the United States. Sci Total Environ. 2006; 354: 191-197.

Kunder CA, St John AL, Abraham SN. Mast cell modulation of the vascular and lymphatic endothelium. Blood. 2011; 118: 5383-5393.

Langiano C, Martinez CB. Toxicity and effects of a glyphosate-based herbicide on the Neotropical fish Prochilodus lineatus. Comp Biochem Physiol C Toxicol Pharmacol. 2008; 147: 222-231.

Lauriano ER, Calo M, Silvestri G, Zaccone D, Pergolizzi S, Lo Cascio P. Mast cells in the intestine and gills of the sea bream, Sparus aurata, exposed to a polychlorinated biphenyl, PCB 126. Acta Histochem. 2012; 114: 166-171.

Lauth X, Shike H, Burns JC, Westerman ME, Ostland VE, Carlberg JM, Van Olst JC, Nizet V, Taylor SW, Shimizu C, Bulet P. Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. J Biol Chem. 2002; 277: 5030-5039.

Leknes IL. Eosinophilic granule cells and endocytic cells in intestinal wall of pearl gouramy (Anabantidae: Teleostei). Fish Shellfish Immunol. 2007; 23: 897-900.

Lema SC, Hodges MJ, Marchetti MP, Nevitt GA. Proliferation zones in the salmon telencephalon and evidence for environmental influence on proliferation rate. Comp Biochem Physiol A Mol Integr Physiol. 2005; 141: 327-335.

Lourenço J, Silva A, Carvalho F, Oliveira J, Malta M, Mendo S, Gonçalves F, Pereira R. Histopathological changes in the earthworm Eisenia andrei associated with the exposure to metals and radionuclides. Chemosphere. 2011; 85: 1630-1634.

Lushchak OV, Kubrak OI, Storey JM, Storey KB, Lushchak VI. Low toxic herbicide Roundup induces mild oxidative stress in goldfish tissues. Chemosphere, 2009; 76: 932-937.

Marc J, Bellé R, Morales J, Cormier P, Mulner-Lorillon O. Formulated Glyphosate Activates the DNA-Response Checkpoint of the Cell Cycle Leading to the Prevention of G2/M Transition. Toxicol Sci. 2004a; 82: 436-442.

Marc J, Le Breton M, Cormier P, Morales J, Belle R, Mulner-Lorillon O. A glyphosate-based pesticide impinges on transcription. Toxicol Appl Pharmacol. 2005; 203: 1-8.

Marc J, Mulner-Lorillon O, Belle R. Glyphosate-based pesticides affect cell cycle regulation. Biol Cell. 2004b; 96: 245-249.

Marc J, Mulner-Lorillon O, Boulben S, Hureau D, Durand G, Belle R. Pesticide Roundup provokes cell division dysfunction at the level of CDK1/cyclin B activation. Chem Res Toxicol. 2002; 15: 326-331.

Marc J, Mulner-Lorillon O, Durand G, Belle R. Embryonic cell cycle for risk assessment of pesticides at the molecular level. Environ Chem Lett. 2003; 1: 8-12.

Marchand J, Tanguy A, Charrier G, Quiniou L, Plee-Gauthier E, Laroche J. Molecular identification and expression of differentially regulated genes of the European flounder, Platichthys flesus, submitted to pesticide exposure. Mar Biotechnol (NY). 2006; 8: 275-294.

Matsuyama T, Iida T. Degranulation of eosinophilic granular cells with possible involvement in neutrophil migration to site of inflammation in tilapia. Dev Comp Immunol. 1999; 23: 451-457.

Matsuyama T, Iida T. Influence of tilapia mast cell lysate on vascular permeability. Fish Shellfish Immunol. 2001; 11: 549-556.

Matsuyama T, Iida T. Tilapia mast cell lysates enhance neutrophil adhesion to cultured vascular endothelial cells. Fish Shellfish Immunol. 2002; 13: 243-250.

