Localization of the two constitutively expressed nitric oxide synthase isoforms (nNOS and eNOS) in the same cell types in the saccule maculae of the frog Rana pipiens by immunoelectron microscopy: Evidence for a back-up system?

Journal of Electron Microscopy

Volumn 52, Issue 2, 2003, Pages 197-206

  Heinrich, Ulf Rüdiger ^a   Lioudyno, Maria ^b   Maurer, Jan ^a   Mann, Wolf ^a   Guth, Paul S ^b   Förstermann, Ulrich ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Frog; Hair cells; Immunocytochemistry; Nitric oxide synthase; Vestibular

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ISOENZYME; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CORTI ORGAN; ENZYMOLOGY; FROG; HAIR CELL; HISTOLOGY; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; VESTIBULAR LABYRINTH;

ACOUSTIC MACULAE; ANIMALS; HAIR CELLS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MICROSCOPY, IMMUNOELECTRON; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; ORGAN OF CORTI; RANA PIPIENS;

ANIMALIA; ANURA; RANA PIPIENS;

BACTERIOPHAGES; MAMMALS; NITRIC OXIDE; SIGNAL TRANSDUCTION;

CELL TYPES; FROG; HAIR CELLS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITIES; ISOFORMS; LOCALISATION; NITRIC OXIDE SYNTHASES; SUB-CELLULAR; VESTIBULAR;

ANTIBODIES;

EID: 0037745635     PISSN: 00220744     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (40)

