Effects of hypoxia-induced gill remodelling on the innervation and distribution of ionocytes in the gill of goldfish, Carassius auratus

Journal of Comparative Neurology

Volumn 522, Issue 1, 2014, Pages 118-130

  Tzaneva, Velislava ^a   Vadeboncoeur, Claudia ^a   Ting, Jaimee ^a   Perry, Steve F ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Gill epithelia; Gill remodelling; Hypoxia; ILCM

Indexed keywords

ACCLIMATIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL FATE; CELL MIGRATION; CELL RENEWAL; CELL TYPE; CELLULAR PARAMETERS; CONTROLLED STUDY; FEMALE; GILL; GOLDFISH; HYPOXIA; INTERLAMELLAR CELL MASS; ION TRANSPORT; IONOCYTE; MALE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; STEM CELL; TISSUE DISTRIBUTION;

GILL EPITHELIA; GILL REMODELLING; HYPOXIA; ILCM;

ANIMALS; ANOXIA; CELL DIFFERENTIATION; CELL MOVEMENT; FEMALE; GILLS; GOLDFISH; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; TEMPERATURE; TIME FACTORS;

EID: 84888218412     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23392     Document Type: Article

References (47)

1. Bindon S, Gilmour K, Fenwick J, Perry S. 1994. The effects of branchial chloride cell proliferation on respiratory function in the rainbow trout, Oncorhynchus mykiss. J Exp Biol 197:47-63.
2. Bradshaw JC, Kumai Y, Perry SF. 2012. The effects of gill remodeling on transepithelial sodium fluxes and the distribution of presumptive sodium-transporting ionocytes in goldfish (Carassius auratus). J Comp Physiol B 182:351-366.
3. Chang IC, Lee TH, Yang CH, Wei YY, Chou FI, Hwang PP. 2001. Morphology and function of gill mitochondria-rich cells in fish acclimated to different environments. Physiol Biochem Zool 74:111-119.
4. Degnan KJ, Karnaky KJ Jr, Zadunaisky JA. 1977. Active chloride transport in the in vitro opercular skin of a teleost (Fundulus heteroclitus), a gill-like epithelium rich in chloride cells. J Physiol 271:155-191.
5. 2+ influx into the gills of rainbow trout, Salmo gairdneri. J Exp Biol 141:441.
6. Dymowska AK, Hwang PP, Goss GG. 2012. Structure and function of ionocytes in the freshwater fish gill. Respir Physiol Neurobiol 184:282-292.
7. Evans DH. 2002. Cell signaling and ion transport across the fish gill epithelium. J Exp Zool 293:336-347.
8. Fu SJ, Brauner CJ, Cao ZD, Richards JG, Peng JL, Dhillon R, Wang YX. 2011. The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (carassius auratus). J Exp Biol 214(Pt 12):2080-2088.
9. Gibbins IL, Olsson C, Holmgren S. 1995. Distribution of neurons reactive for NADPH-diaphorase in the branchial nerves of a teleost fish, Gadus morhua. Neurosci Lett 193:113-116.
10. Greco AM, Fenwick JC, Perry SF. 1996. The effects of soft-water acclimation on gill structure in the rainbow trout oncorhynchus mykiss. Cell Tissue Res 285:75-82.
11. Jonz MG, Nurse CA. 2006. Epithelial mitochondria-rich cells and associated innervation in adult and developing zebrafish. J Comp Neurol 497:817-832.
12. Jonz MG, Nurse CA. 2008. New developments on gill innervation: insights from a model vertebrate. J Exp Biol 211:2371-2378.
13. Krogh A. 1939. The active uptake of ions into cells and organisms. Proc Natl Acad Sci U S A 25:275-277.
14. Kumai Y, Perry SF. 2012. Mechanisms and regulation of na(+) uptake by freshwater fish. Respir Physiol Neurobiol 184:249-256.
15. + uptake by larval zebrafish Danio rerio in acidic and ion-poor environments. Am J Physiol Regul Integr Comp Physiol 303:R1031-R1041.
16. Lin LY, Horng JL, Kunkel JG, Hwang PP. 2006. Proton pump-rich cell secretes acid in skin of zebrafish larvae. Am J Physiol Cell Physiol 290:C371-C378.
17. Marshall WS, Bern HA. 1980. Ion transport across the isolated skin of the teleost Gillichthys mirabilis. In: Lahlou B, editor. Epithelial transport in the lower vertebrates. New York: Cambridge University Press. p. 337-350.
18. Marshall WS, Duquesnay RM, Gillis JM, Bryson SE, Liedtke CM. 1998. Neural modulation of salt secretion in teleost opercular epithelium by 2-adrenergic receptors and inositol 1, 4, 5-trisphosphate. J Exp Biol 201:1959-1965.
19. Marshall WS, Lynch EM, Cozzi RRF. 2002. Redistribution of immunofluorescence of CFTR anion channel and NKCC cotransporter in chloride cells during adaptation of the killifish Fundulus heteroclitus to sea water. J Exp Biol 205:1265-1273.
20. Matey V, Richards JG, Wang Y, Wood CM, Rogers J, Davies R, Murray BW, Chen XQ, Du J, Brauner CJ. 2008. The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. J Exp Biol 211:1063-1074.
21. Matsukawa T, Arai K, Koriyama Y, Liu Z, Kato S. 2004. Axonal regeneration of fish optic nerve after injury. Biol Pharm Bull 27:445-451.
