New developments on gill innervation: Insights from a model vertebrate

Journal of Experimental Biology

Volumn 211, Issue 15, 2008, Pages 2371-2378

  Jonz, Michael G ^a   Nurse, Colin A ^b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Gill; Innervation; Ion regulation; Mitochondria rich cell; MRC; NEC; Neuroepithelial cell; Oxygen sensing; Pseudobranch; Zebrafish

Indexed keywords

OXYGEN;

ANIMAL; ANOXIA; BIOLOGICAL MODEL; BLOOD; BRANCHIAL ARCH; GILL; INNERVATION; METABOLISM; NOTE; PHYSIOLOGY; ZEBRA FISH;

ANIMALS; ANOXIA; BRANCHIAL REGION; GILLS; MODELS, BIOLOGICAL; OXYGEN; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 50649083715     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.010587     Document Type: Note

References (70)

1. Adriaensen, D. and Scheuermann, D. W. (1993) Neuroendocrine cells and nerves of the lung. Anat. Rec. 236, 70-85.
2. Bailly, Y., Dunel-Erb, S., Geffard, M. and Laurent, P. (1989). The vascular and epithelial serotonergic innervation ol the actinopterygian gill filament with special reference to the trout, Salmo gairdneri. Cell Tissue Res. 258, 349-363.
3. Bailly, Y., Dunel-Erb, S. and Laurent, P. (1992). The neuroepithelial cells of the fish gill filament: indolamine-immunocytochemistry and innervation. Anat. Rec. 233, 143-161.
4. Booth, J. H. (1978). The distribution of blood flow in the gills of fish: application of a new technique to rainbow trout (Salmo gairdneri). J. Exp. Biol. 73, 119-129.
5. Booth, J. H. (1979). The effects of oxygen supply, epinephrine, and acetylcholine on the distribution of blood flow in trout gills. J. Exp. Biol. 83, 31-39.
6. Bridges, C. R., Berenbrink, M., Müller, R. and Waser, W. (1998). Physiology and biochemistry of the pseudobranch: an unanswered question? Comp. Biochem. Physiol. 119A, 67-77.
7. Buckley, K. and Kelly, R. B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J. Cell Biol. 100, 1284-1294.
8. Burleson, M. L. and Milsom, W. K. (1993). Sensory receptors in the first gill arch of rainbow trout. Respir. Physiol. 93, 97-110.
9. Burleson, M. L. and Milsom, W. K. (1995a). Cardio-ventilatory control in rainbow trout: I. Pharmacology of branchial, oxygen-sensitive chemoreceptors. Respir. Physiol. 100, 231-238.
10. Burleson, M. L. and Milsom, W. K. (1995b). Cardio-ventilatory control in rainbow trout: II. Reflex effects of exogenous neurochemicals. Respir. Physiol. 101, 289-299.
11. 2 chemoreception: anatomy, physiology, and environmental adaptations. In Oxygen Sensing: Responses and Adaptation to Hypoxia, (ed. S. Lahiri, G. L. Semenza and N. R. Prabhakar), pp. 685-707. New York: Marcel Dekker.
12. 2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus). Brain Res. 1092, 100-107.
13. Campanuccl, V. A. and Nurse, C. A. (2007). Autonomic innervation of the carotid body: role of efferent inhibition. Respir. Physiol. Neuroblol. 157, 83-92.
14. Coolldge, E. H., Cluhandu, C. S. and Milsom, W. K. (2008). A comparative analysis of putative oxygen-sensing cells in the fish gill. J. Exp. Biol. 211, 1231-1242.
15. Cutz, E. and Jackson, A. (1999). Neuroepithelial bodies as airway oxygen sensors. Respir. Physiol. 115, 201-214.
16. DiBona, G. F. and Kopp, U. C. (1997). Neural control of renal function. Physiol. Rev. 77, 75-197.
17. Donald, J. A. (1984). Adrenergic innervation of the gills of brown and rainbow trout, Salmo trutta and S. gaidneri. J. Morphol. 182, 307-316.
18. Donald, J. A. (1987). Comparative study of the adrenergic innervation of the teleost gill. J. Morphol. 193, 63-73.
19. 45Ca influx into the gills of rainbow trout, Salmo gairdneri. J. Exp. Biol. 141, 441-445.
20. Dunel-Erb, S., Bailly, Y. and Laurent, P. (1982). Neuroepithelial cells in fish gill primary lamellae. J. Appl. Physiol. 53, 1342-1353.
