Journal of Life Science (생명과학회지)

Korean Society of Life Science (한국생명과학회)
권호 표지
DOI QR코드

DOI QR Code

Immunocytochemical Localization of Melanopsin-immunoreactive Neurons in the Mouse Visual Cortex

생쥐 시각피질에서 melanopsin을 가지는 신경세포의 면역조직화학적 위치

  • Lee, Won-Sig (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Noh, Eun-Jong (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Seo, Yoon-Dam (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Jeong, Se-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Lee, Eun-Shil (Department of Biology, College of Natural Sciences, Kyungpook National University) ;
  • Jeon, Chang-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University)
  • 이원식 (경북대학교 자연과학대학 생물학과) ;
  • 노은종 (경북대학교 자연과학대학 생물학과) ;
  • 서윤담 (경북대학교 자연과학대학 생물학과) ;
  • 정세진 (경북대학교 자연과학대학 생물학과) ;
  • 이은실 (경북대학교 자연과학대학 생물학과) ;
  • 전창진 (경북대학교 자연과학대학 생물학과)
  • Received : 2013.03.20
  • Accepted : 2013.06.19
  • Published : 2013.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Melanopsin is an opsin-like photopigment found in the small proportion of photosensitive ganglion cells of the retina. It is involved in the regulation of the synchronization of the circadian cycle as well as in the control of pupillary light reflex. The purpose of the present study is to investigate whether melanopsin is also expressed in the other areas of the central visual system outside the retina. We have studied the distribution and morphology of neurons containing melanopsin in the mouse visual cortex with antibody immunocytochemistry. Melanopsin immunoreactivity was mostly present in neuronal soma, but not in nuclei. We found that melanopsin was present in a large subset of neurons within the adult mouse visual cortex with the highest density in layer II/III. In layer I of the visual cortex, melanopsin-immunoreactive (IR) neurons were rarely encountered. In the mouse visual cortex, the majority of the melanopsin-IR neurons consisted of round/oval cells, but was varied in morphology. Vertical fusiform and pyramidal cells were also rarely labeled with the anti-melanopsin antibody. The labeled cells did not show any distinctive distributional pattern. Some melanopsin-IR neurons in mouse visual cortex co-localized with nitricoxide synthase, calbindin and parvalbumin. Our data indicate that melanopsin is located in specific neurons and surprisingly widespread in visual cortex. This finding raises the need of the functional study of melanopsin in central visual areas outside the retina.

Melanopsin은 옵신과 비슷한 광색소로 망막 광민감성 신경절 세포에서 적은 비율로 발견 된다. Melanopsin은 일주기 리듬조절에 관여 하고 동공반사를 조절한다. 이번 연구의 목적은 melanopsin이 망막 이외의 중추 시각계 에서도 발견 되는지를 알아 보는 것이다. 우리는 생쥐 시각 피질에 존재하는 melanopsin을 가지는 신경세포를 면역조직화학법을 통해 염색하여 melanopsin의 분포와 형태를 분석하였다. Melanopsin 면역반응은 핵을 제외한 신경세포의 세포체에서 일어났다. 우리는 melanopsin이 성체 생쥐의 시각 피질의 2,3층에서 높은 밀도로 모여서 존재하는 것을 확인했다. 시각 피질 1층에서 melanopsin 면역반응을 보인 신경세포는 드물게 발견 되었다. 생쥐 시각 피질에서 발견된 melanopsin의 세포종류는 주로 round/oval 세포였으나, vertical fusiform 그리고 pyramidal 세포 등도 드물게 발견 되었다. 염색된 세포들의 분포는 특이적이지 않았다. 우리의 실험 데이터로 melanopsin이 시각피질에도 분포한다는 것을 알 수 있었다. 또한, melanopsin을 가지는 신경세포는 nitric oxide synthase, calbindin and parvalbumin과도 같이 발현 되는 것을 관찰했다. 이러한 실험결과는 망막 이외의 부분에서 발견되는 melanopsin의 기능에 대한 연구가 필요함을 야기한다.