Matthiessen P, Roberts RJ. Histopathological changes in the liver and brain of fish exposed to endosulfan insecticide during tsetse fly control operations in Botswana. J Fish Dis. 1982; 5: 153-159.

Mazon AF, Huising MO, Taverne-Thiele AJ, Bastiaans J, Verburg-Van Kemenade BM. The first appearance of Rodlet cells in carp (Cyprinus carpio L.) ontogeny and their possible roles during stress and parasite infection. Fish Shellfish Immunol. 2007; 22: 27-37.

Mitchell DG, Chapman PM, Long TJ. Acute toxicity of Roundup and Rodeo herbicides to rainbow trout, chinook, and coho salmon. Bull Environ Contam Toxicol. 1987; 39: 1028-1035.

Modesto KA, Martinez CB. Effects of Roundup Transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere. 2010a; 81: 781-787.

Modesto KA, Martinez CB. Roundup causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere. 2010b; 78: 294-299.

Monheit S. 2003. Glyphosate - based aquatic herbicides an overview of risk [Online]. Available: https://scholar.google.com.co/scholar?q=Glyphosate+-+based+aquatic+herbicides+an+overview+of+risk.&-hl=es&-as_sdt=0&-as_vis=1&-oi=scholart&-sa=X&-ei=-g_ZVKWdI8OVNrKUgZAL&-ved=0CBoQgQMwAA [Accessed 09/02/2015]
.

Monsanto. 2010. Roundup Transorb [Online]. Available: http://monsanto.com.br/produtos/herbicidas/fichas-deemergencia-e-bulas/pdf/roundup-transorb-bula.pdf [Accessed 02/20/2015]
.

Moreno NC, Sofia SH, Martinez CB. Genotoxic effects of the herbicide Roundup Transorb and its active ingredient glyphosate on the fish Prochilodus lineatus. Environ Toxicol Pharmacol. 2014; 37: 448-454.

Mortensen DA, Franklin Egan J, Maxwell BD, Ryan MR, Smith RG. Navigating a Critical Juncture for Sustainable Weed Management. Bio Science. 2012; 62: 9.

Mulero I, Noga EJ, Meseguer J, Garcia-Ayala A, Mulero V. The antimicrobial peptides piscidins are stored in the granules of professional phagocytic granulocytes of fish and are delivered to the bacteria-containing phagosome upon phagocytosis. Dev Comp Immunol. 2008; 32: 1531-1538.

Mulero I, Sepulcre MP, Meseguer J, Garcia-Ayala A, Mulero V. Histamine is stored in mast cells of most evolutionarily advanced fish and regulates the fish inflammatory response. Proc Natl Acad Sci USA. 2007; 104: 19434-19439.

Mutoloki S, Reite OB, Brudeseth B, Tverdal A, Evensen O. A comparative immunopathological study of injection site reactions in salmonids following intraperitoneal injection with oil-adjuvanted vaccines. Vaccine. 2006; 24: 578-588.

Neskovic NK, Poleksic V, Elezovic I, Karan V, Budimir M. Biochemical and histopathological effects of glyphosate on carp, Cyprinus carpio L. Bull Environ Contam Toxicol. 1996; 56: 295-302.

Niu SF, Jin Y, Xu X, Qiao Y, Wu Y, Mao Y, Su YQ, Wang J. Characterization of a novel piscidin-like antimicrobial peptide from Pseudosciaena crocea and its immune response to Cryptocaryon irritans. Fish Shellfish Immunol. 2013; 35: 513-524.

Nivia E. 2001. Las Guerras en Colombia: Drogas, Armas y Petróleo. Drugs, Guns and Oil [Online]. Davis, CA: Universidad de California. Available: http://www.glifocidio.org/docs/plan%20colombia%20doc/pc13.pdf [Accessed 15/02/2015]
.

