Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Dysfunction of Retinal Cell and Optic Nerve by Continuous Cerebroventricular Infusion of Glucosamine

  • Jang, So-Yong (Department of Neuroscience, School of Medicine, Ewha Womans University) ;
  • Han, Inn-Oc (Department of Physiology and Biophysics, College of Medicine, Inha University) ;
  • Jun, Gyo (Department of Biochemistry, Graduate School of Medicine, Gachon University of Medicine and Science) ;
  • Oh, Sei-Kwan (Department of Neuroscience, School of Medicine, Ewha Womans University)
  • Published : 2009.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

We have investigated the effect of glucosamine on the retinal cells after continuous infusion into cerebroventricle by using osmotic minipump to avoid peripheral effect. Continuous intracerebroventricular (i.c.v) infusion of glucosamine with the rate of 0.1 ${\mu}mol$/10 ${\mu}l$/hr for 7 days resulted in morphological changes of the optic nerve in electron microscopic level as well as morphological changes of the retina in light microscopic level. Retinal sections were immunostained for the detection of morphological changes of astrocytes. GFAP immunoreactivity appeared not only in the Muller cells but also many of the radial processes of Muller cells. The optic nerve showed deformed axon and slight lamellar separation of myelin sheath after continuous infusion of glucosamine in observing with electron microscope. Interestingly, vacuoles were observed in deformed axons and retinal layers were folded and detached. These results suggested that glucosamine plays a role in induction of morphological dysfunction in retina and optic nerves.

Keywords

References

  1. Arnold, C. S., Johnson, G. V., Cole, R. N., Dong, D. L., Lee, M. and Hart, G. W. (1996). The microtubule-associated protein tau is extensively modified with O-linked-N-acetylglucosamine. J. Biol. Chem. 271, 28741-28744. https://doi.org/10.1074/jbc.271.46.28741
  2. Baron, A. D., Zhu, J. S., Zhu, J. H., Weldeon, H., Maniau, L. and Garvry, T. W. (1995). Glucosamine induces insulin resistance in vivo by affecting GLUT4 translocation in skeletal muscle. Implication for glucose toxicity. J. Clin. Invest. 96, 2792- 2801. https://doi.org/10.1172/JCI118349
  3. Calvo, J. L., Carbonell, A. L. and Boya, J. (1991). Co-expression of glial fibrillary acidic protein and vimentin in reactive astrocytes following brain injury in rats. Brain Res. 556, 333-336. https://doi.org/10.1016/0006-8993(91)91720-L
  4. Cole, R. N. and Hart, G. W. (1999). Glycosylation sites flank phosphorylation sites on synapsin I: O-linked N acetylglucosamine residue localized within domains mediating synapsin I interactions. J. Neurochem. 73, 418-428. https://doi.org/10.1046/j.1471-4159.1999.0730418.x
  5. Crook, E. D., Daniels, M. C., Smith, T. M. and McClain, D. A. (1993). Regulation of insulin-stimulated glycogen synthase activity by overexpression of glutamine: fructose-6-phosphate aminotransferase in rat-1 fibroblast. Diabetes 42, 1289-1296. https://doi.org/10.2337/diabetes.42.9.1289
  6. Daniel, M. C., Kanal, P., Smith, T. M., Paterson, A. J., Kuldow, J. E. and McCalin, D. A. (1993). Glucose regulation of transforming growth factor-alpha expression is mediated by products of hexosamine biosynthesis pathway. Mol. Endocrinol. 7, 1041-1048. https://doi.org/10.1210/me.7.8.1041
  7. Degrell, P., Cseh J., Mohas M., Molnar G. A., Pajor, L., Chatham, J. C., Fulop, N. and Wittmann, I. (2009). Evidence of O-linked N-acetylglucosamine in diabetic nephropathy. Life Sci. 84, 389-393. https://doi.org/10.1016/j.lfs.2009.01.007
  8. Diloreto, D. A., Martzen, M. R., del Cerro, C., Coleman, P. D. and del Cerro, M. (1995). Muller cell changes precede photoreceptor cell degeneration in the age-related retinal degeneration of the Fischer 344 rat. Brain Res. 698, 1-14. https://doi.org/10.1016/0006-8993(95)00647-9
  9. Eisenfeld, A. J., Bunt-Milam, A. H. and Sarthy, P. V. (1984). Muller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Invest Ophthalmol. Vis. Sci. 25, 1321-1328.
  10. Ekstrom, P., Sanyal, S., Narfstrom, K., Chader, G. J. and van Veen, T. (1988). Accumulation of glial fibrillary acidic protein in Muller radial glia during retinal degeneration. Invest Opthalmol. Vis. Sci. 29, 1363-1371.
  11. Eng, L. F. and Ghirnikar, R. S. (1994). GFAP and astrogliosis. Brain Pathol. 4, 229-237. https://doi.org/10.1111/j.1750-3639.1994.tb00838.x
  12. Erickson, P. A., Feinastein, S. C., Lewis, G. P. and Fisher, S. K. (1992). Glial fibrillary acidic protein and its mRNA: Ultrastructural detection and determination of changes after CNS injury. J. Struct. Biol. 108, 148-161. https://doi.org/10.1016/1047-8477(92)90014-2
  13. Erickson, P. A., Fisher, S. K., Guerin, C. J., Anderson, D. H. and Kaska, D. D. (1987). Glial fibrillary acidic protein increases Muller cells after retinal detachment. Exp. Eye Res. 44, 37-48. https://doi.org/10.1016/S0014-4835(87)80023-4
  14. Farach, A. M. and Galileo, D. S. (2008). O-GlcNAc modification of radial glial vimentin filaments in the developing chick brain. Brain Cell Biol. 36, 191-202. https://doi.org/10.1007/s11068-008-9036-5
  15. Fisher, S. K. and Anderson, D. H. (1989). Cellular effects of detachment on neural retina and retinal pigment epithelium. In Retina (B. M. Glaser and R.G. Nichels, Eds.) Vol. 3. pp. 165-190. Mosby, St Louis.
  16. Griffith, L. S., Mathes, M. and Schmitz, B. (1995a). Beta-amyloid precursor protein is modified with O-linked-N-acetylglucosamine. J. Neurosci. Res. 41, 270-278. https://doi.org/10.1002/jnr.490410214
  17. Griffith, L. S., Mathes, M. and Schmitz, B. (1995b). O-linked-Nacetylglucosamine is unregulated in Alzheimer brains. Biochem. Biophys. Res. Commun. 213, 424-431. https://doi.org/10.1006/bbrc.1995.2149
