The early ontogeny of neuronal nitric oxide synthase systems in the zebrafish

Journal of Experimental Biology

Volumn 207, Issue 6, 2004, Pages 923-935

  Holmqvist, B ^a   Ellingsen, B ^a   Forsell, J ^a   Zhdanova, I ^b   Alm, P ^a  

^a LUND UNIVERSITY   (Sweden)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain; Danio rerio; Development; Gut; Hybridisation; In situ; Intestine; Morphogenesis; Neuronal differentiation; Regeneration; Retina; Zebrafish

Indexed keywords

CYCLIC GMP; MESSENGER RNA; NITRIC OXIDE SYNTHASE;

ANIMAL; ARTICLE; BIOSYNTHESIS; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; NERVOUS SYSTEM; PRENATAL DEVELOPMENT; RADIOIMMUNOASSAY; TIME; ZEBRA FISH;

ANIMALS; CYCLIC GMP; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; NERVOUS SYSTEM; NITRIC OXIDE SYNTHASE; RADIOIMMUNOASSAY; RNA, MESSENGER; TIME FACTORS; ZEBRAFISH;

ANIMALIA; DANIO; DANIO RERIO; VERTEBRATA;

EID: 1642358516     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00845     Document Type: Article

References (82)

1. Alderton, W. K., Cooper, C. E. and Knowles, R. G. (2001). Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593-615.
2. Angotzi, A. R., Hirano, J., Vallerga, S. and Djamgoz, M. B. A. (2002). Role of nitric oxide in control of light adaptive cone photomechanical movements in retinas of lower vertebrates: a comparative study. Nitric Oxide 6, 200-204.
3. Bogdan, C. (2001). Nitric oxide and regulation of gene expression. Trends Cell Biol. 11, 66-75.
4. Bredt, D. S. and Snyder, S. H. (1994). Nitric oxide: A physiologic messenger molecule. Annu. Rev. Biochem. 63, 175-195.
5. Brüning, G., Hattwig, K. and Mayer, B. (1996). Nitric oxide synthase in the peripheral nervous system of the goldfish, Carassius auratus. Cell Tiss. Res. 284, 87-98.
6. Chitnis, A. B. and Kuwada, J. Y. (1990). Axogenesis in the brain of zebrafish embryos. J. Neurosci. 10, 1892-1905.
7. Cox, R. L., Mariano, T., Heck, D. E., Laskin, J. D. and Stegeman, J. J. (2001). Nitric oxide synthase sequences in the marine fish Stenotomus chrysops and the sea urchin Arbacia punctulata, and phylogenetic analysis of nitric oxide synthase calmodulin-binding domains. Comp. Biochem. Physiol. Biochem. Mol. Biol. 130, 479-491.
8. Denninger, J. W. and Marletta, M. A. (1999). Guanylate cyclase and the NO/cGMP signaling pathway. Biochim. Biophys. Acta 1411, 334-350.
9. Derer, P. and Derer, M. (1993). Ontogenesis of NADPH-diaphorase neurons in the mouse forebrain. Neurosci. Lett. 152, 21-24.
10. Devadas, M., Liu, Z., Kaneda, M., Arai, K., Matsukawa, T. and Kato, S. (2001). Changes in NADPH diaphorase expression in the fish visual system during optic nerve regeneration and retinal development. Neurosci. Res. 40, 359-365.
11. Dippel, E., Mayer, B., Schonfelder, G., Czarnetski, B. M. and Paus, R. (1994). Distribution of constitutive nitric oxide synthase immunoreactivity and NADPH-diaphorase activity in murine telogen and anagen skin. J. Invest. Dermatol. 103, 112-115.
12. Doldan, M., Prego, B., Holmqvist, B. and Miguel, E. (1999). Distribution of GABA-immunolabelling in the brain of early zebrafish (Danio rerio). E. J. Morphol. 37, 64-67.
13. Downen, M., Zhao, M. L., Lee, P., Weidenheim, K. M., Dickson, D. W. and Lee, S. C. (1999). Neuronal nitric oxide synthase expression in developing and adult human CNS. J. Neuropathol. Exp. Neurol. 58, 12-21.
