Main Article Content
Abstract
Gentamicin is known to stimulate the production of reactive oxygen species and lead to renal damage in some groups of vertebrates through oxidative stress. The kidney regeneration of the killifish Aphanius furcatus was studied after gentamicin-induced oxidative stress. In addition, we evaluated the possible role of vitamin C as an antioxidant in the reduction of renal toxicity. A total of 24 specimens (3.5-4cm in total length) were divided into four groups: In group-I two fish specimens treated with 7.5µl of normal saline injection; in group-II, 10 specimens received 10µg/g body weight (b.w) gentamicin; in group-III, two fish were treated with totally 60µg/g b.w vitamin C; and in group-IV, 10 specimens received both 10µg/g gentamicin and 60µg/g b.w vitamin C. The kidney tissues of group-I, III and IV were sampled during the nephrotoxicity phase (i.e., 10 hours post injection (hpi) to 5 days post injection (dpi)) and kidney tissues of group-II sampled daily for 10 dpi until regeneration completed. The kidney regeneration of A. furcatus through nephron neogenesis was detected by newly formed nephron on 8 dpi, and it is completed on 10 dpi. Our histological results in gentamicin-induced oxidative stress (group-II) clearly showed that the most severe damage is occurred in the kidney tissue within 1-4 dpi. However, in the specimens that antioxidant therapy supplied with vitamin C (group-IV), damage effect of gentamicin has remarkably repressed within these days. The outcome of this study revealed that administration of vitamin C is effective in reduction of gentamicin-induced nephrotoxicity in A. furcatus. Vitamin C reduces the toxicity effect of gentamicin by reduction of free radicals and reactive oxygen species (ROS) through its antioxidant activity. Therefore, using vitamin C together with gentamicin enhances the body resistance to the stress condition and reduces the toxicity effect of gentamicin.
Keywords
Nephron neogenesis
Antioxidant
Gentamicin
Renal toxicity.
Article Details
License
The authors transfer the copyrights of their papers to the Iranian Society of Ichthyology. However, the information could be used in accordance with the Creative Commons licence (Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
How to Cite
Motamedi, M., Iranmanesh, A., & Teimori, A. (2019). Kidney regeneration in Aphanius furcatus (Teleostei: Aphaniidae) after damage induced by gentamicin and evaluation of vitamin C in toxicity reduction. Iranian Journal of Ichthyology, 6(1), 65–72. https://doi.org/10.22034/iji.v6i1.351
References
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Bhatt, V.S. 1971. Studies on the biology of some freshwater fishes. Part V. Mystus vittatus (Bloch). Journal of the Bombay Natural History Society 68(3): 556-572.
Bhuiyan, A.L. 1964. Fishes of Dacca. Asiatic Society of Pakistan. Publication 1, No.13, Dacca. 60-61.
Abdel-Naim, A.B.; Abdel-Wahab, M.H. & Attia, F.F. 1999. Protective effects of vitamin e and probucol against Gentamicin nephrotoxicity in rats. Pharmacological Research 40: 183-187.
Anbarasu, K. & Chandran, M.R. 2001. Effects of ascorbic acid on the immune response of the catfish, Mystus gulio (Hamilton), to different bacterins of Ameromonas hydrophila. Fish and Shellfish Immunology 11: 347-355.
Augusto, J.; Smith, B.; Smith, S.; Robertson, J. & Reimschuessel, R. 1996. Gentamicin-induced nephrotoxicity and nephroneogenesis in Oreochromis nilotica, a tilapian fish. Diseases of Aquatic Organisms 26: 49-58.
Baliga, R.; Ueda, N.; Walker, P.D. & Shah, S.V. 1997. Oxidant mechanisms in toxic acute renal failure American journal of kidney disease 29: 465-477.
Cormier, S.M; Neiheisel, T.W.; Racine, R.N. & Reimschuessel, R. 1995. New nephron development in fish from polluted waters: A possible biomarker. Ecotoxicology 4: 157-168.