  18. Hanover, J. A. (2001). Glycan-dependent signaling: O-linked N-acetylglucosamine. FASEB J. 15, 1865-1876. https://doi.org/10.1096/fj.01-0094rev
  19. Hart, G. W., Kreppel, L. K., Comer, F. I., Arnorld, C. S., Snow, D. M., Ye, Z., Cheng, X., DellaManna, D., Caine, D. S., Earles, B. J., Akimoto, Y., Cole, R. N. and Hayes, B. K. (1996). O-GlcNAcylation of key nuclear and cytoskeletal proteins: reciprocity with O-phosphorylation and putative roles in protein multimerization. Glycobiology 6, 711-716. https://doi.org/10.1093/glycob/6.7.711
  20. Hawkins, M., Hu, M., Yu, J., Eder, H., Vuguin P., She, L., Barzilai, N., Leriser, M., Backer, J. M. and Rossetti, L. (1999). Discordant effects of glucosamine on insulin-stimulated glucose metabolism and phophatidylinositol 3-kinase activity. J. Biol. Chem. 274, 31313-31319. https://doi.org/10.1074/jbc.274.44.31312
  21. Hjelmeland, L. M. and Harvey, A. K. (1988). Gliosis in the mammalian retina: Migration and proliferation of retina glia. In Progress in Retinal Research (N. Osborn and G. Chader Eds.). Vol. 7. pp. 259-281. Pergamonn Press, Oxford.
  22. Hussains, M. A. (1998). A case of for glucosamine. Eur. J. Endocrinol. 139, 472-475. https://doi.org/10.1530/eje.0.1390472
  23. Ino-ue, M., Ohgiya, N. and Yamamoto, M. (1998a). Effect of aminoguanidine on optic nerve involvement in experimental diabetic rats. Brain Res. 800, 319-322. https://doi.org/10.1016/S0006-8993(98)00512-5
  24. Ino-ue, M., Yokogawa, H., Yamamoto, M., Naka, H. and Kuriyama, H. (1991). Structural impairments in optic nerve of diabetic rats ameliorated mesangial expansion and tissue fluorescence in streptozotocin-induced diabetic rat. Diabetes 40, 1328-1334. https://doi.org/10.2337/diabetes.40.10.1328
  25. Ino-ue, M., Yokogawa, H., Yamamoto, M., Naka, H. and Kuriyama, H. (1998b). Structural impairments in optic nerve of diabetic ameliorated with the aldose reductase inhibitor. Exp. Eye Res. 66. 397-401. https://doi.org/10.1006/exer.1997.0426
  26. Kang, E. S., Han, D., Park, J., Kwak, T. K., Oh, M. A., Lee, S. A., Choi, S., Park, Z. Y., Kim, Y. and Lee, J. W. (2008). OGlcNAc modulation at Akt1 Ser473 correlates with apoptosis of murine pancreatic beta cells. Exp. Cell Res. 314, 2238-2248. https://doi.org/10.1016/j.yexcr.2008.04.014
  27. Lewis, G. P., Erickson, P. A., Guerin, C. J., Anderson, D. H. and Fisher, S. K. (1989). Changes in the expression of specific Muller cell proteins during long-term retinal detachment. Exp. Eye Res. 49, 93-111. https://doi.org/10.1016/0014-4835(89)90079-1
  28. Lieth, E., Barber, A. J., Xu, B., Dice, C., Ratz, M. J., Tanase, D. and Strother, J. M. (1998). Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Diabetes 47, 815-820. https://doi.org/10.2337/diabetes.47.5.815
  29. Lieth, E., Gardner, T. W., Barber, A. J. and Antontti,. D. A. (2000). Retinal neurodegeneration: early pathology in diabetes. Clinic. Exp. Opthalmol. 28, 3-8. https://doi.org/10.1046/j.1442-9071.2000.00222.x
  30. Liu, F., Shi, J., Tanimukai, H., Gu, J., Gu, J., Grundke-Iqbal, I., Iqbal, K. and Gong C. X. (2009). Reduced O-GlcNAcyclation links lower brain glucose metabolism and tau pathology in Alzheimers disease. Brain Res. 132, 1820-1832.
  31. Liu, K., Paterson, A. J., Chinn, E. and Kudlow, J. E. (2000). Glucose stimulates protein modification by O-linked GlcNAc in pancreatic beta cells: Linkage of O-linked GlcNAc to beta cell death. Proc. Natl. Acad. Sci. USA 97, 2820-2825. https://doi.org/10.1073/pnas.97.6.2820
  32. Longo, J. G., Powell, H. C., Le Beau, J., Gerrero, M. R., Heckman, H. and Myers, R. R. (1985). Delayed nerve regeneration in streptozotocin-diabetic rats. Muscle Nerve 9, 385-393. https://doi.org/10.1002/mus.880090502
  33. Marshall, S., Bacote, V. and Traxinger, P. R. (1991). Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance. J. Biol. Chem. 266, 4706-4712.
  34. Nakamura, M., Barber, A. J., Antonetti, D. A., Lanoue, K. F., Robinson, K. A., Bruse, M. G. and Gardner, T. W. (2001). Excessive hexosamines block the neuroprotective effect of insulin and induce apoptosis in retinal neurons. J. Biol. Chem. 276, 43748-43755. https://doi.org/10.1074/jbc.M108594200