14. Ekström, P., Johnsson, C.-M. and Ohlin, L.-M. (2001). Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration (secondary matrix) zones. J. Comp. Neurol. 436, 92-110.
15. Ellingsen, B., Fjose, A., Edvardsson, K. and Holmqvist, B. (1998). Neuronal differentiation and transmitter expression in the forebrain of embryonic zebrafish. Soc. Neurosci. Abstr. 24 B, 607.1.
16. Eliasson, M. J. L., Blackshaw, S., Schnell, M. J. and Snyder, S. H. (1997). Neuronal nitric oxide synthase alternatevily spliced forms: Prominent functional localizations in the brain. Proc. Natl. Acad. Sci. USA 94, 3396-3401.
17. Enikolopov, G., Banerji, J. and Kusin, B. (1999). Nitric oxide and Drosophila development. Cell Death Diff. 6, 957-963.
18. Fritsche, R., Schwerte, T. and Peltser, B. (2000). Nitric oxide and vascular reactivity in developing zebrafish, Danio rerio. Am. J. Physiol. Reg. Int. Comp. Physiol. 279, 2200-2207.
19. Gibbs, S. M., Ngai, J., Ekker, S. and McLoon, S. C. (2001). Regulation of ventral spinal cord development in zebrafish by nitric oxide and cyclic GMP. Soc. Neurosci. Abstr. 27, 360.14.
20. Gibbs, S. M. and Truman, J. W. (2000). Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe in Drosophila. Curr. Biol. 10, 459-462.
21. Gibbs, S. M., Becker, A., Hardy, R. W. and Truman, J. (2001). Soluble guanylate cyclase is required during development for visual system function in Drosophila. J. Neurosci. 21, 7705-7714.
22. Giulli, G., Luzi, A., Poyard, M. and Guellan, G. (1994). Expression of mouse brain soluble guanylyl cyclase and NO synthase during ontogeny. Dev. Brain Res. 81, 269-283.
23. Gorbatyuk, O., Landry, M., Emson, P., Akmayev, I. and Hökfelt, T. (1997). Developmental expression of nitric oxide synthase in the rat diencephalon with special references to the thalamic paratenial nucleus. Int. J. Dev. Neurosci. 15, 931-938.
24. Gouge, R. C., Marshburn, P., Gordon, B. E., Nunley, W. and Huet-Hudson, Y. M. (1998). Nitric oxide as a regulator of embryonic development. Biol. Reprod. 58, 875-879.
25. Guido, W., Scheiner, C. A., Mize, R. R. and Kratz, K. E. (1997). Developmental changes in the pattern of NADPH-diaphorase staining in the cat's internal geniculate nucleus. Vis. Neurosci. 14, 1167-1173.
26. Hisatomi, O., Honkawa, H., Imanishi, Y., Satoh, T. and Tokunaga, F. (1999). Three kinds of cuanylate cyclase expressed in Medaka photoreceptor cells in both retina and pineal organ. Biochem. Biophys. Res. Comm. 255, 216-220.
27. Holmqvist, B., Falk-Olsson, C., Larsson, B. and Alm, P. (2001). The ontogeny of nitric oxide synthase systems in the mouse. Soc. Neurosci. Abstr. 27, 693.4.
28. Holmqvist, B., Ellingsen, B., Alm, P., Forsell, J., Øyan, A.-M., Goksøyr, A., Fjose, H.-C. and Seo, H.-C. (2000a). Identification and distribution of nitric oxide synthase in the brain of adult zebrafish. Neurosci. Lett. 292, 119-122.
29. Holmqvist, B., Ellingsen, B., Östholm, T. and Alm, P. (2000b). Ontogeny of nitric oxide synthase in the CNS of zebrafish. Soc. Neurosci. Abstr. 26, 693.
30. Holmqvist, B., Goksøyr, A. and Øyan, A. (1998). Distributional expression of brain neuronal nitric oxide synthase mRNA during developmental life stages of Atlantic salmon. Soc. Neurosci. Abstr. 24, 215.14.