Keywords

References

  1. Berson, D. M., Dunn, F. A. and Takao, M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070-1073. https://doi.org/10.1126/science.1067262
  2. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. and Deisseroth, K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8, 1263-1268. https://doi.org/10.1038/nn1525
  3. Cassone, M. C., Lombard, A., Rossetti, V., Urciuoli, R. and Rolfo, P. M. 1993. Effect of in vivo He–Ne laser irradiation on biogenic amine levels in rat brain. J Photochem Photobiol B 18, 291-294. https://doi.org/10.1016/1011-1344(93)80078-N
  4. Cellerino, A., Siciliano, R., Domenici, L. and Mafferi, L. 1992. Parvalbumin immunoreactivity: a reliable marker for the effects of monocular deprivation in the rat visual cortex. Neuroscience 51, 749-753. https://doi.org/10.1016/0306-4522(92)90514-3
  5. Gonchar, Y. and Burkhalter, A. 1997. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7, 347-358. https://doi.org/10.1093/cercor/7.4.347
  6. Gonchar, Y. and Burkhalter, A. 1999. Differential subcellualr localization of forward and feedback interareal inputs to parvalbumin expressing GABAergic neurons in rat visual cortex. J Comp Neurol 406, 346-360. https://doi.org/10.1002/(SICI)1096-9861(19990412)406:3<346::AID-CNE4>3.0.CO;2-E
  7. Hannibal, J., Hindersson, P., Nevo, E. and Fahrenkrug, J. 2002. The circadian photopigment melanopsin is expressed in the blind subterranean mole rat, Spalax. Neuroreport 13, 1411-1414. https://doi.org/10.1097/00001756-200208070-00013
  8. Hannibal, J., Hindersson, P., Knudsen, S. M., Georg, B. and Fahrenkrug, J. 2002. The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-contaning retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22, RC191.
  9. Hartwick, A. T., Bramley, J. R., Yu, J., Stevens, K. T., Allen, C. N., Baldridge, W. H., Sollars, P. J. and Pickard, G. E. 2007. Light-evoked calcium responses of isolated melanopsin-expressing retinal ganglion cells. J Neurosci 27, 13468-13480. https://doi.org/10.1523/JNEUROSCI.3626-07.2007
  10. Hatori, M. and Panda, S. 2010. The emerging roles of melanopsin in behabioral adaptation to light. Trends Mol Med 16, 435-446. https://doi.org/10.1016/j.molmed.2010.07.005
  11. Hattar, S., Liao, H.-W., Takao, M., Berson, D. M. and Yau, K.-W. 2002. Melanopsin-contaning retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science 295, 1065-1070. https://doi.org/10.1126/science.1069609
  12. Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K. W. and Berson, D. M. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497, 326-349. https://doi.org/10.1002/cne.20970
  13. Jeon, M. H., Jeon, C. J. and Yang, H. W. 1998. Calretinin and calbindin D28K immunoreactivity in the superficial layers of the rabbit superior colliculus. Neuroreport 9, 3847-3852. https://doi.org/10.1097/00001756-199812010-00015
  14. Lee, J. E., Ahn, C. H., Lee, J. Y., Chung, E. S. and Jeon, C. J. 2004. Nitric oxide synthase and calcium-binding protein-containing neurons in the hamster visual cortex. Mol Cells 18, 30-39.
  15. Lee, J. E. and Jeon, C. J. 2005. Immunocytochemical localization of nitric oxide synthase-containing neurons in mouse and rabbit visual cortex and co-localization with calcium- binding proteins. Mol Cells 19, 408-417.
