Effect of acute copper sulfate exposure on olfactory responses to amino acids and pheromones in goldfish (Carassius auratus)

Environmental Science and Technology

Volumn 43, Issue 21, 2009, Pages 8393-8399

  Kolmakov, Nikolay N ^a   Hubbard, Peter C ^a   Lopes, Orlando ^b   Canario, Adelino V M ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b UNIVERSITY OF ÉVORA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; CELL TYPES; COPPER EXPOSURE; COPPER SULFATE; L-ARGININE; L-SERINE; POST TREATMENT; RECEPTOR CELLS; TRANSDUCTION PATHWAYS;

AMINATION; AMINES; AMINO ACIDS; BODY FLUIDS; COPPER; HORMONES; ORGANIC ACIDS; SCANNING ELECTRON MICROSCOPY;

RECOVERY;

AMINO ACID; BILE ACID; CATECHOLAMINE; COPPER SULFATE; PHEROMONE DERIVATIVE;

AMINO ACID; COPPER COMPOUND; CYPRINID; MORPHOLOGY; OLFACTION; PHEROMONE; POLLUTION EXPOSURE; SCANNING ELECTRON MICROSCOPY; STEROID; SULFATE;

ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; GOLDFISH; NERVE CELL; NONHUMAN; OLFACTOMETRY; SCANNING ELECTRON MICROSCOPY; SMELLING;

ACUTE TOXICITY TESTS; AMINO ACIDS; ANIMALS; COPPER SULFATE; ENVIRONMENTAL EXPOSURE; EPITHELIUM; GOLDFISH; OLFACTORY RECEPTOR NEURONS; PHEROMONES; SMELL; TIME FACTORS;

CARASSIUS AURATUS;

EID: 70350787219     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es901166m     Document Type: Article

References (55)