Noga EJ, Ullal AJ, Corrales J, Fernandes JM. Application of antimicrobial polypeptide host defenses to aquaculture: Exploitation of downregulation and upregulation responses. Comp Biochem Physiol Part D Genomics Proteomics. 2011; 6: 44-54.

Pacheco M, Santos MA. Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol Environ Saf. 2002; 53: 331-347.

Patrzykat A, Gallant JW, Seo JK, Pytyck J, Douglas SE. Novel Antimicrobial Peptides Derived from Flatfish Genes. Antimicrobial Agents and Chemotherapy. 2003; 47: 2464-2470.

Paulsen SM, Sveinbjørnsson B, Robertsen B. Selective staining and disintegration of intestinal eosinophilic granule cells in Atlantic salmon after intraperitoneal injection of the zinc chelator dithizone. J Fish Biol. 2001; 58: 768-775.

Paz-Y-Mino C, Davalos MV, Sanchez ME, Arevalo M, Leone PE. Should gaps be included in chromosomal aberration analysis? Evidence based on the comet assay. Mutat Res. 2002; 516: 57-61.

Peixoto F. Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation. Chemosphere. 2005; 61: 1115-1122.

Peterson RKD, Hulting AG. A comparative ecological risk assessment for herbicides used on spring wheat: the effect of glyphosate when used within a glyphosate-tolerant wheat system. Weed Science. 2004; 52: 834-844.

Powell MD, Wright GM, Burka JF. Morphological and distributional changes in the eosinophilic granule cell (EGC) population of the rainbow trout (Oncorhynchus mykiss walbaum) intestine following systemic administration of capsaicin and substance P. J Exp Zool. 1993; 266: 19-30.

Press CM, Evensen Ø. The morphology of the immune system in teleost fishes. Fish Shellfish Immun. 1999; 9: 309-318.

Prykhozhij SV, Berman JN. The progress and promise of zebrafish as a model to study mast cells. Dev Comp Immunol. 2014; 46: 74-83.

Ramirez-Duarte WF, Rondon-Barragan IS, Eslava-Mocha PR. Acute toxicity and histopathological alterations of Roundup® herbicide on "cachama blanca" (Piaractus brachypomus). Pesq Vet Bras. 2008; 28(11): 547-554.

Ramírez DW, Rondón BI, Vidal BH, Eslava MP. Toxicidad aguda y lesiones histopatológicas en cachama blanca (Piaractus brachypomus) expuestas a la mezcla de herbicida Roundup® más surfactante Cosmoflux® 411f. Revista MVZ Córdoba. 2009; 14: 1563-1575.

Reber LL, Marichal T, Galli SJ. New models for analyzing mast cell functions in vivo. Trends Immuno. 2012; 33: 613-625.

Rehen SK, Mcconnell MJ, Kaushal D, Kingsbury MA, Yang AH, Chun J. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proceedings of the National Academy of Sciences. 2001; 98: 13361-13366.

Reite OB. The mast cell nature of granule cells in the digestive tract of the pike, Esox lucius: similarity to mammalian mucosal mast cells and globule leucocytes. Fish Shellfish Immun. 1996; 6: 363-369.

Reite OB. Mast cells/eosinophilic granule cells of salmonids: staining properties and responses to noxious agents. Fish Shellfish Immun. 1997; 7: 567-584.

Reite OB. Mast cells/eosinophilic granule cells of teleostean fish: a review focusing on staining properties and functional responses. Fish Shellfish Immun. 1998; 8: 489-513.

Reite OB. The rodlet cells of teleostean fish: their potential role in host defence in relation to the role of mast cells/eosinophilic granule cells. Fish Shellfish Immun. 2005; 19: 253-267.

Reite OB, Evensen Ø. Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immun. 2006; 20: 192-208.

Relyea RA. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl. 2005; 15: 618-627.

Roberts RJ, Young H, Milne JA. Studies on the skin of plaice (Pleuronectes platessa L.). J Fish Biol. 1972; 4: 87-98.

