Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 May 23;92(11):5121–5123. doi: 10.1073/pnas.92.11.5121

Differentiation of short-wavelength-sensitive cones by NADPH diaphorase histochemistry.

H M Petry 1, H A Murphy 1
PMCID: PMC41860  PMID: 7761459

Abstract

NADPH diaphorase (NADPH dehydrogenase; EC 1.6.99.1) histochemistry labels neurons that synthesize the neurotransmitter nitric oxide (NO). In retina, it has been demonstrated that NO can affect the metabolism of cGMP in rod photoreceptors. To investigate potential involvement of NO in cone photoreceptor activity, we utilized NADPH diaphorase histochemistry to study the cone-dominated retina of the tree shrew (Tupaia belangeri). Unexpectedly, our results revealed different NADPH diaphorase activity in the cellular subcompartments of the spectral classes of cone photoreceptors. Although all cones showed intense labeling of inner segment ellipsoids, the short-wavelength-sensitive (SWS or "blue-sensitive") cones and the rods displayed intense staining of the myoid inner segment subcompartment as well. Furthermore, only SWS cones and rods displayed surface labeling of their nuclei. These findings indicate a manner in which SWS cones differ biochemically from other cone types and in which they are more similar to rods. Such differences may underlie some of the unusual functional properties of the SWS cone system, which have been attributed to postreceptoral processes.