Durve, V.S. & Lovell, R.T. 1982. Vitamin C and disease resistance in channel catfish (Ictalurus punctatus). Canadian Journal of Fish and Aquatic Science 39: 948-951.
Halver, J.E.; Ashley, L.M. & Smith, R.E. 1969. Ascorbic acid requirements of Coho salmon and rainbow trout. Transactions of the American Fisheries Society 98: 762-772.
Huth, M.E.; Ricci, A.J. & Cheng, A.G. 2011. Mechanisms of aminoglycoside ototoxicity and targets of hair cell protection. International Journal of Otolaryngology 937861: 1-19.
Iranmanesh, A. & Motamedi, M. 2018. Histopathological changes of hepatorenal toxicity induced by gentamicin in killifish, Aphanius hormuzensis (Aphaniidae) and its kidney regeneration through nephron neogenesis. Journal of Ichthyology 58: 932-938.
Jeffrey, W.C.; Roger, G.U.; Philip, G.L. & Clay, T.C. 1988. Acute hepatocellular effects of erythromycin, gentamicin, and trospectomycin in the perfused rat liver: Lack of correlation between lamellar body induction potency and cytotoxicity. Pharmacology Toxicology 62: 337-343.
Kamel, M.A. & Hosny Abdel Fadil, I. 2015. Prevention of hepato-renal toxicity with vitamin E, vitamin C and their combination in Gentamicin treated rats. International Journal of Pharmacology Science 5: 1289-1296.
Kovacs, E.; Savopol, T.; Iordache, M.M.; Saplacan, L.; Sobaru, I.; Istrate, C.; Mingeot-Leclercq, M.P. & Moisescu, M.G. 2012. Interaction of gentamicin polycation with model and cell membranes. Bioelectrochemistry 87: 230-235.
Montero, D.; Marrero, M.; Izquierdo, M.S.; Robaina, L.; Vergara, J.M. & Tort, L. 1999. Effect of vitamin E and C dietary supplementation on some immune parameters of gilthead seabream (Sparus aurata) juveniles subjected to crowding stress. Aquaculture 171: 269-278.
Nagai, J.; Tanaka, H.; Nakanishi, N.; Murakami, T. & Takano, M. 2001. Role of megalin in renal handling of aminoglycosides. American Journal of Physiology-Renal Physiology 281: 337-344.
Nagai, J. 2006. Molecular mechanisms underlying renal accumulation of aminoglycoside antibiotics and mechanism-based approach for developing non-nephrotoxic aminoglycoside therapy. Yakugaku Zasshi 126: 327-335.
Ortuno, J. & Esteban, M.J. 1999. Effects of high dietary intake of vitamin C on non-specific immune response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunology 9: 429-443.
Ortuno, J.; Cuesta, A.; Esteban, A. & Meseguer, J. 2001. Effect of oral administration of high vitamin C and E dosages on the gilthead seabream (Sparus aurata L.) innate immune system. Veterinary Immunology and Immunopathology 79: 167-180.
Reimschuessel, R.; Chamie, S.J. & Kinnel, M. 1996. Evaluation of gentamicin-induced nephrotoxicosis in toadfish. Journal of the American Veterinary Medical Association 209: 137-139.
Reimschuessel, R. 2001. A fish model of renal regeneration and development. Ilar Journal 42: 285-291.
Roberts, M.L.; Davies, S.J. & Pulsford, A.L. 1995. The influence of ascorbic acid (vitamin C) on non-specific immunity in the turbot (Scophthalmus maximus L.). Fish and Shellfish Immunology 5: 27-38.
Salice, C.J.; Rokous, J.S.; Kane, A.S. & Reimschuessel, R. 2001. New nephron development in goldfish (Carassius auratus) kidneys following repeated gentamicin-induced nephrotoxicosis. Comparative Medicine 51: 56-59.
Selimoglu, E. 2007. Aminoglycoside-induced ototoxicity. Current Pharmaceutical Design 13:119-126.