Rodriguez B, Almeida F. 2005. Guia De Herbicidas, Londrina, Uel Editora.

Rombout JHWM, Abelli L, Picchietti S, Scapigliati G, Kiron V. Teleost intestinal immunology. Fish Shellfish Immun. 2011; 31(5): 616-626.

Rondón Barragán I, Pardo Hernández D, Eslava Mocha P. Efecto de los herbicidas sobre el sistema inmune: una aproximación en peces. RCCV. 2010; 4(1): 1-22.

Salbego J, Pretto A, Gioda CR, De Menezes CC, Lazzari R, Radunz Neto J, Baldisserotto B, Loro VL. Herbicide formulation with glyphosate affects growth, acetylcholinesterase activity, and metabolic and hematological parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol. 2010; 58: 740-745.

Salerno G, Parrinello N, Roch P, Cammarata M. cDNA sequence and tissue expression of an antimicrobial peptide, dicentracin; a new component of the moronecidin family isolated from head kidney leukocytes of sea bass, Dicentrarchus labrax. Comp Biochem Physiol B Biochem Mol Biol. 2007; 146: 521-529.

Secombes C, Cunningham C. Cytokines: an evolutionary perspective: Forward. Dev Comp Immunol. 2004; 28: 373-374.

Secombes CJ, Wang T, Hong S, Peddie S, Crampe M, Laing KJ, Cunningham C, Zou J. Cytokines and innate immunity of fish. Dev Comp Immunol. 2001; 25: 713-723.

Sfacteria A, Brines M, Blank U. The mast cell plays a central role in the immune system of teleost fish. Mol Immunol. 2015; 63: 3-8.

Shiogiri NS, Paulino MG, Carraschi SP, Baraldi FG, Da Cruz C, Fernandes MN. Acute exposure of a glyphosate-based herbicide affects the gills and liver of the Neotropical fish, Piaractus mesopotamicus. Environ Toxicol Pharmacol. 2012; 34: 388-396.

Silphaduang U, Noga EJ. Antimicrobials: Peptide antibiotics in mast cells of fish. Nature. 2001; 414: 268-269.

Silver R, Curley JP. Mast cells on the mind: new insights and opportunities. Trends Neurosci. 2013; 36: 513-521.

Sitjà-Bobadilla A, Peña-Llopis S, Gómez-Requeni P, Médale F, Kaushik S, Pérez-Sánchez J. Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture. 2005; 249: 387-400.

Sivikova K, Dianovsky J. Cytogenetic effect of technical glyphosate on cultivated bovine peripheral lymphocytes. Int J Hyg Environ Health. 2006; 209: 15-20.

Solomon KR, Dalhoff K, Volz D, Van Der Kraak G. 2013. 7 - Effects Of Herbicides On Fish. In: Keith B. Tierney, A. P. F. & Colin, J. B. (eds.) Fish Physiology. Academic Press.

Sparling DW, Matson C, Bickham J, Doelling-Brown P. Toxicity of glyphosate as Glypro and LI700 to red-eared slider (trachemys scripta elegans) embryos and early hatchlings. Environ Toxicol Chem. 2006; 25: 2768-2774.

Sperstad SV, Haug T, Blencke HM, Styrvold OB, Li C, Stensvag K. Antimicrobial peptides from marine invertebrates: challenges and perspectives in marine antimicrobial peptide discovery. Biotechnol Adv, 2011; 29: 519-530.

Sutterlin A, Sutterlin N, Rand S. 1971. The Influence of Synthetic Surfactants on the Functional Properties of the Olfactory Epithelium of Atlantic Salmon. In: CANADA, F. R. B. O. (ed.). Thechnical Report No. 287. p.p. 2-8.

Szarek J, Siwicki A, Andrzejewska A, Terech-Majewska E, Banaszkiewicz T. Effects of the herbicide Roundup on the ultrastructural pattern of hepatocytes in carp (Cyprinus carpio). Mar Environ Res. 2000; 50: 263-566.