21. Dunel-Erb, S., Bailly, Y. and Laurent, P. (1989). Neurons controlling the gill vasculature in five species of teleosts. Cell Tissue Res. 255, 567-573.
22. Evans, D. H. (2002). Cell signaling and ion transport across the fish gill epithelium. J. Exp. Zool. 293, 336-347.
23. Evans, D. H., Piermarini, P. M. and Potts, W. T. W. (1999). Ionic transport in the fish gill epithelium. J. Exp. Zool. 283, 641-652.
24. Evans, D. H., Rose, R. E., Roeser, J. M., Stidham, J. D. (2004). NaCl transport across the opercular epithelium of Fundulus heteroclitus is inhibited by an endothelin to NO, superoxide, and prostanoid signalling axis. Am. J. Physiol. Reg. Integr. Comp. Physiol. 286, R560-R568.
25. Evans, D. H., Plermarini, P. M. and Choe, K. P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev. 85, 97-177.
26. Fujita, T. (1989). Present status of paraneuron concept. Arch. Histol. Cytol. 52 (Suppl.), 1-8.
27. González, C., Almaraz, L., Obeso, A. and Rigual, R. (1994). Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol. Rev. 74, 829-898.
28. Heasman, J. (2002). Morpholino oligos: making sense of antisense? Dev. Biol. 243, 209-214.
29. Jonz, M. G. and Nurse, C. A. (2003). Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. J. Comp. Neurol. 461, 1-17.
30. Jonz, M. G. and Nurse, C. A. (2005). Development of oxygen sensing in the gills of zebrafish. J. Exp. Biol. 208, 1537-1549.
31. Jonz, M. G. and Nurse, C. A. (2006). Epithelial mitochondria-rich cells and associated innervation in adult and developing zebrafish. J. Comp. Neurol. 497, 817-832.
32. Jonz, M. G., Fearon, I. M. and Nurse, C. A. (2004). Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J. Physiol. 560, 737-752.
33. Kern, G., Bösch, S. T., Unterhuber, E. and Pelster, B. (2002). Mechanisms of acid secretion in pseudobranch cells of rainbow trout Oncorhynchus mykiss. J. Exp. Biol. 205, 2943-2954.
34. Lahiri, S., Roy, A., Baby, S. M., Hoshi, T., Semenza, G. L., Prabhakar, N. R. (2006). Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 91, 249-286.
35. Laurent, P. and Dunel-Erb, S. (1984). The pseudobranch: morphology and function. In Fish Physiology. Vol. 10, part B (ed. W. S. Hoar and D. J. Randall), pp. 285-323. San Diego: Academic Press.
36. + ions. Respir. Physiol. 14, 307-331.
37. López-Barneo, J., Pardal, R. and Ortega-Sáenz, P. (2001). Cellular mechanisms of oxygen sensing. Annu. Rev. Physiol. 63, 259-287.
38. 2+ transport by fish gills: retrospective review and prospective synthesis. J. Exp. Zool. 293, 264-283.
39. Marshall, W. S. (2003). Rapid regulation of NaCl secretion by estaurine teleost fish: coping strategies for short-duration freshwater exposures. Biochim. Biophys. Acta 1618, 95-105.
40. 2-adrenergic receptors and inositol 1,4,5-triphosphate. J. Exp. Biol. 201, 1959-1965.
41. Marshall, W. S., Ossum, C. G. and Hoffmann, E. K. (2005). Hypotonic shock mediation by p38 MAPK. JNK, PKC, FAK, OSR1 and SPAK in osmosensing chloride secreting cells of killifish opercular epithelium. J. Exp. Biol. 208, 1063-1077.
42. Mayer-Gostan, N. and 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.
43. McCormick, S. D. (2001). Endocrine control of osmoregulation in teleost fish. Am. Zool. 41, 781-794.
44. Milsom, W. K. and Burleson, M. L. (2007). Peripheral arterial chemoreceptors and the evolution of the carotid body. Respir. Physiol. Neurobiol. 157, 4-11.
45. Mistry, A. C., Kato, A., Tran, Y. H., Honda, S., Tsukada, T., Takel, Y. and Hirose, S. (2004). FHL5, a novel actin-binding protein, is highly expressed in eel gill pillar cells and responds to wall tension. Am. J. Physiol.Regul. Integr. Comp. Physiol. 287, R1141-R1154.
