Spermidine ameliorates neurodegeneration in a mouse model of normal tension glaucoma

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 8, 2015, Pages 5012-5019

  Noro, Takahiko ^a,b   Namekata, Kazuhiko ^a   Azuchi, Yuriko ^a   Kimura, Atsuko ^a   Guo, Xiaoli ^a   Harada, Chikako ^a   Nakano, Tadashi ^b   Tsuneoka, Hiroshi ^b   Harada, Takayuki ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Animal model; Glaucoma; Neuroprotection; Oxidative stress; Spermidine

Indexed keywords

4 HYDROXYNONENAL; EXCITATORY AMINO ACID TRANSPORTER 3; SPERMIDINE; SLC1A1 PROTEIN, MOUSE;

ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAM; HISTOPATHOLOGY; IMAGING; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; LOW TENSION GLAUCOMA; MOUSE; NERVE DEGENERATION; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; RETINA DEGENERATION; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; VISION; VISUAL IMPAIRMENT; ANIMAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ELECTRORETINOGRAPHY; GENETICS; KNOCKOUT MOUSE; ORAL DRUG ADMINISTRATION; PATHOLOGY; PATHOPHYSIOLOGY; RETINA; RETINAL DEGENERATION;

ADMINISTRATION, ORAL; ANIMALS; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; EXCITATORY AMINO ACID TRANSPORTER 3; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; LOW TENSION GLAUCOMA; MICE; MICE, KNOCKOUT; RETINA; RETINAL DEGENERATION; SPERMIDINE; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84939782527     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-17142     Document Type: Article

References (50)