1. Hillman D E (1976) Vestibular and lateral line system 14. Morphology and peripheral and central vestibular systems. In: Frog Neurobiology, eds. Llinas R and Precht W, pp. 452-480, (Springer-Verlag, Berlin).
2. Flock Å (1964) Structure of the maculi utriculi special reference to directional interplay of sensory responses as revealed by morphologic polarization. J. Cell Biol. 22: 413-431.
3. Guth P S, Fermin C D, Pantoja M, Edwards R, and Norris C (1994) Hair cells of different shapes and their placement along the frog crista ampullaris. Hear. Res. 73: 109-115.
4. Hudspeth A J (1989) How the ear's works work. Nature 341: 397-404.
5. Wilson V J and Melvill-Jones G (1979) Mammalian Vestibular Physiology. (Plenum Press, New York.)
6. Corey D and Hudspeth A (1979) Response latency of vertebrate hair cells. Biophys. J. 26: 499-506.
7. Guth P S, Perin P, Norris H, and Valli P (1998) The vestibular hair cells. Post-transductional signal processing. Prog. Neurobiol. 54: 193-247.
8. Su Z-L, Jiang S-C, Gu R, and Yang W-P (1995) TWo types of calcium channels in bullfrog saccular hair cells. Hear. Res. 87: 62-68.
9. Norris C H, Ricci A J, Housley G D, and Guth P S (1992) The inactivating potassium currents of hair cells isolated from the crista ampullaris of the frog. J. Neurophys. 68: 1642-1653.
10. Fessenden J D and Schacht J (1998) The nitric oxide/cyclic GMP pathway: a potential major regulator of cochlear physiology. Hear. Res. 118: 168-176.
11. Förstermann U and Kleinert H (1995) Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmiedebergs Arch. Pharmacol. 352: 351-364.
12. Schmidt H H H W, Lohmann S M, and Malter U (1993) The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochem. Biophys. Acta 1178: 153-175.
13. Mayer B, John M, and Böhme E (1990) Purification of a calcium/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor role of tetrahydrobiopterin. FEBS Lett. 277: 215-219.
14. Schmidt H H H W, Pollock J S, Nakane M, Gorsky L D, Förstermann U, and Murad F (1991) Purification of a soluble isoform of guanylyl cyclase-activating-factor synthase. Proc. Natl. Acad. Sci. USA 88: 365-369.
15. Bredt D S and Snyder S H (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87: 682-685.
16. Förstermann U, Pollock J S, Schmidt H H H W, Heller M, and Murad F (1991) Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA 88: 1788-1792.
17. Pollock J S, Nakane M, Buttery L K, Martinez A, Springall D, Polak J M, Förstermann U, and Murad F (1993) Characterization and localization of endothelial nitric oxide synthase using specific monoclonal antibodies. Am. J. Physiol. 265: C1379-C1387.
18. Fessenden J D, Atschuler R A, Seasholtz A F, and Schacht J (1999) Nitric oxide/cyclic guanosine monophosphate pathway in the peripheral and central auditory system of the rat. J. Comp. Neurology 404: 52-63.
19. Franz P, Hauser-Kronberger C, Böck P, Quint C, and Baumgartner W D (1996) Localization of nitric oxide synthase I and III in the cochlea. Acta Otolaryngol. (Stockh) 116: 726-731.
20. Gosepath K, Gath I, Maurer J, Pollock J S, Amedee R, Förstermann U, and Mann W (1997) Characterization of NO synthase isoforms expressed in different structures of the guinea pig cochlea. Brain Res. 747: 26-33.
21. Heinrich U-R, Maurer J, Gosepath K, and Mann W (1997) Electron microscopic localization of nitric oxide I synthase in the organ of Corti of the guinea pig. Eur. Arch. Otorhinolaryngol. 254: 396-400.
22. Heinrich U-R, Maurer J, Gosepath K, and Mann W (1998) Immunoelectron microscopic localization of nitric oxide synthase III in the guinea pig organ of Corti. Eur. Arch. Otorhinolaryngol. 255: 483-490.
23. Hess A, Bloch W, Arnhold S, Andressen C, Stennert E, Addicks K, and Michel O (1998) Nitric oxide synthase in the vestibulocochlear system of mice. Brain Res. 813: 97-102.
24. Harper A, Blythe W R, Zdanski C J, Prazma J, and Pillsbuy H C (1994) Nitric oxide in the rat vestibular system. Otolaryngol. Head Neck Surg. 4: 430-438.
25. Hess A, Bloch W, Su J, Stennert E, Addicks K, and Michel O (1998) Localization of the nitric oxide (NO)/cGMP-pathway in the vestibular system of guinea pigs. Neurosci. Lett. 251: 185-188.
26. Takumida M and Anniko M (2000) Direct evidence of nitric oxide production in guinea pig vestibular sensory cells. Acta Otolaryngol. 120: 34-38.
27. Guth P S, Dunn A, Kronomer K, and Norris C H (1994) The cholinergic pharmacology of the frog saccule. Hear. Res. 75: 225-232.
28. Guth P S, Holt J C, Perin P, Athas G, Garcia M, Puri A, Zucca G, Botta L, and Valli P (1998) The metabotropic glutamate receptors of the vestibular organs. Hear. Res. 125: 154-162.
29. Lenzi D and Roberts W M (1994) Calcium signalling in hair cells. Multiple roles in a compact cell. Curr. Opin. Neurobiol. 4: 496-502.
30. Reimer L (1995) Energy-Filtering Transmission Electron Microscopy (Springer Series in Optical Sciences, vol. 71). (Springer, Berlin, Heidelberg, New York.)
31. Griffiths G (1993) Fine Structure Immunocytochemistry. ( Springer, Berlin, Heidelberg, New York.)
32. Lucocq J (1994) Quantitation of gold labelling and antigens in immunolabelled ultrathin sections. J. Anat. 184: 1-13.
33. Mayhew T M, Lucocq J M, and Griffiths G (2002) Relative labelling index: a novel stereological approach to test for non-random immunogold labelling of organelles and membranes on transmission electron microscopy thin sections, J. Microsc. 205: 153-164.
34. Förstermann U, Boissel J-P, and Kleinert H (1998) Expressional control of the 'constitutive' isoforms of nitric oxide synthase (nNOS and eNOS). FASEB J. 12: 773-790.
35. Brenman J E, Chao D S, Gee S H, McGee A W, Craven S E, Santillano D R, Wu Z, Huang F, Xia H, Peters M F, Froehner S C, and Bredt D S (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha-syntrophin mediated by PDZ domains. Cell 84: 757-767.
36. Fulton D, Gratton J-P, and Sessa W C (2001) Post-translational control of endothelial nitric oxide synthase: Why isn't calcium/calmodulin enough? J. Pharmacol. Exp. Therapeutics 299: 818-824.
37. 1-subunits of soluble guanylyl cyclase in the guinea pig organ of Corti. Brain Res. 885: 6-13.
38. Boissel J P, Schwarz P M, and Förstermann U (1998) Neuronal-type NO synthase: transcript diversity and expressional regulation. Nitric Oxide 2: 337-349.
39. Li H, Wallerath T, and Förstermann U (2002) Physiological mechanisms regulating the expression of endothelial-type NO synthase. Nitric Oxide Biol. Chem. 7: 132-147.
40. Son H, Hawkins R D, Martin K, Kiebler M, Huang P L, Fishman M C, and Kandel E R (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87: 1015-1023.