46. Nilsson, S. (1984). Innervation and pharmacology of the gills. In Fish Physiology. Vol. 10, part A (ed. W. S. Hoar and D. J. Randall), pp. 185-227. San Diego: Academic Press.
47. Nilsson, S. and Sundin, L. (1998). Gill blood flow control. Comp. Biochem. Physiol. 119A, 137-147.
48. Nurse, C.A. (2005). Neurotransmission and neuromodulation in the chemosensory carotid body. Auton. Neurosci. 120, 1-9.
49. Olson, K. R. (2002). Vascular anatomy of the fish gill. J. Exp. Zool. 293, 214-231.
50. Pequlgnot, J. and Gas, N. (1971). Modifications histologiques de l'épithélium branchial sous l'influence de la vagotomie chez la Tanche. C. R. Séances. Soc. Biol. Fil. 165, 1172-1176.
51. Perry, S. F. (1997). The chloride cell: structure and function in the gills of freshwater fishes. Annu. Rev. Physiol. 59, 325-347.
52. 2 sensors and multiple transmitters? Exp Physiol. 91, 17-23.
53. +-ATPase activity in juvenile chinook salmon, Oncorhynchus tshawytscha: developmental changes and effects of growth hormone, cortisol and seawater transfer. Comp. Biochem. Physiol. 135A, 249-262.
54. 2 chemoreceptors mediate humoral catecholamine secretion from fish chromaffin cells. Am. J. Physiol. Reg. Integr. Comp. Physiol. 284, R990-R999.
55. 2 uptake in developing zebrafish, Danio rerio. J. Exp. Biol. 205, 1787-1794.
56. Saltys, H. A., Jonz, M. G. and Nurse, C. A. (2006). Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell Tissue Res. 323, 1-10.
57. Smith, D. G. and Chamley-Campbell, J. (1981). Localization of smooth-muscle myosin in branchial pillar cells of snapper (Chrysophys auratus) by immunofluorescence histochemistry. J. Exp. Zool. 215, 121-124.
58. Smith, M. P., Russell, M. J., Wincko, J. T. and Olson, K. R. (2001). Effects of hypoxia on isolated vessels and perfused gills of rainbow trout. Comp. Biochem. Physiol. A. 130, 171-181.
59. Stensløkken, K., Sundin, L. and Nilsson, G. E. (1999). Cardiovascular and gill microcirculatory effects of endothelin-1 in Atlantic cod: evidence for pillar cell contraction. J. Exp. Biol. 202, 1151-1157.
60. Sundin, L. and Nilsson, S. (1997). Neurochemical mechanisms behind gill microcirculatory responses to hypoxia in trout: in vivo microscopy study. Am. J. Physiol. Reg. Integr. Comp. Physiol. 41, R576-R585.
61. Sundin, L. and Nilsson, S. (2002). Branchial innervation. J. Exp. Zool. 293, 232-248.
62. Sundin, L., Nilsson, G. E., Block, M. and Löfman, O. (1995). Control of gill filament blood flow by serotonin in the rainbow trout, Oncorhynchus mykiss. Am. J. Physiol. Reg. Integr. Comp. Physiol. 268, R1224-R1229.
63. Sundin, L., Holmgren, S. and Nilsson, S. (1998a). The oxygen receptor of the teleost gill? Acta Zool. 79, 207-214.
64. 2 receptors in the gill vasculature of the Antarctic fish Pagothenia borchgrevinki. J. Exp. Biol. 201, 2129-2138.
65. Trevarrow, B., Marks, D. L. and Kimmel, C. B. (1990). Organization of hindbrain segments in the zebrafish embryo. Neuron 4, 669-679.
66. Welchert, C. K. (1967). Elements of Chordate Anatomy. New York: McGraw-Hill.
67. Wilson, J. M. and Laurent, P. (2002). Fish gill morphology: inside out. J. Exp. Zool. 293, 192-213.
68. Zaccone, G., Fasulo, S. and Ainls, L. (1994). Distribution patterns of the paraneuronal endocrine cells in the skin, gills and the airways of fishes as determined by immunohistochemical and histological methods. Histochem. J. 26, 609-629.
69. Zaccone, G., Fasulo, S., Ainis, L. and Licata, A. (1997). Paraneurons in the gills and airways of fishes. Microsc. Res. Tech. 37, 4-12.
70. Zaccone, G., Mauceri, A. and Fasulo, S. (2006). Neuropeptides and nitric oxide synthase in the gill and the air-breathing organs of fishes. J. Exp. Zool. A 305, 428-439.