1. Kotrschal, K. Taste(s) and olfaction(s) in fish: a review of specialized sub-systems and central integration. Pflügers Arch. 2000, 439 (7), r178-r180.
2. Hara, T. J. Feeding behaviour in some teleosts is triggered by single amino acids primarily through olfaction. J. Fish Biol. 2006, 68 (3), 810-825.
3. Dittman, A.; Quinn, T. Homing in Pacific salmon: mechanisms and ecological basis. J. Exp. Biol. 1996, 199 (Pt 1), 83-91. (Pubitemid 126603940)
4. Evans, R. E.; Hara, T. J. The characteristics of the electroolfactogram (EOG): Its loss and recovery following olfactory nerve section in rainbow trout (Salmo gairdneri). Brain Res. 1985, 330 (1), 65-75.
5. Masukawa, L. M.; Hedlund, B.; Shepherd, G. M. Changes in the electrical properties of olfactory epithelial cells in the tiger salamander after olfactory nerve transection. J. Neurosci. 1985, 5 (1), 136-141.
6. Wang, R. T.; Halpern, M. Neurogenesis in the vomeronasal epithelium of adult garter snakes. 2. Reconstitution of the bipolar neuron layer following experimental vomeronasal axotomy. Brain Res. 1982, 237 (1), 41-59.
7. Jennings, R. A.; Keiger, C. J. H.; Walker, J. C. Time course of reinnervation of the olfactory bulb after transection of the primary olfactory nerve in the pigeon. Brain Res. 1995, 683 (2), 159-163.
8. Graziadei, G. A.; Graziadei, P. P. Neurogenesis and neuron regeneration in the olfactory system of mammals. II Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J. Neurocytol, 1979, 8 (2), 197-213. (Pubitemid 9175213)
9. Konzelmann, S.; Saucier, D.; Strotmann, J.; Breer, H.; Astic, L. Decline and recovery of olfactory receptor expression following unilateral bulbectomy. Cell Tissue Res. 1998, 294 (3), 421-430.
10. Hansen, J. A.; Marr, J. C. A.; Lipton, J.; Cacela, D.; Bergman, H. L. Differences in neurobehavioral responses of chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss) exposed to copper and cobalt: behavioral avoidance. Environ. Toxicol. Chem. 1999, 18 (9), 1972-1978. (Pubitemid 129519805)
11. Sloman, K. A.; Scott, G. R.; Diao, Z.; Rouleau, C.; Wood, C. M.; McDonald, D. G. Cadmium affects the social behaviour of rainbow trout Oncorhynchus mykiss. Aquat. Toxicol. 2003, 65 (2), 171-185. (Pubitemid 37011310)
12. Saglio, P.; Trijasse, S. Behavioral responses to atrazine and diuron in goldfish. Arch. Environ. Contam. Toxicol. 1998, 35 (3), 484-491. (Pubitemid 28409359)
13. Boulay, N.; Edwards, M. Copper in the urban water cycle. Crit. Rev. Environ. Sci. Technol. 2000, 30 (3), 297-326.
14. Sandahl, J. F.; Baldwin, D. H.; Jenkins, J. J.; Scholz, N. L.Asensory system at the interface between urban stormwater runoff and salmon survival. Environ. Sci. Technol. 2007, 41, 2998. (Pubitemid 46626433)
15. Pyle, G. G.; Mirza, R. S. Copper-impaired chemosensory function and behavior in aquatic animals. Hum. Ecol. Risk Assess. 2007, 13 (3), 492-505.
16. Beyers, D. W.; Farmer, M. S. Effects of copper on olfaction of Colorado pikeminnow. Environ. Toxicol. Chem. 2001, 20 (4), 907-912.
17. Carreau, N. D.; Pyle, G. G. Effect of copper exposure during embryonic development on chemosensory function of juvenile fathead minnows (Pimephales promelas). Ecotoxicol. Environ. Saf. 2005, 61 (1), 1-6.
18. Niyogi, S.; Kamunde, C. N.; Wood, C. M. Food selection, growth and physiology in relation to dietary sodium chloride content in rainbow trout (Oncorhynchus mykiss) under chronic waterborne Cu exposure. Aquat. Toxicol. 2006, 77 (2), 210-221.
19. De Boeck, G.; Vlaeminck, A.; Blust, R. Effects of sublethal copper exposure on copper accumulation, food consumption, growth, energy stores, and nucleic acid content in common carp. Arch. Environ. Contam. Toxicol. 1997, 33 (4), 415-422. (Pubitemid 28027742)