Teh SJ, Adams SM, Hinton DE. Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquatic Toxicol. 1997; 37: 51-70.

Tierney KB, Baldwin DH, Hara TJ, Ross PS, Scholz NL, Kennedy CJ. Olfactory toxicity in fishes. Aquat Toxicol. 2010; 96: 2-26.

Tierney KB, Singh CR, Ross PS, Kennedy CJ. Relating olfactory neurotoxicity to altered olfactory-mediated behaviors in rainbow trout exposed to three currently-used pesticides. Aquat Toxicol. 2007; 81: 55-64.

Truta E, Vochita G, Rosu CM, Zamfirache MM, Olteanu Z. Evaluation of Roundup-induced toxicity on genetic material and on length growth of barley seedlings. Acta Biol Hung. 2011; 62: 290-301.

Tsui MT, Wang WX, Chu LM. Influence of glyphosate and its formulation (Roundup) on the toxicity and bioavailability of metals to Ceriodaphnia dubia. Environ Pollut. 2005; 138: 59-68.

Valdez Domingos FX, Azevedo M, Silva MD, Randi MAF, Freire CA, Silva De Assis HC, Oliveira Ribeiro CA. Multibiomarker assessment of three Brazilian estuaries using oysters as bioindicators. Environ Res. 2007; 105: 350-363.

Vallejo AN Jr, Ellis AE. Ultrastructural study of the response of eosinophil granule cells to Aeromonas salmonicida extracellular products and histamine liberators in rainbow trout Salmo gairdneri Richardson. Dev Comp Immunol. 1989; 13: 133-148.

Van Der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol. 2003; 13: 57-149.

Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A. The use of biomarkers in biomonitoring: A 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol C Toxicol Pharmacol. 2007; 146: 281-300.

Vieira CED, Almeida MDS, Galindo BA, Pereira L, Martinez CBDR. Integrated biomarker response index using a Neotropical fish to assess the water quality in agricultural areas. Neotrop Ichthyol. 2014; 12: 153-164.

Vigil JG, Ruiz MMDC, Anacabe DO. 2004. Solid herbicidal formulation of n-(phosphono-methyl)glycine and process for its preparation. United States patent application. US 2004/0102323 A1.

Wang YS, Jaw CG, Chen YL. Accumulation of 2,4-D and glyphosate in fish and water hyacinth. Water Air Soil Pollut. 1994; 74: 397-403.

Williams GM, Kroes R, Munro IC. Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans. Regul Toxicol Pharmacol. 2000; 31: 117-165.

Williams RM, Bienenstock J, Stead RH. Mast cells: the neuroimmune connection. Chem Immunol. 1995; 61: 208-235.

Yin ZX, He W, Chen WJ, Yan JH, Yang JN, Chan SM, He JG. Cloning, expression and antimicrobial activity of an antimicrobial peptide, epinecidin-1, from the orange-spotted grouper, Epinephelus coioides. Aquaculture. 2006; 253: 204-211.

Zaccone G. Histochemical studies of epithelial mucosubstances, respiratory and pentose shunt enzymes in the skin epidermis of the air-breathing fish Mastacembelus erythrotaenia (Mastacembelidae, Pisces). Gegenbaurs Morphol Jahrb. 1982; 128: 918-931.

Zhou Q, Zhang J, Fu J, Shi J, Jiang G. Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta. 2008; 606: 135-150.

Zou J, Mercier C, Koussounadis A, Secombes C. Discovery of multiple beta-defensin like homologues in teleost fish. Mol Immunol. 2007; 44: 638-647.

Zúñiga G. 2001. Sistemas de detección de daño genético, Universidad de Guadalajara.

Zupanc GKH. Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A. 2006; 192: 649-670.

Artículos más leídos del mismo autor/a