  16. Leszkiewicz, D. N., Kandler, K. and Aizenman, E. 2000. Enhancement of NMDA receptor-mediated currents by light in rat neurones invitro. J Physiol 524, 365-374. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00365.x
  17. Leszkiewicz, D. and Aizenman, E. 2003. Reversible modulation of GABA(A) receptor-mediated currents by light is dependent on theredox state of the receptor. Eur J Neurosci 17, 2077-2083. https://doi.org/10.1046/j.1460-9568.2003.02656.x
  18. Letinic, K. and Kostovic, I. 1998. Postnatal development of calcium-binding proteins calbindin and parvalbumin in human visual cortex. Cereb Cortex 8, 660-669. https://doi.org/10.1093/cercor/8.7.660
  19. Leuba, G. and Saini, K. 1996. Calcium-binding proteins immunoreactivity in the human subcortical and cortical visual structures. Vis Neurosci 13, 997-1009. https://doi.org/10.1017/S0952523800007665
  20. Leuba, G. and Saini, K. 1997. Colocalization of parvalbumin, calretinin, and calbindin D-28k in the human cortical and subcortical visual structures. J Chem Neuroanat 13, 41-52. https://doi.org/10.1016/S0891-0618(97)00022-7
  21. Lucas, R., Hattar, S., Takao, M., Berson, D. M., Foster, R. G. and Yau, K. -W. 2003. Diminished papillary light reflex at high irradiances in melanopsin-knockout mice. Science 299, 245-247. https://doi.org/10.1126/science.1077293
  22. Nissila, J., Manttari, S., Tuominen, H., Takala, T., Saarela, S. and Timonen, M. 2012. The abundance and distribution of melanopsin (OPN4) protein in human brain. 20th European Congress of Psychiatry. March 3-6. Prague, Czech Republic.
  23. Panda, S., Sato, T. K., Castrucci, A. M., Rollag, M. D., DeGrip, W. J., Hogenesch, J. B., Provencio, I. and Kay, S. A. 2002. Melanopsin(Opn4) requirement for normal light-induced circadian phase shifting. Science 298, 2213-2216. https://doi.org/10.1126/science.1076848
  24. Park, H. J., Hong, S. K., Kong, J. H. and Jeon, C. J. 1999. Localization of calcium-binding protein parvalbumin immunoreactive neurons in mouse and hamster visual cortex. Mol Cells 9, 542-547.
  25. Park, H. J., Lee, S. N., Lim, H. R., Kong, J. H. and Jeon, C. J. 2000. Calcium-binding protein calbindin D28K, calretinin, and parvalbumin immunoreactivity in the rabbit visual cortex. Mol Cells 10, 206-212. https://doi.org/10.1007/s10059-000-0206-2
  26. Park, H. J., Kong, J. H., Kang, Y. S., Park, W. M., Jeong, S. A., Park, S. M., Lim, J. K. and Jeon, C. J. 2002. The distribution and morphology of calbindin D-28K- and calretinin- immunoreactive neurons in the visual cortex of mouse. Mol Cells 14, 143-149.
  27. Peirson, S. N., Halford, S. and Foster, R. G. 2009. The evolution of irradiance detection: melanopsin and the non-visual opsins. Philos Trans Rsoc Lond B Biol Sci 364, 2849-2865. https://doi.org/10.1098/rstb.2009.0050
  28. Provencio, I., Jiang, G., De Grip, W. J., Hayes, W. P. and Rollag, M. D. 1998. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci USA 95, 340-345. https://doi.org/10.1073/pnas.95.1.340
  29. Provencio, I., Rodriquez, I. R., Jiang, G., Hayes, W. P., Moreira, E. F. and Rollag, M. D. 2000. A novel human opsin in the inner retina. J Neurosci 20, 600-605.
  30. Provencio, I., Rollag, M. D. and Castrucci, A. M. 2002. Photoreceptive net in the mammalian retina. Nature 415, 493.