31. Holmqvist, B., Östholm, T., Alm, P. and Ekström, P. (1994). Nitric oxide synthase in the brain of a teleost. Neurosci. Lett. 171, 205-208.
32. Holzschuh, J., Ryu, S., Arberger, F. and Driever, W. (2001). Dopamine transporter expression distinguishes dopaminergic neurons from catecholaminergic neurons in the developing zebrafish embryo. Mech. Dev. 101, 237-243.
33. Islam, A. T. M. S., Nakamura, K., Seki, T., Kuraoka, A., Hirata, K., Emson, P. C. and Kawabuchi, M. (1998). Expression of NOS, PSA-N-CAM and S-100 protein in the granule cell migration pathway of adult guinea pig forebrain. Dev. Brain Res. 107, 191-205.
34. Iwase, K., Iyama, K., Akagi, K., Yano, S., Fukunaga, K., Miyamoto, E., Mori, M. and Takiguchi, M. (1998). Precise distribution of neuronal nitric oxide synthase mRNA in the rat brain revealed by non-isotopic in situ hybridization. Mol. Brain Res. 53, 1-12.
35. Jablonka-Shariff, A., Basuray. R. and Olson, L. M. (1999). Inhibitors of nitric oxide synthase influence oocyte maturation in rats. J. Soc. Gynecol. Invest. 6, 95-101.
36. Judas, M., Sestan, N. and Kostovic, I. (1999). Nitrinergic neurons in the developing and adult human telencephalon: transient and permanent patters of expression in comparisons to other mammals. Micr. Res. Tech. 45, 401-419.
37. Keilhoff, G., Seidel, B., Noack, H., Tischmeyer, W., Stanek, D. and Wolf, G. (1996). Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat development. Neurosci. 75, 1193-1201.
38. Kim, K.-Y., Ju, W.-K., Oh, S.-J. and Chun, M.-H. (2000). The immunocytochemical localization of neuronal nitric oxide synthase in the developing rat retina. Exp. Brain Res. 133, 419-424.
39. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullman, B. and Schilling, T. F. (1995). Stages of embryonic development of zebrafish. Dev. Dyn. 203, 253-310.
40. Kimura, K. A., Reynolds, J. N. and Brien, J. F. (1999). Ontogeny of nitric oxide synthase I and II protein expression and enzymatic activity in the guinea pig hippocampus. Dev. Brain Res. 116, 211-216.
41. Kuo, R. C., Baxter, G. T., Thompson, S. H., Stricker, S. A., Patton, C., Bonaventura, J. and Epel, D. (2000). NO is necessary and sufficient for egg activation at fertilization. Nature 406, 633-636.
42. Kuzin, B., Roberts, I., Peunova, N. and Enikolopov, G. (1996). Nitric oxide regulates cell proliferation during Drosophila development. Cell 87, 639-649.
43. Kuzin, B., Regulski, M., Stasiv, Y., Scheinker, V., Tully, F. and Enikolopov, G. (2000). Nitric oxide interacts with the retinoblastoma pathway to control eye development in Drosophila. Curr. Biol. 10, 459-462.
44. Lee, M. A., Cai, L., Hubner, N., Lee, Y. A. and Lindpainter, K. (1997). Tissue- and development-specific expression of multiple alternatively spliced transcripts of rat neuronal nitric oxide synthase. Clin. Invest. 100, 1507-1512.
45. Lizasoain, I., Weiner, C. P., Knowles, R. G. and Moncada, S. (1996). The ontogeny of cerebral and cerebellar nitric oxide synthase in the guinea pig and rat. Pediatric Res. 39, 779-783.
46. McDonald, L. J. and Murad, F. (1996). Nitric oxide and cyclic GMP signaling. Proc. Soc. Exp. Biol. Med. 21, 11-16.
47. Mize, R. R., Dawson, T. M., Dawson, V. L. and Friedlander, M. J. (1998) (ed). Nitric oxide in brain development, plasticity and disease. In Progress in Brain Research, Vol. 118, pp. 1-302. Amsterdam: Elsevier Science.
