Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 1, 2009, Pages

  Mitrovic, Dejana ^a   Dymowska, Agnieszka ^b   Nilsson, Goran E ^c   Perry, Steve F ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Cl balance; Hypoxia; Interlamellar cell mass; Ion regulation; Ionocyte; Mitochondrion rich cell; Na+ K+ ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CELL MARKER; CHLORIDE; MACROGOL 4000; MESSENGER RNA;

ACCLIMATIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL STRUCTURE; CELL TYPE; CELLULAR DISTRIBUTION; CHLORIDE TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; GILL; GOLDFISH; HYPOXIA; INTERLAMELLAR CELL MASS; IONOCYTE; LONG TERM EXPOSURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANOXIA; CELL DIFFERENTIATION; CELL MOVEMENT; CHLORIDES; GILLS; GOLDFISH; ION TRANSPORT; KINETICS; PERMEABILITY; POLYETHYLENE GLYCOLS; SODIUM-POTASSIUM-EXCHANGING ATPASE; WATER-ELECTROLYTE BALANCE;

EID: 67650085013     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00189.2009     Document Type: Article

References (40)

1. Bickler PE, Buck LT. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69: 145-170, 2007. (Pubitemid 46457639)
2. + ATPase in trout hepatocytes. J Exp Biol 208: 1793-1801, 2005.
3. Bouvry D, Planes C, Malbert-Colas L, Escabasse V, Clerici C. Hypoxia-induced cytoskeleton disruption in alveolar epithelial cells. Am J Respir Cell Mol Biol 35: 519-527, 2006. (Pubitemid 44706424)
4. Burggren WW. "Air gulping" improves blood oxygen transport during aquatic hypoxia in the goldfish Carassius auratus. Physiol Zool 55: 327-334, 1982.
5. Chretien M, Pisam M. Cell renewal and differentiation in the gill epithelium of fresh- or salt-water-adapted euryhaline fish as revealed by [3H]- thymidine radioautography. Biol Cell 56: 137-150, 1986.
6. Galvez F, Reid SD, Hawkings G, Goss GG. Isolation and characterization of mitochondria-rich cell types from the gill of freshwater rainbow trout. Am J Physiol Regul Integr Comp Physiol 282: R658-R668, 2002. (Pubitemid 34665638)
7. Garcia-Romeu F, Masoni A. Sur la mise en evidence des cellules a chlorure de la branchie des poissons. Arch Anat Microsc 59: 289-294, 1970.
8. Gonzalez RJ, McDonald DG. The relationship between oxygen consumption and ion loss in a freshwater fish. J Exp Biol 163: 317-332, 1992.
9. Goss GG, Adamia S, Galvez F. Peanut lectin binds to a subpopulation of mitochondria-rich cells in the rainbow trout gill epithelium. Am J Physiol Regul Integr Comp Physiol 281: R1718-R1725, 2001. (Pubitemid 33116230)
10. Goss GG, Laurent P, Perry SF. Evidence for a morphological component in the regulation of acid-base balance in hypercapnic catfish (Ictalurus nebulosus). Cell Tiss Res 268: 539-552, 1992.
11. Hwang PP, Lee TH. New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A 148: 479-497, 2007. (Pubitemid 47484222)
12. Hyvarinen H, Holopainen IJ, Piironen J. Anaerobic wintering of crucian carp (Carassius carassius L.). I. Annual dynamics of glycogen reserves in nature. Comp Biochem Physiol A: 82: 797-803, 1985.
13. Katoh F, Kaneko T. Short-term transformation and long-term replacement of branchial chloride cells in killifish transferred from seawater to freshwater, revealed by morphofunctional observations and a newly established "time-differential double fluorescent staining" technique. J Exp Biol 206: 4113-4123, 2003.
14. - uptake in freshwater. Cell Tiss Res 325: 481-492, 2006.
15. Laurent PL, Dunel-Erb S, Chevalier C, Lignon J. Gill epithelial cell kinetics in a freshwater teleost, Oncorhynchus mykiss, during adaptation to ion-poor water and hormonal treatments. Fish Physiol Biochem 13: 353-370, 1995.
16. Marshall WS, Bryson SE, Wood CM. Calcium transport by isolated skin of rainbow trout. J Exp Biol 166: 297-316, 1992.
17. +-ATPase activity. Can J Fish Aquat Sci 50: 656-658, 1993.