20. Winberg, S.; Bjerselius, R.; Baatrup, E.; Doving, K. B. The effect of Cu (II)onthe electro-olfactogram (EOG) of the Atlantic salmon (Salmo salar L) in artificial freshwater of varying inorganic carbon concentrations. Ecotoxicol. Environ. Saf. 1992, 24 (2), 167-178.
21. Hansen, J. A.; Rose, J. D.; Jenkins, R. A.; Gerow, K. G.; Bergman, H. L. Chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss) exposed to copper: Neurophysiological and histological effects on the olfactory system. Environ. Toxicol. Chem. 1999, 18 (9), 1979-1991. (Pubitemid 129519806)
22. Baldwin, D. H.; Sandahl, J. F.; Labenia, J. S.; Scholz, N. L. Sublethal effects of copper on coho salmon: impacts of nonoverlapping receptor pathways in the peripheral olfactory nervous system. Environ. Toxicol. Chem. 2003, 22 (10), 2266-2274.
23. McIntyre, J. K.; Baldwin, D. H.; Meador, J. P.; Scholz, N. L. Chemosensory deprivation in juvenile coho salmon exposed to dissolved copper under varying water chemistry conditions. Environ. Sci. Technol. 2008, 42 (4), 1352-1358.
24. Sandahl, J. F.; Miyasaka, G.; Koide, N.; Ueda, H. Olfactory inhibition and recovery in chum salmon (Oncorhynchus keta) following copper exposure. Can. J. Fish Aquat. Sci. 2006, 63 (8), 1840-1847. (Pubitemid 44483159)
25. Sandahl, J. F.; Baldwin, D. H.; Jenkins, J. J.; Scholz, N. L. Odorevoked field potentials as indicators of sublethal neurotoxicity in juvenile coho salmon (Oncorhynchus kisutch) exposed to copper, chlorpyrifos, or esfenvalerate. Can. J. Fish Aquat. Sci. 2004, 61 (3), 404-413.
26. Starcevic, S. L.; Zielinski, B. S. Neuroprotective effects of glutathione on rainbow trout olfactory receptor neurons during exposure to copper sulfate. Comp. Biochem. Physiol., Part C: Pharmacol. Toxicol. Endocrinol. 1997, 117 (2), 211-219.
27. Moran, D. T.; Rowley, J. C.; Aiken, G. R.; Jafek, B. W. Ultrastructural neurobiology of the olfactory mucosa of the brown trout Salmo trutta. Microsc. Res. Technol. 1992, 23 (1), 28-48.
28. Julliard, A. K.; Saucier, D.; Astic, L. Effects of chronic low-level copper exposure on ultrastructure of the olfactory system in rainbow trout (Oncorhynchus mykiss). Histol. Histopathol. 1993, 8 (4), 655-672. (Pubitemid 23351627)
29. Julliard, A. K.; Saucier, D.; Astic, L. Time-course of apoptosis in the olfactory epithelium of rainbow trout exposed to a low copper level. Tissue Cell 1996, 28 (3), 367-377. (Pubitemid 26192655)
30. Saucier, D.; Astic, L. Morphofunctional alterations in the olfactory system of rainbow trout (Oncorhynchus mykiss) and possible acclimation in response to long-lasting exposure to low copper levels. Comp. Biochem. Physiol., Part A: Physiol. 1995, 112 (2), 273-284.
31. Julliard, A. K.; Saucier, D.; Astic, L. Metal X-Ray microanalysis in the olfactory system of rainbow trout exposed to low level of copper. Biol. Cell 1995, 83 (1), 77-86.
32. NelsonJ. S. Fishes of the World, 4th ed.; John Wiley & Sons: New York, 2006; p 624.
33. Stacey, N.; Chojnacki, A.; Narayanan, A.; Cole, T.; Murphy, C. Hormonally derived sex pheromones in fish: Exogenous cues and signals from gonad to brain. Can. J. Physiol. Pharmacol. 2003, 81 (4), 329-341. (Pubitemid 36683404)
34. Byankin, A. G. Biomonitoring water environment using olfactory organ of fishes. 2003, 6, 1186-1208.
35. Zippel, H. P.; Hansen, A.; Caprio, J. Renewing olfactory receptor neurons in goldfish do not require contact with the olfactory bulb to develop normal chemical responsiveness. J. Comp. Physiol., A 1997, 181 (5), 425-437.
36. Zippel, H. P.; Sorensen, P. W.; Hansen, A. High correlation between microvillous olfactory receptor cell abundance and sensitivity to pheromones in olfactory nerve-sectioned goldfish. J. Comp. Physiol., A 1997, 180 (1), 39-52.
37. Rolen, S. H.; Sorensen, P. W.; Mattson, D.; Caprio, J. Polyamines as olfactory stimuli in the goldfish Carassius auratus. J. Exp. Biol. 2003, 206 (Pt 10), 1683-1696. (Pubitemid 36599394)