Teimori, A.; Esmaeili, H.R.; Erpenbeck, D. & Reichenbacher, B. 2014. A new and unique species of the genus Aphanius Nardo, 1827 (Teleostei: Cyprinodontidae) from Southern Iran: A case of regressive evolution. Zoologischer Anzeiger 253: 327-337.
Teimori, A.; Esmaeili, H.R.; Hamidan, N. & Reichenbacher, B. 2018. Systematics and historical biogeography of the Aphanius dispar species group (Teleostei: Aphaniidae) and description of a new species from Southern Iran. Journal of Zoological Systematics and Evolutionary Research 56: 579-598.
Thomas W.; Viviane V.; Peter G.; Jacques G. & Claude A. 2003. Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquaculture 225: 371-386.
Verlhac, V.; Obach, A.; Gabaudan, J.; Schuep, W. & Hole, R. 1998. Immunomodulation by dietary vitamin C and glucan in rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 8: 409-424.
Wayner, D.D.; Burton, G.W. & Ingold, K.U. 1986. The antioxidant efficiency of vitamin C is concentration-dependent. Biochimica et Biophysica Acta 884: 119-23.
Wiland, P. & Szechcinski, J. 2003. Proximal tubule damage in patients treated with gentamicin or amikacin. Poland Journal of Pharmacology 55: 631-637.
Wojciech, L. & Vincent, L.P. 2005. Ternary complexes of gentamicin with iron and lipid catalyze formation of reactive oxygen species. Chemical Research in Toxicology 18: 357-364.
Zeinali, F. & Motamedi, M. 2017. The regeneration capacity of caudal fin in the common tooth-carp, Aphanius hormuzensis (Rüppell, 1829) (Teleostei: Cyprinodontidae), International Journal of Aquatic Biology 5: 321-327.
References
Bhatt, V.S. 1971. Studies on the biology of some freshwater fishes. Part V. Mystus vittatus (Bloch). Journal of the Bombay Natural History Society 68(3): 556-572.
Bhuiyan, A.L. 1964. Fishes of Dacca. Asiatic Society of Pakistan. Publication 1, No.13, Dacca. 60-61.
Abdel-Naim, A.B.; Abdel-Wahab, M.H. & Attia, F.F. 1999. Protective effects of vitamin e and probucol against Gentamicin nephrotoxicity in rats. Pharmacological Research 40: 183-187.
Anbarasu, K. & Chandran, M.R. 2001. Effects of ascorbic acid on the immune response of the catfish, Mystus gulio (Hamilton), to different bacterins of Ameromonas hydrophila. Fish and Shellfish Immunology 11: 347-355.
Augusto, J.; Smith, B.; Smith, S.; Robertson, J. & Reimschuessel, R. 1996. Gentamicin-induced nephrotoxicity and nephroneogenesis in Oreochromis nilotica, a tilapian fish. Diseases of Aquatic Organisms 26: 49-58.
Baliga, R.; Ueda, N.; Walker, P.D. & Shah, S.V. 1997. Oxidant mechanisms in toxic acute renal failure American journal of kidney disease 29: 465-477.
Cormier, S.M; Neiheisel, T.W.; Racine, R.N. & Reimschuessel, R. 1995. New nephron development in fish from polluted waters: A possible biomarker. Ecotoxicology 4: 157-168.
Durve, V.S. & Lovell, R.T. 1982. Vitamin C and disease resistance in channel catfish (Ictalurus punctatus). Canadian Journal of Fish and Aquatic Science 39: 948-951.
Halver, J.E.; Ashley, L.M. & Smith, R.E. 1969. Ascorbic acid requirements of Coho salmon and rainbow trout. Transactions of the American Fisheries Society 98: 762-772.
Huth, M.E.; Ricci, A.J. & Cheng, A.G. 2011. Mechanisms of aminoglycoside ototoxicity and targets of hair cell protection. International Journal of Otolaryngology 937861: 1-19.
Iranmanesh, A. & Motamedi, M. 2018. Histopathological changes of hepatorenal toxicity induced by gentamicin in killifish, Aphanius hormuzensis (Aphaniidae) and its kidney regeneration through nephron neogenesis. Journal of Ichthyology 58: 932-938.