Full text

PDF
5121

Images in this article

5122Fig. 1
on p.5122
5122Fig. 2
on p.5122

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahnelt P. K., Kolb H., Pflug R. Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. J Comp Neurol. 1987 Jan 1;255(1):18–34. doi: 10.1002/cne.902550103. [DOI] [PubMed] [Google Scholar]
  2. Bredt D. S., Snyder S. H. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci U S A. 1990 Jan;87(2):682–685. doi: 10.1073/pnas.87.2.682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Böhme G. A., Bon C., Lemaire M., Reibaud M., Piot O., Stutzmann J. M., Doble A., Blanchard J. C. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9191–9194. doi: 10.1073/pnas.90.19.9191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cobcroft M., Vaccaro T., Mitrofanis J. Distinct patterns of distribution among NADPH-diaphorase neurones of the guinea pig retina. Neurosci Lett. 1989 Aug 14;103(1):1–7. doi: 10.1016/0304-3940(89)90475-8. [DOI] [PubMed] [Google Scholar]
  5. Crognale M., Jacobs G. H. Temporal properties of the short-wavelength cone mechanism: comparison of receptor and postreceptor signals in the ground squirrel. Vision Res. 1988;28(10):1077–1082. doi: 10.1016/0042-6989(88)90134-4. [DOI] [PubMed] [Google Scholar]
  6. Curcio C. A., Allen K. A., Sloan K. R., Lerea C. L., Hurley J. B., Klock I. B., Milam A. H. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J Comp Neurol. 1991 Oct 22;312(4):610–624. doi: 10.1002/cne.903120411. [DOI] [PubMed] [Google Scholar]
  7. Dawson T. M., Bredt D. S., Fotuhi M., Hwang P. M., Snyder S. H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7797–7801. doi: 10.1073/pnas.88.17.7797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DeMonasterio F. M., Schein S. J., McCrane E. P. Staining of blue-sensitive cones of the macaque retina by a fluorescent dye. Science. 1981 Sep 11;213(4513):1278–1281. doi: 10.1126/science.7268439. [DOI] [PubMed] [Google Scholar]
  9. Gillett C. E., Barnes D. M., Camplejohn R. S. Comparison of three cell cycle associated antigens as markers of proliferative activity and prognosis in breast carcinoma. J Clin Pathol. 1993 Dec;46(12):1126–1128. doi: 10.1136/jcp.46.12.1126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gouras P., MacKay C. J. Electroretinographic responses of the short-wavelength-sensitive cones. Invest Ophthalmol Vis Sci. 1990 Jul;31(7):1203–1209. [PubMed] [Google Scholar]
  11. Hamilton S. E., Hurley J. B. A phosphodiesterase inhibitor specific to a subset of bovine retinal cones. J Biol Chem. 1990 Jul 5;265(19):11259–11264. [PubMed] [Google Scholar]
  12. Hope B. T., Michael G. J., Knigge K. M., Vincent S. R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2811–2814. doi: 10.1073/pnas.88.7.2811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hope B. T., Vincent S. R. Histochemical characterization of neuronal NADPH-diaphorase. J Histochem Cytochem. 1989 May;37(5):653–661. doi: 10.1177/37.5.2703701. [DOI] [PubMed] [Google Scholar]
  14. Jacobs G. H., Neitz J. Spectral mechanisms and color vision in the tree shrew (Tupaia belangeri). Vision Res. 1986;26(2):291–298. doi: 10.1016/0042-6989(86)90026-x. [DOI] [PubMed] [Google Scholar]
  15. Margulis A., Sharma R. K., Sitaramayya A. Nitroprusside-sensitive and insensitive guanylate cyclases in retinal rod outer segments. Biochem Biophys Res Commun. 1992 Jun 30;185(3):909–914. doi: 10.1016/0006-291x(92)91713-z. [DOI] [PubMed] [Google Scholar]
  16. Montague P. R., Gancayco C. D., Winn M. J., Marchase R. B., Friedlander M. J. Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex. Science. 1994 Feb 18;263(5149):973–977. doi: 10.1126/science.7508638. [DOI] [PubMed] [Google Scholar]
  17. Müller B., Peichl L., De Grip W. J., Gery I., Korf H. W. Opsin- and S-antigen-like immunoreactions in photoreceptors of the tree shrew retina. Invest Ophthalmol Vis Sci. 1989 Mar;30(3):530–535. [PubMed] [Google Scholar]
  18. Müller B., Peichl L. Topography of cones and rods in the tree shrew retina. J Comp Neurol. 1989 Apr 22;282(4):581–594. doi: 10.1002/cne.902820409. [DOI] [PubMed] [Google Scholar]
  19. Nork T. M., McCormick S. A., Chao G. M., Odom J. V. Distribution of carbonic anhydrase among human photoreceptors. Invest Ophthalmol Vis Sci. 1990 Aug;31(8):1451–1458. [PubMed] [Google Scholar]
  20. Petry H. M., Erichsen J. T., Szél A. Immunocytochemical identification of photoreceptor populations in the tree shrew retina. Brain Res. 1993 Jul 9;616(1-2):344–350. doi: 10.1016/0006-8993(93)90230-k. [DOI] [PubMed] [Google Scholar]
  21. Petry H. M., Hárosi F. I. Visual pigments of the tree shrew (Tupaia belangeri) and greater galago (Galago crassicaudatus): a microspectrophotometric investigation. Vision Res. 1990;30(6):839–851. doi: 10.1016/0042-6989(90)90053-n. [DOI] [PubMed] [Google Scholar]
  22. Petry H. M., Kelly J. P. Psychophysical measurement of spectral sensitivity and color vision in red-light-reared tree shrews (Tupaia belangeri). Vision Res. 1991;31(10):1749–1757. doi: 10.1016/0042-6989(91)90024-y. [DOI] [PubMed] [Google Scholar]
  23. Provis J. M., Mitrofanis J. NADPH-diaphorase neurones of human retinae have a uniform topographical distribution. Vis Neurosci. 1990 Jun;4(6):619–623. doi: 10.1017/s0952523800005812. [DOI] [PubMed] [Google Scholar]
  24. Sagar S. M. NADPH diaphorase histochemistry in the rabbit retina. Brain Res. 1986 May 14;373(1-2):153–158. doi: 10.1016/0006-8993(86)90325-2. [DOI] [PubMed] [Google Scholar]
  25. Sandell J. H. NADPH diaphorase cells in the mammalian inner retina. J Comp Neurol. 1985 Aug 22;238(4):466–472. doi: 10.1002/cne.902380410. [DOI] [PubMed] [Google Scholar]
  26. Schmidt K. F., Nöll G. N., Yamamoto Y. Sodium nitroprusside alters dark voltage and light responses in isolated retinal rods during whole-cell recording. Vis Neurosci. 1992 Aug;9(2):205–209. doi: 10.1017/s0952523800009664. [DOI] [PubMed] [Google Scholar]
  27. Schnapf J. L., Nunn B. J., Meister M., Baylor D. A. Visual transduction in cones of the monkey Macaca fascicularis. J Physiol. 1990 Aug;427:681–713. doi: 10.1113/jphysiol.1990.sp018193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schuman E. M., Madison D. V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science. 1991 Dec 6;254(5037):1503–1506. doi: 10.1126/science.1720572. [DOI] [PubMed] [Google Scholar]
  29. Szél A., Diamantstein T., Röhlich P. Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. J Comp Neurol. 1988 Jul 22;273(4):593–602. doi: 10.1002/cne.902730413. [DOI] [PubMed] [Google Scholar]
  30. Tsuyama Y., Nöll G. N., Schmidt K. F. L-arginine and nicotinamide adenine dinucleotide phosphate alter dark voltage and accelerate light response recovery in isolated retinal rods of the frog (Rana temporaria). Neurosci Lett. 1993 Jan 4;149(1):95–98. doi: 10.1016/0304-3940(93)90356-p. [DOI] [PubMed] [Google Scholar]
  31. Vaccaro T. M., Cobcroft M. D., Provis J. M., Mitrofanis J. NADPH-diaphorase reactivity in adult and developing cat retinae. Cell Tissue Res. 1991 Aug;265(2):371–379. doi: 10.1007/BF00398085. [DOI] [PubMed] [Google Scholar]
  32. Venturini C. M., Knowles R. G., Palmer R. M., Moncada S. Synthesis of nitric oxide in the bovine retina. Biochem Biophys Res Commun. 1991 Oct 31;180(2):920–925. doi: 10.1016/s0006-291x(05)81153-2. [DOI] [PubMed] [Google Scholar]
  33. Vincent S. R., Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience. 1992;46(4):755–784. doi: 10.1016/0306-4522(92)90184-4. [DOI] [PubMed] [Google Scholar]
  34. Weiler R., Kewitz B. The marker for nitric oxide synthase, NADPH-diaphorase, co-localizes with GABA in horizontal cells and cells of the inner retina in the carp retina. Neurosci Lett. 1993 Aug 20;158(2):151–154. doi: 10.1016/0304-3940(93)90251-f. [DOI] [PubMed] [Google Scholar]
  35. Yamamoto R., Bredt D. S., Snyder S. H., Stone R. A. The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience. 1993 May;54(1):189–200. doi: 10.1016/0306-4522(93)90393-t. [DOI] [PubMed] [Google Scholar]
  36. Zrenner E., Gouras P. Blue-sensitive cones of the cat produce a rodlike electroretinogram. Invest Ophthalmol Vis Sci. 1979 Oct;18(10):1076–1081. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES