RNA sequence reveals mouse retinal transcriptome changes early after axonal injury

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Yasuda, Masayuki ^a   Tanaka, Yuji ^a   Ryu, Morin ^a   Tsuda, Satoru ^a   Nakazawa, Toru ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ACTIVATING TRANSCRIPTION FACTOR 4; EARLY GROWTH RESPONSE FACTOR 1; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEME OXYGENASE 1; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ACTIVATING TRANSCRIPTION FACTOR 3 GENE; ACTIVATING TRANSCRIPTION FACTOR 4 GENE; ACTIVATING TRANSCRIPTION FACTOR 5 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; C EBP HOMOLOGOUS PROTEIN GENE; C1QA GENE; C1QB GENE; C1QC GENE; CATION TRANSPORT REGULATOR LIKE 1 GENE; CONTROLLED STUDY; EARLY GROWTH RESPONSE 1 GENE; ENDOPLASMIC RETICULUM STRESS; GENE; GENE EXPRESSION; HEME OXYGENASE 1 GENE; MOUSE; NERVE CRUSH; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE INJURY; RETINA GANGLION CELL; RNA SEQUENCE; SRXN1 GENE; TRANSCRIPTOMICS; TRIBBLE HOMOLOG 3 GENE; UPREGULATION; ANIMAL; CLUSTER ANALYSIS; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HIGH THROUGHPUT SEQUENCING; MALE; METABOLISM; NERVE FIBER; REPRODUCIBILITY; RETINA; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; MICE; OPTIC NERVE INJURIES; REPRODUCIBILITY OF RESULTS; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84899823237     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093258     Document Type: Article

References (79)

1. Kwon YH, Fingert JH, Kuehn MH, Alward WL (2009) Primary open-angle glaucoma. New England Journal of Medicine 360: 1113-1124.
2. Weinreb RN, Khaw PT (2004) Primary open-angle glaucoma. The Lancet 363: 1711-1720. (Pubitemid 38670330)
3. Calkins DJ (2012) Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog Retin Eye Res 31: 702-719.
4. Heijl A, Leske MC, Bengtsson B, Hyman L, Bengtsson B, et al. (2002) Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol 120: 1268-1279. (Pubitemid 36105431)
5. Collaborative Normal-Tension Glaucoma Study Group (1998) The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol 126: 498-505.
6. Hollands H, Johnson D, Hollands S, Simel DL, Jinapriya D, et al. (2013) Do findings on routine examination identify patients at risk for primary open-angle glaucoma? The rational clinical examination systematic review. JAMA : the journal of the American Medical Association 309: 2035-2042.
7. De Moraes CGV, Juthani VJ, Liebmann JM, Teng CC, Tello C, et al. (2011) Risk factors for visual field progression in treated glaucoma. Archives of ophthalmology 129: 562-568.
8. Nakazawa T, Chiba N, Omodaka K, Yokoyama Y, Aizawa N, et al. (2011) Association between optic nerve blood flow and objective examinations in glaucoma patients with generalized enlargement disc type. Clinical ophthalmology (Auckland, NZ): 1549.
9. Himori N, Yamamoto K, Maruyama K, Ryu M, Taguchi K, et al. (2013) Critical role of Nrf2 in oxidative stress-induced retinal ganglion cell death. J Neurochem.
10. Ryu M, Yasuda M, Shi D, Shanab AY, Watanabe R, et al. (2012) Critical role of calpain in axonal damage-induced retinal ganglion cell death. J Neurosci Res 90: 802-815.
11. Fujimoto JG (2003) Optical coherence tomography for ultrahigh resolution in vivo imaging. Nat Biotechnol 21: 1361-1367.
12. Allcutt D, Berry M, Sievers J (1984) A qualitative comparison of the reactions of retinal ganglion cell axons to optic nerve crush in neonatal and adult mice. Brain Res 318: 231-240. (Pubitemid 15200283)
13. Li Y, Schlamp CL, Nickells RW (1999) Experimental induction of retinal ganglion cell death in adult mice. Invest Ophthalmol Vis Sci 40: 1004-1008. (Pubitemid 29153269)
14. Libby RT, Li Y, Savinova OV, Barter J, Smith RS, et al. (2005) Susceptibility to neurodegeneration in a glaucoma is modified by Bax gene dosage. PLoS Genet 1: 17-26.