1. Lindsey JD, Weinreb RN. Elevated intraocular pressure and transgenic applications in the mouse. J Glaucoma. 2005;14: 318–320.
2. Quigley HA. Number of people with glaucoma worldwide. Br J Ophthalmol. 1996;80:389–393.
3. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:262–267.
4. Iwase A, Suzuki Y, Araie M, et al. The prevalence of primary open-angle glaucoma in Japanese: the Tajimi Study. Ophthalmology. 2004;111:1641–1648.
5. Desai PV, Caprioli J. The treatment of normal-tension glaucoma. Prog Brain Res. 2008;173:195–210.
6. Harada T, Harada C, Nakamura K, et al. The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. J Clin Invest. 2007;117:1763–1770.
7. Osborne NN. Pathogenesis of ganglion ‘‘cell death’’ in glaucoma and neuroprotection: focus on ganglion cell axonal mitochondria. Prog Brain Res. 2008;173:339–352.
8. Naskar R, Vorwerk CK, Dreyer EB. Concurrent downregulation of a glutamate transporter and receptor in glaucoma. Invest Ophthalmol Vis Sci. 2000;41:1940–1944.
9. Gherghel D, Mroczkowska S, Qin L. Reduction in blood glutathione levels occurs similarly in patients with primaryopen angle or normal tension glaucoma. Invest Ophthalmol Vis Sci. 2013;54:3333–3339.
10. Goyal A, Srivastava A, Sihota R, Kaur J. Evaluation of oxidative stress markers in aqueous humor of primary open angle glaucoma and primary angle closure glaucoma patients. Curr Eye Res. 2014;39:823–829.
11. Namekata K, Kimura A, Kawamura K, et al. Dock3 attenuates neural cell death due to NMDA neurotoxicity and oxidative stress in a mouse model of normal tension glaucoma. Cell Death Differ. 2013;20:1250–1256.
12. Harada C, Namekata K, Guo X, et al. ASK1 deficiency attenuates neural cell death in GLAST-deficient mice, a model of normal tension glaucoma. Cell Death Differ. 2010;17:1751–1759.
13. Semba K, Namekata K, Kimura A, et al. Renin-angiotensin system regulates neurodegeneration in a mouse model of normal tension glaucoma. Cell Death Dis. 2014;5:e1333.
14. Semba K, Namekata K, Kimura A, et al. Brimonidine prevents neurodegeneration in a mouse model of normal tension glaucoma. Cell Death Dis. 2014;5:e1341.
15. Kimura A, Guo X, Noro T, et al. Valproic acid prevents retinal degeneration in a murine model of normal tension glaucoma. Neurosci Lett. 2015;588:108–113.
16. Dornay M, Gilad VH, Shiler I, Gilad GM. Early polyamine treatment accelerates regeneration of rat sympathetic neurons. Exp Neurol. 1986;92:665–674.
17. Slotkin TA, Bartolome J. Role of ornithine decarboxylase and the polyamines in nervous system development: a review. Brain Res Bull. 1986;17:307–320.
18. Gilad GM, Gilad VH. Early polyamine treatment enhances survival of sympathetic neurons after postnatal axonal injury or immunosympathectomy. Brain Res. 1988;466:175–181.
19. Gilad VH, Tetzlaff WG, Rabey JM, Gilad GM. Accelerated recovery following polyamines and aminoguanidine treatment after facial nerve injury in rats. Brain Res. 1996;724:141–144.
20. Laube G, Veh RW. Astrocytes, not neurons, show most prominent staining for spermidine/spermine-like immunoreactivity in adult rat brain. Glia. 1997;19:171–179.
21. Biedermann B, Skatchkov SN, Bringmann A, et al. Spermine/ spermidine is expressed by retinal glial (Müller) cells, and controls distinct Kþ channels of their membrane. Glia. 1998; 23:209–220.
22. Rider JE, Hacker A, Mackintosh CA, et al. Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids. 2007;33:231–240.
23. Eisenberg T, Knauer H, Schauer A, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol. 2009;11:1305–1314.
24. Guo X, Harada C, Namekata K, et al. Spermidine alleviates severity of murine experimental autoimmune encephalomyelitis. Invest Ophthalmol Vis Sci. 2011;52:2696–2703.
25. Noro T, Namekata K, Kimura A, et al. Spermidine promotes retinal ganglion cell survival and optic nerve regeneration in adult mice following optic nerve injury. Cell Death Dis. 2015; 6:e1720.
26. Katome T, Namekata K, Guo X, et al. Inhibition of ASK1-p38 pathway prevents neural cell death following optic nerve injury. Cell Death Differ. 2013;20:270–280.
27. Harada C, Nakamura K, Namekata K, et al. Role of apoptosis signal-regulating kinase 1 in stress-induced neural cell apoptosis in vivo. Am J Pathol. 2006;168:261–269.
28. Aihara M, Lindsey JD, Weinreb RN. Twenty-four-hour pattern of mouse intraocular pressure. Exp Eye Res. 2003;77:681–686.
29. Bearse MA Jr, Sutter EE, Sim D, Stamper R. Glaucomatous dysfunction revealed in higher order components of the electroretinogram. Vis Sci App. 1996;1:105–107.
30. Majima HJ, Nakanishi-Ueda T, Ozawa T. 4-hydroxy-2-nonenal (4-HNE) staining by anti-HNE antibody. Methods Mol Biol. 2002;196:31–34.
31. Namekata K, Kimura A, Kawamura K, Harada C, Harada T. Dock GEFs and their therapeutic potential: neuroprotection and axon regeneration. Prog Retin Eye Res. 2014;43:1–16.
32. Osborne NN, del Olmo-Aguado S. Maintenance of retinal ganglion cell mitochondrial functions as a neuroprotective strategy in glaucoma. Curr Opin Pharmacol. 2013;13:16–22.
33. Farbiszewski R, Bielawski K, Bielawska A, Sobaniec W. Spermine protects in vivo the antioxidant enzymes in transiently hypoperfused rat brain. Acta Neurobiol Exp. 1995;55:253–258.
34. Adibhatla RM, Hatcher JF, Sailor K, Dempsey RJ. Polyamines and central nervous system injury: spermine and spermidine decrease following transient focal cerebral ischemia in spontaneously hypertensive rats. Brain Res. 2002;938:81–86.
35. Soga M, Matsuzawa A, Ichijo H. Oxidative stress-induced diseases via the ASK1 signaling pathway. Int J Cell Biol. 2012; 2012:439587.
36. Kawarazaki Y, Ichijo H, Naguro I. Apoptosis signal-regulating kinase 1 as a therapeutic target. Expert Opin Ther Targets. 2014;18:651–664.
37. Guo X, Harada C, Namekata K, et al. Regulation of the severity of neuroinflammation and demyelination by TLR-ASK1-p38 pathway. EMBO Mol Med. 2010;2:504–515.
38. Skatchkov SN, Woodbury-Farina MA, Eaton M. The role of glia in stress: polyamines and brain disorders. Psychiatr Clin North Am. 2014;37:653–678.
39. Harada T, Harada C, Nakayama N, et al. Modification of glialneuronal cell interactions prevents photoreceptor apoptosis during light-induced retinal degeneration. Neuron. 2000;26: 533–541.
40. Harada T, Harada C, Kohsaka S, et al. Microglia-Muller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci. 2002;22:9228–9236.
41. Harada C, Guo X, Namekata K, et al. Glia- and neuron-specific functions of TrkB signalling during retinal degeneration and regeneration. Nat Commun. 2011;2:189.
42. Pernet V, Bourgeois P, Di Polo A. A role for polyamines in retinal ganglion cell excitotoxic death. J Neurochem. 2007; 103:1481–1490.
43. Williams K. Modulation and block of ion channels: a new biology of polyamines. Cell Signal. 1997;9:1–13.
44. Bai N, Hayashi H, Aida T, et al. Dock3 interaction with a glutamate-receptor NR2D subunit protects neurons from excitotoxicity. Mol Brain. 2013;6:22.
45. Namekata K, Harada C, Taya C, et al. Dock3 induces axonal outgrowth by stimulating membrane recruitment of the WAVE complex. Proc Natl Acad Sci U S A. 2010;107:7586–7591.
46. Namekata K, Harada C, Guo X, et al. Dock3 stimulates axonal outgrowth via GSK-3b-mediated microtubule assembly. J Neurosci. 2012;32:264–274.
47. Namekata K, Watanabe H, Guo X, et al. Dock3 regulates BDNFTrkB signaling for neurite outgrowth by forming a ternary complex with Elmo and RhoG. Genes Cells. 2012;17:688–697.
48. Almasieh M, Lieven CJ, Levin LA, Di Polo A. A cell-permeable phosphine-borane complex delays retinal ganglion cell death after axonal injury through activation of the pro-survival extracellular signal-regulated kinases 1/2 pathway. J Neurochem. 2011;118:1075–1086.
49. Kimura A, Namekata K, Guo X, et al. Valproic acid prevents NMDA-induced retinal ganglion cell death via stimulation of neuronal TrkB receptor signaling. Am J Pathol. 2015;185:756–764.
50. Soda K, Kano Y, Sakuragi M, et al. Long-term oral polyamine intake increases blood polyamine concentrations. J Nutr Sci Vitaminol. 2009;55:361–366.