18. McCormick SD, Hasegawa S, Hirano T. Calcium uptake in the skin of a freshwater teleost. Proc Natl Acad Sci USA 89: 3635-3638, 1992.
19. Mitrovic D, Perry SF. The effects of thermally induced gill remodelling on ionocyte distribution and branchial chloride fluxes in goldfish (Carassius auratus). J Exp Biol 212: 843-852, 2009.
20. Morgan JD, Iwama GK. Energy cost of NaCl transport in isolated gills of cutthroat trout. Am J Physiol 99: 631-639, 1999. (Pubitemid 29458133)
21. Nilsson GE. Long-term anoxia in crucian carp: changes in the levels of amino acid and monoamine neurotransmitters in the brain, catecholamines in chromaffin tissue, and liver glycogen. J Exp Biol 150: 295-320, 1990. (Pubitemid 20176490)
22. Nilsson GE. Gill remodeling in fish-a new fashion or an ancient secret? J Exp Biol 210: 2403-2409, 2007. (Pubitemid 47235030)
23. Nilsson GE, Renshaw GMC. Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207: 3131-3139, 2004. (Pubitemid 39275287)
24. Perry SF. The chloride cell: structure and function in the gill of freshwater fishes. Annu Rev Physiol 59: 325-347, 1997. (Pubitemid 27142445)
25. Perry SF, Goss GG, Fenwick JC. Interrelationships between gill chloride cell morphology and calcium uptake in freshwater teleosts. Fish Physiol Biochem 10: 327-337, 1992.
26. Perry SF, Goss GG, Laurent P. The interrelationships between gill chloride cell morphology and ionic uptake in four freshwater teleosts. Can J Zool 70: 1737-1742, 1992.
27. Perry SF, Shahsavarani A, Georgalis T, Bayaa M, Furimsky M, Thomas SLY. Channels, pumps and exchangers in the gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. J Exp Zool 300: 53-62, 2003. (Pubitemid 37529029)
28. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29: 2002-2007, 2001.
29. Piermarini PM, Verlander JW, Royaux IE, Evans DH. Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am J Physiol Regul Integr Comp Physiol 283: R983-R992, 2002. (Pubitemid 35056543)
30. Pisam M. Membranous systems in the chloride cell of teleostean fish gill-their modifications in response to the salinity of the environment. Anat Rec 200: 401-414, 1981. (Pubitemid 11044359)
31. Randall DJ, Baumgarten D, Malyusz M. The relationship between gas and ion transfer across the gills of fishes. Comp Biochem Physiol A 41: 629-637, 1972.
32. Sollid J, De Angelis P, Gundersen K, Nilsson GE. Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206: 3667-3673, 2003. (Pubitemid 37343070)
33. Sollid J, Nilsson GE. Plasticity of respiratory structures-adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154: 241-251, 2006. (Pubitemid 44666572)
34. Sollid J, Weber RE, Nilsson GE. Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208: 1109-1116, 2005. (Pubitemid 40526494)
35. Tresguerres M, Katoh F, Orr E, Parks SK, Goss GG. Chloride uptake and base secretion in freshwater fish: a transepithelial ion-transport metabolon? Physiol Biochem Zool 79: 981-996, 2006. (Pubitemid 44728730)
36. Vanwaversveld J, Addink ADF, Vandenthillart G. The anaerobic energy-metabolism of goldfish determined by simultaneous direct and indirect calorimetry during anoxia and hypoxia. J Comp Physiol [B] 159: 263-268, 1989.
37. Wilson JM, Laurent P, Tufts BL, Benos DJ, Donowitz M, Vogl AW, Randall DJ. NaCl uptake by the branchial epithelium in freshwater teleost fish: an immunological approach to ion-transport protein localization. J Exp Biol 203: 2279-2296, 2000. (Pubitemid 30656241)
38. + fluxes and ammonia excretion in response to acute environmental hypoxia in the Amazonian oscar, Astronotus ocellatus. Am J Physiol Regul Integr Comp Physiol 292: R2048-R2058, 2007.
39. Wu RS. Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45: 35-45, 2002.
40. Zall DM, Fisher MD, Garner QM. Photometric determination of chloride in water. Anal Chem 28: 1665-1678, 1956.