15. Weinreb RN, Friedman DS, Fechtner RD, Cioffi GA, Coleman AL, et al. (2004) Risk assessment in the management of patients with ocular hypertension. Am J Ophthalmol 138: 458-467. (Pubitemid 39208574)
16. Fischer D, Petkova V, Thanos S, Benowitz LI (2004) Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. The Journal of neuroscience : the official journal of the Society for Neuroscience 24: 8726-8740.
17. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature reviews Genetics 10: 57-63.
18. Tong M, Chan KW, Bao JY, Wong KY, Chen JN, et al. (2012) Rab25 is a tumor suppressor gene with antiangiogenic and anti-invasive activities in esophageal squamous cell carcinoma. Cancer Res 72: 6024-6035.
19. Greenwald JW, Greenwald CJ, Philmus BJ, Begley TP, Gross DC (2012) RNA-seq analysis reveals that an ECF sigma factor, AcsS, regulates achromobactin biosynthesis in Pseudomonas syringae pv. syringae B728a. PLoS One 7: e34804.
20. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. NatMethods 5: 621-628. (Pubitemid 351911867)
21. Ramskold D, Wang ET, Burge CB, Sandberg R (2009) An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol 5: e1000598.
22. Team RC (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.R-project.org.
23. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445. (Pubitemid 37033947)
24. Huang TH, Uthe JJ, Bearson SM, Demirkale CY, Nettleton D, et al. (2011) Distinct peripheral blood RNA responses to Salmonella in pigs differing in Salmonella shedding levels: intersection of IFNG, TLR and miRNA pathways. PLoS One 6: e28768.
25. Kamei S, Chen-Kuo-Chang M, Cazevieille C, Lenaers G, Olichon A, et al. (2005) Expression of the Opa1 mitochondrial protein in retinal ganglion cells: its downregulation causes aggregation of the mitochondrial network. Invest Ophthalmol Vis Sci 46: 4288-4294. (Pubitemid 44264634)
26. Fernandes KA, Harder JM, Kim J, Libby RT (2013) JUN regulates early transcriptional responses to axonal injury in retinal ganglion cells. Exp Eye Res 112: 106-117.
27. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer New York.
28. Ward Jr JH (1963) Hierarchical grouping to optimize an objective function. Journal of the American statistical association 58: 236-244.
29. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, et al. (2013) gplots: Various R programming tools for plotting data. R package version 2.12.1. http://CRAN.R-project.org/package=gplots.
30. Nadal-Nicolas FM, Jimenez-Lopez M, Sobrado-Calvo P, Nieto-Lopez L, Canovas-Martinez I, et al. (2009) Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50: 3860-3868.
31. Kim CY, Kuehn MH, Clark AF, Kwon YH (2006) Gene expression profile of the adult human retinal ganglion cell layer. Mol Vis 12: 1640-1648. (Pubitemid 46050312)
32. Chidlow G, Casson R, Sobrado-Calvo P, Vidal-Sanz M, Osborne NN (2005) Measurement of retinal injury in the rat after optic nerve transection: an RT-PCR study. Mol Vis 11: 387-396. (Pubitemid 41358268)
33. Liang SH, Zhang W, McGrath BC, Zhang P, Cavener DR (2006) PERK (eIF2alpha kinase) is required to activate the stress-activated MAPKs and induce the expression of immediate-early genes upon disruption of ER calcium homoeostasis. Biochem J 393: 201-209. (Pubitemid 43049316)
34. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H (2005) TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24: 1243-1255. (Pubitemid 40516607)
35. Logue SE, Cleary P, Saveljeva S, Samali A (2013) New directions in ER stress-induced cell death. Apoptosis 18: 537-546.
36. Ramayo-Caldas Y, Mach N, Esteve-Codina A, Corominas J, Castello A, et al. (2012) Liver transcriptome profile in pigs with extreme phenotypes of intramuscular fatty acid composition. BMC Genomics 13: 547.