Jeffrey, W.C.; Roger, G.U.; Philip, G.L. & Clay, T.C. 1988. Acute hepatocellular effects of erythromycin, gentamicin, and trospectomycin in the perfused rat liver: Lack of correlation between lamellar body induction potency and cytotoxicity. Pharmacology Toxicology 62: 337-343.
Kamel, M.A. & Hosny Abdel Fadil, I. 2015. Prevention of hepato-renal toxicity with vitamin E, vitamin C and their combination in Gentamicin treated rats. International Journal of Pharmacology Science 5: 1289-1296.
Kovacs, E.; Savopol, T.; Iordache, M.M.; Saplacan, L.; Sobaru, I.; Istrate, C.; Mingeot-Leclercq, M.P. & Moisescu, M.G. 2012. Interaction of gentamicin polycation with model and cell membranes. Bioelectrochemistry 87: 230-235.
Montero, D.; Marrero, M.; Izquierdo, M.S.; Robaina, L.; Vergara, J.M. & Tort, L. 1999. Effect of vitamin E and C dietary supplementation on some immune parameters of gilthead seabream (Sparus aurata) juveniles subjected to crowding stress. Aquaculture 171: 269-278.
Nagai, J.; Tanaka, H.; Nakanishi, N.; Murakami, T. & Takano, M. 2001. Role of megalin in renal handling of aminoglycosides. American Journal of Physiology-Renal Physiology 281: 337-344.
Nagai, J. 2006. Molecular mechanisms underlying renal accumulation of aminoglycoside antibiotics and mechanism-based approach for developing non-nephrotoxic aminoglycoside therapy. Yakugaku Zasshi 126: 327-335.
Ortuno, J. & Esteban, M.J. 1999. Effects of high dietary intake of vitamin C on non-specific immune response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunology 9: 429-443.
Ortuno, J.; Cuesta, A.; Esteban, A. & Meseguer, J. 2001. Effect of oral administration of high vitamin C and E dosages on the gilthead seabream (Sparus aurata L.) innate immune system. Veterinary Immunology and Immunopathology 79: 167-180.
Reimschuessel, R.; Chamie, S.J. & Kinnel, M. 1996. Evaluation of gentamicin-induced nephrotoxicosis in toadfish. Journal of the American Veterinary Medical Association 209: 137-139.
Reimschuessel, R. 2001. A fish model of renal regeneration and development. Ilar Journal 42: 285-291.
Roberts, M.L.; Davies, S.J. & Pulsford, A.L. 1995. The influence of ascorbic acid (vitamin C) on non-specific immunity in the turbot (Scophthalmus maximus L.). Fish and Shellfish Immunology 5: 27-38.
Salice, C.J.; Rokous, J.S.; Kane, A.S. & Reimschuessel, R. 2001. New nephron development in goldfish (Carassius auratus) kidneys following repeated gentamicin-induced nephrotoxicosis. Comparative Medicine 51: 56-59.
Selimoglu, E. 2007. Aminoglycoside-induced ototoxicity. Current Pharmaceutical Design 13:119-126.
Teimori, A.; Esmaeili, H.R.; Erpenbeck, D. & Reichenbacher, B. 2014. A new and unique species of the genus Aphanius Nardo, 1827 (Teleostei: Cyprinodontidae) from Southern Iran: A case of regressive evolution. Zoologischer Anzeiger 253: 327-337.
Teimori, A.; Esmaeili, H.R.; Hamidan, N. & Reichenbacher, B. 2018. Systematics and historical biogeography of the Aphanius dispar species group (Teleostei: Aphaniidae) and description of a new species from Southern Iran. Journal of Zoological Systematics and Evolutionary Research 56: 579-598.
Thomas W.; Viviane V.; Peter G.; Jacques G. & Claude A. 2003. Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquaculture 225: 371-386.
