The neuronal egf-related gene nell2 interacts with macf1 and supports survival of retinal ganglion cells after optic nerve injury

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Munemasa, Yasunari ^a,c   Chang, Chang Sheng ^a   Kwong, Jacky M K ^a   Kyung, Haksu ^a   Kitaoka, Yasushi ^c   Caprioli, Joseph ^a,b   Piri, Natik ^a,b  

^a JULES STEIN EYE INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; EPIDERMAL GROWTH FACTOR; MACF1 PROTEIN; MESSENGER RNA; MICROTUBULE PROTEIN; NELL2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; MACF1 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; NELL2 PROTEIN, RAT; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CELL SURVIVAL; CONTROLLED STUDY; GENE; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MACF1 GENE; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NELL2 GENE; NERVE CELL; NONHUMAN; OPTIC NERVE; OPTIC NERVE INJURY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE; ANIMAL; GENE EXPRESSION; GENETICS; METABOLISM; NERVE FIBER TRANSECTION; PHYSIOLOGY; PROTEIN BINDING; WISTAR RAT;

RATTUS;

ANIMALS; AXOTOMY; CELL SURVIVAL; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MICROFILAMENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; OPTIC NERVE INJURIES; PROTEIN BINDING; RATS; RATS, WISTAR; RETINAL GANGLION CELLS;

EID: 84859317344     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034810     Document Type: Article

References (45)