48. Moncada, S., Nistico, G., Bagetta, G. and Higgs, E. A. (1998) (ed). Nitric Oxide and the Cell Proliferation, Differentiation and Death, pp. 1-305. London: Portland Press Ltd.
49. Moncada, S., Palmer, R. M. J. and Higgs, E. A. (1991). Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol. Rev. 43, 109-142.
50. Moreno-Lopez, B., Noval, J. A., González-Bonet, L. G. and Estrada, C. (2000). Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res. 869, 244-250.
51. Northington, F. J., Koehler, R. C., Traystman, R. T. and Martin, L. J. (1996). Nitric oxide synthase 1 and nitric oxide synthase 3 expression is regionally and temporally regulated in the fetal brain. Dev. Brain Res. 95, 1-14.
52. Oermann, E., Bidmon, H.-J., Mayer, B. and Zilles, K. (1999). Differential maturational patterns of nitric oxide synthase-I and NADPH diaphorase in functionally distinct cortical areas of the mouse cerbral cortex. Anat. Embryol. 200, 27-41.
53. Ogura, T., Nakayama, N., Fujisawa, H. and Esumi, H. (1996). Neuronal nitric oxide synthase expression in neuronal cell differentiation. Neurosci. Lett. 204, 89-92.
54. Ohyu, J. and Takashima, S. (1998). Developmental characteristics of neuronal nitric oxide synthase (nNOS) immunoreactive neurons in fetal and adolescent human brains. Dev. Brain Res. 110, 193-202.
55. Östholm, T., Holmqvist, B. I., Alm, P. and Ekström, P. (1994). Nitric oxide synthase in the retina of a teleost. Neurosci. Lett. 168, 233-237.
56. Øyan, A.-M., Goksør, A. and Holmqvist, B. (2000). Partial cloning of neuronal nitric oxide synthase and expression in the brain of adult Atlantic salmon. Mol. Brain Res. 78, 38-49.
57. Puenova, N., Scheinker, V., Cline, H. and Enikolopov, G. (2001). Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 21, 8809-8818.
58. Puenova, N. and Enikolopov, G. (1995). Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375, 68-73.
59. Ribera, J., Marsal, J., Casanovas, A., Hukkanen, M. and Tarabal, O. (1998). Nitric oxide synthase in rat neuromuscular junctions and in nerve terminals of Torpedo electric organ: Its role as regulator of acetylcholine release. J. Neurosci. Res. 51, 90-102.
60. Ross, L. S., Parret, T. and Easter, S. S., Jr. (1992). Agonenesis and morphogenesis in the embryonic zebrafish brain. J. Neurosci. 12, 467-482.
61. Saeij, J. P., Stet, R. J., Groeneveld, A., Verburg-van Kemenade, L. B., van Muiswinkel, W. B. and Wiegertjes, G. F. (2000). Molecular and functional characterization of a fish inducible-type nitric oxide synthase. Immunogen. 51, 339-346.
62. Seimiya, M., Kusakabe, T. and Suzuki, N. (1997). Primary structure and differential gene expression of three forms of guanylyl cyclase found in the eye of the teleost Oryzias latipes. J. Biol. Chem. 272, 23407-23417.
63. Serfözö, Z. and Elekes, K. (2002). Nitric oxide level regulates the embryonic development of the pond snail Lymnaea stagnalis: pharmacological, behavioral, and ultrastructural studies. Cell Tiss. Res. 10, 119-130.
64. Shin, D. H., Lim, H. S., Cho, S. K., Lee, H. Y., Lee, H. W., Lee, K. H., Chung, Y. H., Cho, S. S., Ik Cha, C. and Hwang, D. H. (2000). Immunocytochemical localization of neuronal and inducible nitric oxide synthase in the retina of zebrafish, Brachydanio rerio. Neurosci. Lett. 292, 220-222.