Verlhac, V.; Obach, A.; Gabaudan, J.; Schuep, W. & Hole, R. 1998. Immunomodulation by dietary vitamin C and glucan in rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 8: 409-424.
Wayner, D.D.; Burton, G.W. & Ingold, K.U. 1986. The antioxidant efficiency of vitamin C is concentration-dependent. Biochimica et Biophysica Acta 884: 119-23.
Wiland, P. & Szechcinski, J. 2003. Proximal tubule damage in patients treated with gentamicin or amikacin. Poland Journal of Pharmacology 55: 631-637.
Wojciech, L. & Vincent, L.P. 2005. Ternary complexes of gentamicin with iron and lipid catalyze formation of reactive oxygen species. Chemical Research in Toxicology 18: 357-364.
Zeinali, F. & Motamedi, M. 2017. The regeneration capacity of caudal fin in the common tooth-carp, Aphanius hormuzensis (Rüppell, 1829) (Teleostei: Cyprinodontidae), International Journal of Aquatic Biology 5: 321-327.
Bhuiyan, A.L. 1964. Fishes of Dacca. Asiatic Society of Pakistan. Publication 1, No.13, Dacca. 60-61.
Abdel-Naim, A.B.; Abdel-Wahab, M.H. & Attia, F.F. 1999. Protective effects of vitamin e and probucol against Gentamicin nephrotoxicity in rats. Pharmacological Research 40: 183-187.
Anbarasu, K. & Chandran, M.R. 2001. Effects of ascorbic acid on the immune response of the catfish, Mystus gulio (Hamilton), to different bacterins of Ameromonas hydrophila. Fish and Shellfish Immunology 11: 347-355.
Augusto, J.; Smith, B.; Smith, S.; Robertson, J. & Reimschuessel, R. 1996. Gentamicin-induced nephrotoxicity and nephroneogenesis in Oreochromis nilotica, a tilapian fish. Diseases of Aquatic Organisms 26: 49-58.
Baliga, R.; Ueda, N.; Walker, P.D. & Shah, S.V. 1997. Oxidant mechanisms in toxic acute renal failure American journal of kidney disease 29: 465-477.
Cormier, S.M; Neiheisel, T.W.; Racine, R.N. & Reimschuessel, R. 1995. New nephron development in fish from polluted waters: A possible biomarker. Ecotoxicology 4: 157-168.
Durve, V.S. & Lovell, R.T. 1982. Vitamin C and disease resistance in channel catfish (Ictalurus punctatus). Canadian Journal of Fish and Aquatic Science 39: 948-951.
Halver, J.E.; Ashley, L.M. & Smith, R.E. 1969. Ascorbic acid requirements of Coho salmon and rainbow trout. Transactions of the American Fisheries Society 98: 762-772.
Huth, M.E.; Ricci, A.J. & Cheng, A.G. 2011. Mechanisms of aminoglycoside ototoxicity and targets of hair cell protection. International Journal of Otolaryngology 937861: 1-19.
Iranmanesh, A. & Motamedi, M. 2018. Histopathological changes of hepatorenal toxicity induced by gentamicin in killifish, Aphanius hormuzensis (Aphaniidae) and its kidney regeneration through nephron neogenesis. Journal of Ichthyology 58: 932-938.
Jeffrey, W.C.; Roger, G.U.; Philip, G.L. & Clay, T.C. 1988. Acute hepatocellular effects of erythromycin, gentamicin, and trospectomycin in the perfused rat liver: Lack of correlation between lamellar body induction potency and cytotoxicity. Pharmacology Toxicology 62: 337-343.
Kamel, M.A. & Hosny Abdel Fadil, I. 2015. Prevention of hepato-renal toxicity with vitamin E, vitamin C and their combination in Gentamicin treated rats. International Journal of Pharmacology Science 5: 1289-1296.
Kovacs, E.; Savopol, T.; Iordache, M.M.; Saplacan, L.; Sobaru, I.; Istrate, C.; Mingeot-Leclercq, M.P. & Moisescu, M.G. 2012. Interaction of gentamicin polycation with model and cell membranes. Bioelectrochemistry 87: 230-235.