1. Matsuhashi S, Noji S, Koyama E, Myokai F, Ohuchi H, et al. (1995) New gene, nel, encoding a M(r) 93 K protein with EGF-like repeats is strongly expressed in neural tissues of early stage chick embryos. Dev Dyn 203: 212-222.
2. Jiang Y, Obama H, Kuan SL, Nakamura R, Nakamoto C, et al. (2009) In vitro guidance of retinal axons by a tectal lamina-specific glycoprotein. Nel Mol Cell Neurosci 41: 113-9.
3. Watanabe TK, Katagiri T, Suzuki M, Shimizu F, Fujiwara T, et al. (1996) Cloning and characterization of two novel human cDNAs (NELL1 and NELL2) encoding proteins with six EGF-like repeats. Genomics 38: 273-6.
4. Kuroda S, Oyasu M, Kawakami M, Kanayama N, Tanizawa K, et al. (1999) Biochemical characterization and expression analysis of neural thrombospondin-1-like proteins NELL1 and NELL2. Biochem Biophys Res Commun 265: 79-86.
5. Aihara K, Kuroda S, Kanayama N, Matsuyama S, Tanizawa K, et al. (2003) A neuron-specific EGF family protein, NELL2, promotes survival of neurons through mitogen-activated protein kinases. Mol Brain Res 116: 86-93.
6. Rosenblum K, Futter M, Voss K, Erent M, Skehel PA, et al. (2002) The role of extracellular regulated kinases I/II in late-phase long-term potentiation. J Neurosci 22: 5432-41.
7. Vereker E, O'Donnell E, Lynch MA, (2000) The inhibitory effect of interleukin-1beta on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J Neurosci 20: 6811-9.
8. Matsuyama S, Aihara K, Nishino N, Takeda S, Tanizawa K, et al. (2004) Enhanced long-term potentiation in vivo in dentate gyrus of NELL2-deficient mice. Neuroreport 15: 417-20.
9. Piri N, Kwong JM, Song M, Elashoff D, Caprioli J, (2006) Gene expression changes in the retina following optic nerve transection. Mol Vis 12: 1660-73.
10. Dacey DM, Petersen MR, (1992) Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. Proc Natl Acad Sci USA 89: 9666-70.
11. Rodieck RW, Watanabe M, (1993) Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. J Comp Neurol 338: 289-303.
12. Dacey DM, (1999) Primate retina: cell types, circuits and color opponency. Prog Retin Eye Res 18: 737-63.
13. Yamada ES, Silveira LCL, Perry VH, Franco ECS, (2001) M and P retinal ganglion cells of the owl monkey: morphology, size and photoreceptor convergence. Vision Res 41: 119-31.
14. Dacey DM, (1993) The mosaic of midget ganglion cells in the human retina. J Neurosci 13: 5334-55.
15. Schiller PH, Malpeli JG, (1978) Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. J Neurolphysiol 41: 788-97.
16. Jeong JK, Ryu BJ, Choi J, Kim DH, Choi EJ, et al. (2008) NELL2 participates in formation of the sexually dimorphic nucleus of the pre-optic area in rats. J Neurochem 106: 1604-13.
17. Choi EJ, Kim DH, Kim JG, Kim DY, Kim JD, et al. (2010) Estrogen-dependent transcription of the NEL-like 2 (NELL2) gene and its role in protection from cell death. J Biol Chem 285: 25074-84.
18. Nelson BR, Claes K, Todd V, Chaverra M, Lefcort F, (2004) NELL2 promotes motor and sensory neuron differentiation and stimulates mitogenesis in DRG in vivo. Dev Biol 270: 322-35.
19. Kielczewski JL, Pease ME, Quigley HA, (2005) The effect of experimental glaucoma and optic nerve transection on amacrine cells in the rat retina. Invest Ophthalmol Vis Sci 46: 3188-96.
20. Hwang EM, Kim DG, Lee BJ, Choi J, Kim E, et al. (2007) Alternative splicing generates a novel non-secretable cytosolic isoform of NELL2. Biochem Biophys Res Commun 353: 805-11.
21. Davis CG, (1990) The many faces of epidermal growth factor repeats. New Biol 2: 410-9.
22. Kimura H, (1993) Schwannoma-derived growth factor must be transported into the nucleus to exert its mitogenic activity. Proc Natl Acad Sci USA 90: 2165-9.
23. Spencer AG, Woods JW, Arakawa T, Singer II, Smith WL, (1998) Subcellular localization of prostaglandin endoperoxide H synthases-1 and-2 by immunoelectron microscopy. J Biol Chem 273 pp. 86-9893.
24. Oyasu M, Kuroda S, Nakashita M, Fujimiya M, Kikkawa U, et al. (2000) Immunocytochemical localization of a neuron-specific thrombospondin-1-like protein, NELL2: light and electron microscopic studies in the rat brain. Mol Brain Res 76 pp. 151-60.
25. Sonnenberg A, Liem RK, (2007) Plakins in development and disease. Exp Cell Res 313: 2189-203.
26. Leung CL, Sun D, Zheng M, Knowles DR, Liem RK, (1999) Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 147: 1275-86.
27. Goryunov D, He CZ, Lin CS, Leung CL, Liem RK, (2010) Nervous-tissue-specific elimination of microtubule-actin crosslinking factor 1a results in multiple developmental defects in the mouse brain. Mol Cell Neurosci 44: 1-14.
28. Chen HJ, Lin CM, Lin CS, Perez-Olle R, Leung CL, et al. (2006) The role of microtubule actin cross-linking factor 1 (MACF1) in the Wnt signaling pathway. Genes Dev 20: 1933-45.
29. Kim H, Ha CM, Choi J, Choi EJ, Jeon J, et al. (2002) Ontogeny and the possible function of a novel epidermal growth factor-like repeat domain-containing protein, NELL2, in the rat brain. J Neurochem 83: 1389-400.
30. Quigley HA, Dunkelberger GR, Green WR, (1988) Chronic human glaucoma causing selectively greater loss of large optic nerve fibers. Ophthalmology 95: 357-63.
31. Sommer A, Katz J, Quigley HA, Miller NR, Robin AL, et al. (1991) Clinically detectable nerve fiber atrophy precedes the onset of glaucomatous field loss. Arch Ophthalmol 109: 77-83.
32. Glovinsky Y, Quigley HA, Dunkelberger GR, (1991) Retinal ganglion cell loss is size dependent in experimental glaucoma. Invest Ophthalmol Vis Sci 31: 484-91.
33. Paquet-Durand F, Johnson L, Ekstrom P, (2007) Calpain activity in retinal degeneration. J Neurosci Res 85: 693-702.
34. Wang X, Ng YK, Tay SS, (2005) Factors contributing to neuronal degeneration in retinas of experimental glaucomatous rats. J Neurosci Res 5: 674-89.
35. Martin KR, Quigley HA, Zack DJ, Levkovitch-Verbin H, Kielczewski J, et al. (2003) Gene therapy with brain-derived neurotrophic factor as a protection: retinal ganglion cells in a rat glaucoma model. Invest Ophthalmol Vis Sci 10: 4357-65.
36. Ishii Y, Kwong JM, Caprioli J, (2003) Retinal ganglion cell protection with geranylgeranylacetone, a heat shock protein inducer, in a rat glaucoma model. Invest Ophthalmol Vis Sci 44: 1982-92.
37. Tahzib NG, Ransom NL, Reitsamer HA, McKinnon SJ, (2004) Alpha-fodrin is cleaved by caspase-3 in a chronic ocular hypertensive (COH) rat model of glaucoma. Brain Res Bull 6: 491-5.
38. Haefliger IO, Dettmann E, Liu R, Meyer P, Prünte C, et al. (1999) Potential role of nitric oxide and endothelin in the pathogenesis of glaucoma. Surv Ophthalmol 43: S51-8.
39. Schori H, Kipnis J, Yoles E, WoldeMussie E, Ruiz G, et al. (2001) Vaccination for protection of retinal ganglion cells against death from glutamate cytotoxicity and ocular hypertension: implications for glaucoma. Proc Natl Acad Sci USA 98: 3398-403.
40. Munemasa Y, Kim SH, Ahn JH, Kwong JM, Caprioli J, et al. (2008) Protective effect of thioredoxins 1 and 2 in retinal ganglion cells after optic nerve transection and oxidative stress. Invest Ophthalmol Vis Sci 49 pp. 3535-43.
41. Munemasa Y, Kwong JM, Caprioli J, Piri N, (2009) The role of alphaA- and alphaB-crystallins in the survival of retinal ganglion cells after optic nerve axotomy. Invest Ophthalmol Vis Sci 50: 3869-75.
42. Munemasa Y, Ahn JH, Kwong JM, Caprioli J, Piri N, (2009) Redox proteins thioredoxin 1 and thioredoxin 2 support retinal ganglion cell survival in experimental glaucoma. Gene Ther 16: 17-25.
43. Dezawa M, Takano M, Negishi H, Mo X, Oshitari T, et al. (2002) Gene transfer into retinal ganglion cells by in vivo electroporation: a new approach. Micron 33: 1-6.
44. Mo X, Yokoyama A, Oshitari T, Negishi H, Dezawa M, et al. (2002) Rescue of axotomized retinal ganglion cells by BDNF gene electroporation in adult rats. Invest Ophthalmol Vis Sci 43: 2401-5.
45. Ishikawa H, Takano M, Matsumoto N, Sawada H, Ide C, et al. (2005) Effect of GDNF gene transfer into axotomized retinal ganglion cells using in vivo electroporation with a contact lens-type electrode. Gene Ther 12: 289-98.