  31. Rahman, S. A., Marcu, S., Shapiro, C. M., Brown, T. J. and Casper, R. F. 2011. Spectral modulation attenuates molecular, endocrine, and neu-robehavioral disruption induced by nocturnal light exposure. Am J Physiol 300, E518-E527.
  32. Rollag, M. D., Berson, D. M. and Provencio, I. 2003. Melanopsin, ganglion-cell photoreceptors, and mammalian photoentrainment. J Biol Rhythms 18, 227-234. https://doi.org/10.1177/0748730403018003005
  33. Ruby, N. F., Brennan, T. J., Xie, X., Cao, V., Franken, P., Heller, H. C. and O’Hara, B. F. 2002. Role of melanopsin in circadian responses to light. Science 298, 2211-2213. https://doi.org/10.1126/science.1076701
  34. Rusak, B., Meijer, J. H. and Harrington, M. E. 1989. Hamster circadian rhythms are phase-shifted by electrical stimulation of the geniculo-hypothalamic tract. Brain Res 493, 283-291. https://doi.org/10.1016/0006-8993(89)91163-3
  35. Sandbakken, M., Ebbesson, L., Stefansson, S. and Helvik, J. V. 2012. Isolation and characterization of melanopsin photoreceptors of Atlantic salmon (Salmo salar). J Comp Neurol 520, 3732-3736.
  36. Schwaller, B. 2007. Emerging functions of the "$Ca^{2+}$ buffers" parvalbumin, calbindin D-28k and calretinin in the brain, pp. 198-221. In: Lajtha, A. and Banik, N. (eds.), Handbook of Neurochemistry and Molecular Neurobiology. Springer Science+Business Media: Berlin Heidelberg, German.
  37. Sexton, T., Buhr, E. and Van Gelder, R. N. 2012. Melanopsin and mechanisms of non-visual ocular photoreception. J Biol Chem 287, 1649-1656. https://doi.org/10.1074/jbc.R111.301226
  38. Shichida, Y. and Matsuyama, T. 2009. Evolution of opsins and phototrans-duction. Philos Trans R Soc Lond B Biol Sci 364, 2881-2895. https://doi.org/10.1098/rstb.2009.0051
  39. Shen-Zeng, Xiao-Jian., Lin, S. Z. and Wang, L. H. 1982. Effects of a lowpower laser beam guided by optic fiber on rat brain striatal monoamines and amino acids. Neurosci Lett 32, 203-208. https://doi.org/10.1016/0304-3940(82)90275-0
  40. Tsunematsu, T., Tanaka, K. F., Yamanaka, A. and Koizumi, A. 2012. Ectopic expression of melanopsin in orexin/hypocretin neurons enables control of wakefulness of mice in vivo by blue light. Neurosci Res 75, 23-28.
  41. Van Brundt, E. E., Shepherd, M. D., Wale, J. R, Ganong, W. F. and Clegg, M.-T. 1964. Penetration of light into the brain of mammals. Ann NY Acad Sci 117, 217-224.
  42. Wade, P. D., Taylor, J. and Siekevitz, P. 1988. Mammalian cerebral corticaltissue responds to low-intensity visible light. Proc Natl Acad Sci USA 85, 9322-9326. https://doi.org/10.1073/pnas.85.23.9322
  43. Warren, E. J., Allen, C. N., Brown, R. L. and Robinson, D. W. 2006. The light-activated signaling pathway in SCN-projecting rat retinalganglion cells. Eur J Neurosci 23, 2477-2487. https://doi.org/10.1111/j.1460-9568.2006.04777.x
  44. Yamashita, T., Terakita, A., Kai, T. and Shichida, Y. 2008. Conformational change of the transmembrane helices II and IV of metabotropic glutamate receptor involved in G protein activation. J Neurochem 106, 850-859. https://doi.org/10.1111/j.1471-4159.2008.05443.x
  45. Zhang, D. Q., Wong, K. Y., Sollars, P. J., Berson, D. M., Pickard, G. E. and McMahon, D. G. 2008. Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc Natl Acad Sci USA 105, 14181-14186. https://doi.org/10.1073/pnas.0803893105