Montero, D.; Marrero, M.; Izquierdo, M.S.; Robaina, L.; Vergara, J.M. & Tort, L. 1999. Effect of vitamin E and C dietary supplementation on some immune parameters of gilthead seabream (Sparus aurata) juveniles subjected to crowding stress. Aquaculture 171: 269-278.
Nagai, J.; Tanaka, H.; Nakanishi, N.; Murakami, T. & Takano, M. 2001. Role of megalin in renal handling of aminoglycosides. American Journal of Physiology-Renal Physiology 281: 337-344.
Nagai, J. 2006. Molecular mechanisms underlying renal accumulation of aminoglycoside antibiotics and mechanism-based approach for developing non-nephrotoxic aminoglycoside therapy. Yakugaku Zasshi 126: 327-335.
Ortuno, J. & Esteban, M.J. 1999. Effects of high dietary intake of vitamin C on non-specific immune response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunology 9: 429-443.
Ortuno, J.; Cuesta, A.; Esteban, A. & Meseguer, J. 2001. Effect of oral administration of high vitamin C and E dosages on the gilthead seabream (Sparus aurata L.) innate immune system. Veterinary Immunology and Immunopathology 79: 167-180.
Reimschuessel, R.; Chamie, S.J. & Kinnel, M. 1996. Evaluation of gentamicin-induced nephrotoxicosis in toadfish. Journal of the American Veterinary Medical Association 209: 137-139.
Reimschuessel, R. 2001. A fish model of renal regeneration and development. Ilar Journal 42: 285-291.
Roberts, M.L.; Davies, S.J. & Pulsford, A.L. 1995. The influence of ascorbic acid (vitamin C) on non-specific immunity in the turbot (Scophthalmus maximus L.). Fish and Shellfish Immunology 5: 27-38.
Salice, C.J.; Rokous, J.S.; Kane, A.S. & Reimschuessel, R. 2001. New nephron development in goldfish (Carassius auratus) kidneys following repeated gentamicin-induced nephrotoxicosis. Comparative Medicine 51: 56-59.
Selimoglu, E. 2007. Aminoglycoside-induced ototoxicity. Current Pharmaceutical Design 13:119-126.
Teimori, A.; Esmaeili, H.R.; Erpenbeck, D. & Reichenbacher, B. 2014. A new and unique species of the genus Aphanius Nardo, 1827 (Teleostei: Cyprinodontidae) from Southern Iran: A case of regressive evolution. Zoologischer Anzeiger 253: 327-337.
Teimori, A.; Esmaeili, H.R.; Hamidan, N. & Reichenbacher, B. 2018. Systematics and historical biogeography of the Aphanius dispar species group (Teleostei: Aphaniidae) and description of a new species from Southern Iran. Journal of Zoological Systematics and Evolutionary Research 56: 579-598.
Thomas W.; Viviane V.; Peter G.; Jacques G. & Claude A. 2003. Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquaculture 225: 371-386.
Verlhac, V.; Obach, A.; Gabaudan, J.; Schuep, W. & Hole, R. 1998. Immunomodulation by dietary vitamin C and glucan in rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 8: 409-424.
Wayner, D.D.; Burton, G.W. & Ingold, K.U. 1986. The antioxidant efficiency of vitamin C is concentration-dependent. Biochimica et Biophysica Acta 884: 119-23.
Wiland, P. & Szechcinski, J. 2003. Proximal tubule damage in patients treated with gentamicin or amikacin. Poland Journal of Pharmacology 55: 631-637.
Wojciech, L. & Vincent, L.P. 2005. Ternary complexes of gentamicin with iron and lipid catalyze formation of reactive oxygen species. Chemical Research in Toxicology 18: 357-364.
Zeinali, F. & Motamedi, M. 2017. The regeneration capacity of caudal fin in the common tooth-carp, Aphanius hormuzensis (Rüppell, 1829) (Teleostei: Cyprinodontidae), International Journal of Aquatic Biology 5: 321-327.