38. Hubbard, P. C.; Barata, E. N.; Canario, A. V. M. Olfactory sensitivity to catecholamines and their metabolites in the goldfish. Chem. Senses 2003, 28 (3), 207-218.
39. Sorensen, P.; Hara, T.; Stacey, N.; Goetz, F. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 1988, 39 (5), 1039-1150.
40. Sorensen, P. W.; Scott, A. P.; Stacey, N. E.; Bowdin, L. Sulfated 17,20β-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen. Comp. Endrocrinol. 1995, 100 (1), 128-142.
41. Sorensen, P. W.; Hara, T. J.; Stacey, N. E. Extreme olfactory sensitivity of mature and gonadally-regressed goldfish to a potent steroidal pheromone, 17α,20β-dihydroxy-4-pregnen-3-one. J Comp. Physiol. 1987, 16A, 305-313.
42. Hubbard, P. C.; Barata, E. N.; Canario, A. V.M.Possible disruption of pheromonal communication by humic acid in the goldfish Carassius auratus. Aquat. Toxicol. 2002, 60 (3-4), 169-183.
43. De Boeck, G.; Meeus, W.; De Coen, W.; Blust, R. Tissue-specific Cu bioaccumulation patterns and differences in sensitivity to waterborne Cu in three freshwater fish: rainbow trout (Oncorhynchus mykiss), common carp (Cyprinus carpio), and gibel carp (Carassius auratus gibelio). Aquat. Toxicol. 2004, 70 (3), 179-188. (Pubitemid 39506828)
44. Hansen, A.; Zippel, H. P.; Sorensen, P. W.; Caprio, J. Ultrastructure of the olfactory epithelium in intact, axotomized, and bulbectomized goldfish Carassius auratus. Microsc. Res. Tech. 1999, 45 (4-5), 325-338. (Pubitemid 29264996)
45. Nair, A. V.; Mazzolini, M.; Codega, P.; Giorgetti, A.; Torre, V. LockingCNGA1channels in the open and closed state. Biophys. J. 2006, 90 (10), 3599-3607.
46. Gao, X. L.; Du, Z. Y.; Patel, T. B. Copper and zinc inhibit G alpha(s) function. J. Biol. Chem. 2005, 280 (4), 2579-2586.
47. Susankova, K.; Tousova, K.; Vyklicky, L.; Teisinger, J.; Vlachova, V. Reducing and oxidizing agents sensitize heat-activated vanilloid receptor (TRPV1) current. Mol. Pharmacol. 2006, 70 (1), 383-394.
48. Sato, Y.; Miyasaka, N.; Yoshihara, Y. Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. J. Neurosci. 2005, 25 (20), 4889-4897. (Pubitemid 40712832)
49. Kolmakov, N. N.; Kube, M.; Reinhardt, R.; Canario, A. V. Analysis of the goldfish Carassius auratus olfactory epithelium transcriptome reveals the presence of numerous non-olfactory GPCR and putative receptors for progestin pheromones. BMC Genomics 2008, 9, 429.
50. Mangos, S.; Liu, Y.; Drummond, I. A. Dynamic expression of the osmosensory channel trpv4 in multiple developing organs in zebrafish. Gene Expression Patterns 2007, 7 (4), 480-484.
51. Keller, J. N.; Hanni, K. B.; Markesbery, W. R. Oxidized low-density lipoprotein induces neuronal death. Implications for calcium, reactive oxygen species, and caspases. J. Neurochem. 1999, 72 (6), 2601-2609.
52. Chen, T. G.; Chen, T. L.; Chang, H. C.; Tai, Y. T.; Cherng, Y. G.; Chang, Y. T.; Chen, R. M. Oxidized low-density lipoprotein induces apoptotic insults to mouse cerebral endothelial cells via a Bax-mitochondria-caspase protease pathway. Toxicol. Appl. Pharmacol. 2007, 219 (1), 42-53.
53. Hansen, A.; Rolen, S. H.; Anderson, K.; Morita, Y.; Caprio, J.; Finger, T. E. Correlation between olfactory receptor cell type and function in the channel catfish. J. Neurosci. 2003, 23 (28), 9328-9339. (Pubitemid 37323032)
54. Tilton, F.; Tilton, S. C.; Bammler, T. K.; Beyer, R.; Farin, F.; Stapleton, P. L.; Gallagher, E. P. Transcriptional biomarkers and mechanisms of copper-induced olfactory injury in zebrafish. Environ. Sci. Technol. 2008, 42 (24), 9404-9411.
55. Nikonov, A. A.; Caprio, J. Electrophysiological evidence for a chemotopy of biologically relevant odors in the olfactory bulb of the channel catfish. J. Neurophysiol. 2001, 86 (4), 1869-1876. (Pubitemid 32953234)