22. Mattheij JA, Stroband HW. 1971. The effects of osmotic experiments and prolactin on the mucous cells in the skin and the ionocytes in the gills of the teleost cichlasoma biocellatum. Z Zellforsch Mikrosk Anat 121:93-101.
23. Mayer-Gostan N, Hirano T. 1976. The effects of transecting the IXth and Xth cranial nerves on hydromineral balance in the eel Anguilla anguilla. J Exp Biol 64:461-475.
24. Metcalfe WK, Myers PZ, Trevarrow B, Bass MB, Kimmel CB. 1990. Primary neurons that express the L2/HNK-1 carbohydrate in the zebrafish. Development 110:491-504.
25. Mitrovic D, Dymowska A, Nilsson GE, Perry SF. 2009. Physiological consequences of gill remodeling in goldfish (carassius auratus) during exposure to long-term hypoxia. Am J Physiol Regul Integr Comp Physiol 297:R224-R234.
26. Mitrovic D, Perry SF. 2009. The effects of thermally induced gill remodeling on ionocyte distribution and branchial chloride fluxes in goldfish (carassius auratus). J Exp Biol 212(Pt 6):843-852.
27. Nilsson GE. 1984. Innervation and pharmacology of the gills. In: Fish physiology. Hoar WS, Randall DJ, editors. Orlando: Academic Press. p.185-227.
28. Nilsson S, Sundin L. 1998. Gill blood flow control. Comp Biochem Physiol A Mol Integr Physiol 119:137-147.
29. Pequignot J, Gas N. 1971. Histologic modifications of branchial epithelium following vagotomy in the tench. C R Seances Soc Biol Fil 165:1172-1176.
30. Perry SF, Payan P, Girard JP. 1984. Adrenergic control of branchial chloride transport in the isolated perfused head of the freshwater trout (Salmo gairdneri). J Comp Physiol B Biochem Syst Environ Physiol 154:269-274.
31. Perry SF, Laurent P. 1989. Adaptational responses of rainbow trout to lowered external NaCl concentration: Contribution of the branchial chloride cell. J Exp Biol 147:147-168.
32. Perry SF, Shahsavarani A, Georgalis T, Bayaa M, Furimsky M, Thomas SL. 2003. Channels, pumps, and exchangers in the gill and kidney of freshwater fishes: Their role in ionic and acid-base regulation. J Exp Zool A Comp Exp Biol 300:53-62.
33. Pisam M, Auperin B, Prunet P, Rentier-Delrue F, Martial J, Rambourg A. 1993. Effects of prolactin on α and β chloride cells in the gill epithelium of the saltwater adapted tilapia, Oreochromis niloticus. Anat Rec 235:275-284.
34. Prunet P, Pisam M, Claireaux JP, Boeuf G, Rambourg A. 1994. Effects of growth hormone on gill chloride cells in juvenile atlantic salmon (I). Am J Physiol 266:R850-R857.
35. Saltys HA, Jonz MG, Nurse CA. 2006. Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell Tissue Res 323:1-10.
36. Sollid J, De Angelis P, Gundersen K, Nilsson GE. 2003. Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667-3673.
37. Sollid J, Weber RE, Nilsson GE. 2005. Temperature alters the respiratory surface area of crucian carp, Carassius carassius, and goldfish, Carassius auratus. J Exp Biol 208:1109-1116.
38. Sundin L, Nilsson S. 2002. Branchial innervation. J Exp Zool 293:232-248.
39. Thomas S, Fievet B, Claireaux G, Motais R. 1988. Adaptive respiratory responses of trout to acute hypoxia. I. Effects of water ionic composition on blood acid-base status response and gill morphology. Respir Physiol 74:77-89.
40. +-ATPase expression in the branchial epithelium of brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). J Exp Zool 293:106-118.
41. Tipsmark CK, Madsen SS, Borski RJ. 2004. Effect of salinity on expression of branchial ion transporters in striped bass (Morone saxatilis). J Exp Zool 301A:979-991.
42. Trevarrow B, Marks DL, Kimmel CB. 1990. Organization of hindbrain segments in the zebrafish embryo. Neuron 4:669-679.
43. Tsai J, Hwang PP. 1998. The wheat germ agglutinin binding sites and development of the mitochondria-rich cells in gills of tilapia (Oreochromis mossambicus). Fish Physiol Biochem 19:95-102.
44. Tzaneva V, Bailey S, Perry SF. 2011. The interactive effects of hypoxemia, hyperoxia and temperature on the gill morphology of goldfish (carassius auratus). Am J Physiol Regul Integr Comp Physiol.
45. Wilson JM, Laurent P, Tufts BL, Benos DJ, Donowitz M, Vogl AW, Randall DJ. 2000. NaCl uptake by the branchial epithelium in freshwater teleost fish: an immunological approach to ion-transport protein localization. J Exp Biol 203:2279-2296.
46. Zaccone G, Ainis L, Mauceri A, Lo Cascio P, Lo Giudice F, Fasulo S. 2003. NANC nerves in the respiratory air sac and branchial vasculature of the Indian catfish, Heteropneustes fossilis. Acta Histochem 105:151-163.
47. Zaccone G, Mauceri A, Fasulo S. 2006. Neuropeptides and nitric oxide synthase in the gill and the air-breathing organs of fishes. J Exp Zool A Comp Exp Biol 305:428-439.