  35. Newman, E. and Reichenbach, A. (1996). The Muller cell: a functional element of the retina. Trends Neurosci. 19, 307-312. https://doi.org/10.1016/0166-2236(96)10040-0
  36. Nork, T. M., Wallow, I. H. L., Sramek, S. J. and Anderson, G. (1987). Muller's cell involvement in proliferative diabetic retinopathy. Arch. Opthalmol. 105, 1424-1429. https://doi.org/10.1001/archopht.1987.01060100126042
  37. Rex-Mathen, M., Werner, S., Strutas, D., Griffith, L. S., Viebahn, C., Thelen, K. and Schmitz, B. (2001). O-GlcNAc expression in developing and ageing mouse. Brain Biochimie. 83, 583-590. https://doi.org/10.1016/S0300-9084(01)01305-0
  38. Robinson, K. A., Sens, D. A. and Bruce, M. G. (1993). Preexposure to glucosamine induce insulin resistance of glucose transport and glycogen synthesis in isolated rat skeletal muscles. Diabetes 42, 1333-1346. https://doi.org/10.2337/diabetes.42.9.1333
  39. Rosseti, L., Hwakins, M., Chen, W., Gindi, J. and Birazali, N. (1995). In vivo glucosamine infusion induces insulin resistance in normoglycermic but not hyperglycemic conscious rats. J. Clin. Investi. 96, 132-140. https://doi.org/10.1172/JCI118013
  40. Sarthy, P. V. and Fu, M. (1989). Transcriptional activation an intermediate filament protein gene in mice with retinal dystrophy. DNA 8, 437-446. https://doi.org/10.1089/dna.1.1989.8.437
  41. Sima, A., Zhang, W., Cherian, P. and Chakrabarti, S. (1992). Impaired visual evoked potential and primary axonopathy of the optic nerve in diabetic BB/W-rat. Diabetologia 35, 602-607. https://doi.org/10.1007/BF00400249
  42. Snow, D. M. and Hart, G. W. (1998). Nuclear and cytoplasmic glycosylation. Int. Rev. Cytol. 181, 43-74. https://doi.org/10.1016/S0074-7696(08)60416-7
  43. Tallent, M. K., Varghis, N., Skorobogatko, Y., Hernandez- Cuebas, L., Whelan, K., Vocadlo, D. J. and Vosseller, K. (2009). In vivo modulation of O-GlcNAc levels regulates hippocampal synaptic plasticity through interplay with phosphorylation. J. Biol. Chem. 284, 174-181. https://doi.org/10.1074/jbc.M807431200
  44. Tout, S., Chan-Ling, T., Hollander, H. and Stone, J. (1993). The role of Muller cells in the formation of the blood-retinal barrier. Neuroscience 55, 291-301. https://doi.org/10.1016/0306-4522(93)90473-S
  45. Vinik, A. I., Erbas, T., Stansberry, K. B. and Pittenger, G. L. (2001). Small fiber neuropathy and neurovascular disturbances in diabetes mellitus. Exp. Clin. Endocrinol. Diabetes 109, S451-473. https://doi.org/10.1055/s-2001-18602
  46. Virkamaki, A., Daniel, M. C., Hamalainen, S. Ultriainen, T., Mc- Clain, D. and Yki-Jarvinen, N. (1997). Activation of the hexosamine pathway by glucosamine in vivo induces insulin resistance in multiple insulin sensitive tissue. Endocrinology 138, 2501-2507. https://doi.org/10.1210/en.138.6.2501
  47. Vlassara, H., Fuh, H., Makifa, Z., Krungkrai, S., Cerami, A. and Bucala, K. (1992). Exogenous advanced glycosylation end products induce complex vascular dysfunction in normal animals: a model for diabetic and aging complications. Proc. Natl. Acad. Sci. USA 84, 12043-12047. https://doi.org/10.1073/pnas.89.24.12043
  48. Walker, D., Carrington, A., Cannan, S. A., Sawicki, D., Sredy, J., Boulton, A. J. M. and Malik, R. A. (1999). Structural abnormalities do not explain the early functional abnormalities in the peripheral nerves of the streptozotocin diabetic rat. J. Anat. 195, 419-427. https://doi.org/10.1046/j.1469-7580.1999.19530419.x
  49. Wells, L., Vosseller, K. and Hart, G. W. (2003). A role for N-acetylglucosamine as a nutrient sensor and mediator of insulin resistance. Cell Mol. Life Sci. 60, 222-228. https://doi.org/10.1007/s000180300017
  50. Yanko, L., Ticho, U. and Ivry, M. (1972). Optic nerve involvement in diabetes. Acta. Ophthalmol. 50, 556-564. https://doi.org/10.1111/j.1755-3768.1972.tb05984.x
  51. Yao, P. J. and Coleman, P. D. (1998). Reduction of O-linked Nacetylglucosamine- modified assembly protein-3 in Alzheimer's disease. J. Neurosci. 18, 2399-2411.

Cited by

  1. Modulation of NMDA Receptor Subunits Expression by Concanavalin A vol.41, pp.8, 2016, https://doi.org/10.1007/s11064-016-1900-6