65. Shoham, S., Norris, P. J., Baker, W. A. and Emson, P. C. (1997). Nitric oxide synthase in ventral grafts and in early ventral forebrain development. Dev. Brain Res. 99, 155-166.
66. Stallmeyer, B., Anhold, M., Wetzler, C., Kahlina, K., Pfeilschifter, J. and Frank, S. (2002). Regulation of eNOS in normal and diabetes-impaired skin repair: implications for tissue regeneration. Nitric Oxide 6, 168-177.
67. Takemura, M., Wakisaka, S., Iwase, K., Yabuta, N. H., Nakagawa, S., Chen, K., Bae, Y. C., Yoshida, A. and Shigenaga, Y. (1996). NADPH-diaphorase in the developing rat: lower brainstem and cervical spinal cord, with special reference to the trigemino-solitary complex. J. Comp. Neurol. 365, 511-525.
68. Terada, H. M., Nagai, T., Okada, S., Kimura, H. and Kitahama, K. (2001). Ontogenesis of neurons immunoreactive for nitric oxide synthase in rat forebrain and midbrain. Dev. Brain Res. 128, 121-137.
69. Terada, H. M., Nagai, T., Kimura, H., Kitahama, K. and Okada, S. (1996). Distribution of nitric oxide synthase-immunoreactive neurons in fetal rat brain at embryonic day 15 and day 19. J. Chem. Neuroanat. 10, 273-278.
70. Töpel, A., Stanarius, A. and Wolf, G. (1998). Distribution of the endothelial constitutive nitric oxide synthase in the developing rat brain: an immunohistochemical study. Brain Res. 788, 43-48.
71. Van de Peer, Y., Taylor, J. S., Joseph, J. and Meyer, A. (2002). Wanda: a database of duplicated fish genes. Nucleic Acids Res. 30, 109-112.
72. Villani, L. (1999a). Development of NADPH-diaphorase activity in the central nervous system of the cichlid fish, Tilapia marie. Brain Behav. Evol. 54, 147-158.
73. Villani, L. (1999b). Developmental pattern of NADPH-diaphorase activity in the peripheral nervous system of the cichlid fish Tilapia mariae. Eur. J. Histochem. 43, 301-310.
74. Vincent, S. R. (1994). Nitric oxide: a radical neurotransmitter in the central nervous system. Prog. Brain Res. 42, 129-160.
75. Wang, Y., Newton, D. C. and Marsden, P. A. (1999). Neuronal NOS: gene structure, mRNA diversity, and functional relevance. Crit. Rev. Neurobiol. 13, 21-43.
76. Wang, W., Nakayama, T., Inoue, N. and Kato, T. (1998). Quantitative analysis of nitric oxide synthase expressed in developing and differentiating rat cerebellum. Dev. Brain Res. 111, 65-75.
77. Wang, Y., Newton, D. C. and Marsden, P. A. (1999). Neuronal NOS: gene structure, mRNA diversity, and functional relevance. Crit. Rev. Neurobiol. 13, 21-43.
78. Wilson, S. W., Ross, L. S., Parret, T. and Easter, S. S., Jr. (1990). The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 108, 121-145.
79. Wulliman, M. F. and Knipp, S. (2000). Proliferation pattern changes in the zebrafish brain from embryonic through early postembryonic stages. Anal. Embryol. 202, 385-400.
80. Wulliman, M. F., Rupp, B. and Rechert, H. (1996). Neuroanatomy of the Zebrafish Brain: A Topological Atlas. Birkhäuser. Germany.
81. Yan, X. X. and Ribak, C E. (1997). Prenatal development of nicotinamide adenine dinucleotide phosphate-diaphorase activity in the human hippocampal formation. Hippocampus 7, 215-231.
82. Zemel, E., Eyal, O., Lei, B. and Perlman, I. (1996). NADPHd activity in mammalian retinas is modulated by the state of visual adapation. Vis. Neurosci. 13, 863-871.