37. Levkovitch-Verbin H, Harris-Cerruti C, Groner Y, Wheeler LA, Schwartz M, et al. (2000) RGC death in mice after optic nerve crush injury: oxidative stress and neuroprotection. Invest Ophthalmol Vis Sci 41: 4169-4174.
38. Villegas-Perez MP, Vidal-Sanz M, Rasminsky M, Bray GM, Aguayo AJ (1993) Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J Neurobiol 24: 23-36. (Pubitemid 23001493)
39. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 14: 4368-4374. (Pubitemid 24200558)
40. Nakazawa T, Takahashi H, Nishijima K, Shimura M, Fuse N, et al. (2007) Pitavastatin prevents NMDA-induced retinal ganglion cell death by suppressing leukocyte recruitment. J Neurochem 100: 1018-1031. (Pubitemid 46213926)
41. Lam TT, Abler AS, Kwong JM, Tso MO (1999) N-methyl-D-aspartate (NMDA)-induced apoptosis in rat retina. Invest Ophthalmol Vis Sci 40: 2391-2397. (Pubitemid 29418396)
42. Siliprandi R, Canella R, Carmignoto G, Schiavo N, Zanellato A, et al. (1992) N-methyl-D-aspartate-induced neurotoxicity in the adult rat retina. Vis Neurosci 8: 567-573.
43. Seki T, Nakatani M, Taki C, Shinohara Y, Ozawa M, et al. (2006) Neuroprotective effect of PACAP against kainic acid-induced neurotoxicity in rat retina. Ann N Y Acad Sci 1070: 531-534. (Pubitemid 44126698)
44. Ehrlich D, Teuchert G, Morgan IG (1987) Specific ganglion cell death induced by intravitreal kainic acid in the chicken retina. Brain Res 415: 342-346. (Pubitemid 17100341)
45. Honjo M, Tanihara H, Kido N, Inatani M, Okazaki K, et al. (2000) Expression of ciliary neurotrophic factor activated by retinal Muller cells in eyes with NMDA- and kainic acid-induced neuronal death. Invest Ophthalmol Vis Sci 41: 552-560. (Pubitemid 30080461)
46. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, et al. (2006) Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci 26: 12633-12641. (Pubitemid 44904557)
47. Kitaoka Y, Kitaoka Y, Kwong JM, Ross-Cisneros FN, Wang J, et al. (2006) TNF-alpha-induced optic nerve degeneration and nuclear factor-kappaB p65. Invest Ophthalmol Vis Sci 47: 1448-1457. (Pubitemid 46780751)
48. Liu Y, Tang L, Chen B (2012) Effects of antioxidant gene therapy on retinal neurons and oxidative stress in a model of retinal ischemia/reperfusion. Free Radic Biol Med 52: 909-915.
49. Nakazawa T, Shimura M, Ryu M, Nishida K, Pages G, et al. (2008) ERK1 plays a critical protective role against N-methyl-D-aspartate-induced retinal injury. J Neurosci Res 86: 136-144.
50. Watkins TA, Wang B, Huntwork-Rodriguez S, Yang J, Jiang Z, et al. (2013) DLK initiates a transcriptional program that couples apoptotic and regenerative responses to axonal injury. Proceedings of the National Academy of Sciences of the United States of America 110: 4039-4044.
51. Almasieh M, Wilson AM, Morquette B, Cueva Vargas JL, Di Polo A (2012) The molecular basis of retinal ganglion cell death in glaucoma. Prog Retin Eye Res 31: 152-181.
52. Chidlow G, Casson R, Sobrado-Calvo P, Vidal-Sanz M, Osborne NN (2005) Measurement of retinal injury in the rat after optic nerve transection: an RT-PCR study. Molecular vision 11: 387-396. (Pubitemid 41358268)
53. Quina LA, Pak W, Lanier J, Banwait P, Gratwick K, et al. (2005) Brn3aexpressing retinal ganglion cells project specifically to thalamocortical and collicular visual pathways. J Neurosci 25: 11595-11604. (Pubitemid 43098452)
54. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson EDO, et al. (2008) Retinal ganglion cells downregulate gene expression and lose their Axons within the optic nerve head in a mouse glaucoma model. Journal of Neuroscience 28: 548-561.
55. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI (2000) Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 20: 4615-4626. (Pubitemid 30396627)
56. Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, et al. (2013) Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 12: 105-118.
57. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
58. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389. (Pubitemid 38489416)
59. Hu Y, Park KK, Yang L, Wei X, Yang Q, et al. (2012) Differential effects of unfolded protein response pathways on axon injury-induced death of retinal ganglion cells. Neuron 73: 445-452.
60. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666. (Pubitemid 30070916)
61. Kumar A, Tikoo S, Maity S, Sengupta S, Sengupta S, et al. (2012) Mammalian proapoptotic factor ChaC1 and its homologues function as gamma-glutamyl cyclotransferases acting specifically on glutathione. EMBO Rep 13: 1095-1101.
62. Mungrue IN, Pagnon J, Kohannim O, Gargalovic PS, Lusis AJ (2009) CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 182: 466-476.
63. Barabasi AL, Gulbahce N, Loscalzo J (2011) Network medicine: a network-based approach to human disease. Nat Rev Genet 12: 56-68.
64. Trichonas G, Murakami Y, Thanos A, Morizane Y, Kayama M, et al. (2010) Receptor interacting protein kinases mediate retinal detachment-induced photoreceptor necrosis and compensate for inhibition of apoptosis. Proc Natl Acad Sci U S A 107: 21695-21700.
65. Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov 3: 205-214.
66. Harada C, Namekata K, Guo X, Yoshida H, Mitamura Y, et al. (2010) ASK1 deficiency attenuates neural cell death in GLAST-deficient mice, a model of normal tension glaucoma. Cell death and differentiation 17: 1751-1759.
67. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116.
68. Singh A, Ling G, Suhasini AN, Zhang P, Yamamoto M, et al. (2009) Nrf2-dependent sulfiredoxin-1 expression protects against cigarette smoke-induced oxidative stress in lungs. Free Radic Biol Med 46: 376-386.
69. Tanaka H, Yamashita T, Yachi K, Fujiwara T, Yoshikawa H, et al. (2004) Cytoplasmic p21(Cip1/WAF1) enhances axonal regeneration and functional recovery after spinal cord injury in rats. Neuroscience 127: 155-164. (Pubitemid 38829161)
70. Chen W, Sun Z, Wang XJ, Jiang T, Huang Z, et al. (2009) Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol Cell 34: 663-673.
71. Crehan H, Holton P, Wray S, Pocock J, Guerreiro R, et al. (2012) Complement receptor 1 (CR1) and Alzheimer's disease. Immunobiology 217: 244-250.
72. Templeton JP, Freeman NE, Nickerson JM, Jablonski MM, Rex TS, et al. (2013) Innate immune network in the retina activated by optic nerve crush. Invest Ophthalmol Vis Sci 54: 2599-2606.
73. Shanab AY, Nakazawa T, Ryu M, Tanaka Y, Himori N, et al. (2012) Metabolic stress response implicated in diabetic retinopathy: The role of calpain, and the therapeutic impact of calpain inhibitor. Neurobiology of disease 48: 556-567.
74. Prat-Vidal C, Gálvez-Montón C, Nonell L, Puigdecanet E, Astier L, et al. (2013) Identification of Temporal and Region-Specific Myocardial Gene Expression Patterns in Response to Infarction in Swine. PLoS ONE 8: e54785.
75. Saili KS, Tilton SC, Waters KM, Tanguay RL (2013) Global gene expression analysis reveals pathway differences between teratogenic and non-teratogenic exposure concentrations of bisphenol A and 17β-estradiol in embryonic zebrafish. Reproductive Toxicology 38: 89-101.
76. Gusberti M, Gessler C, Broggini GA (2013) RNA-Seq Analysis Reveals Candidate Genes for Ontogenic Resistance in Malus-Venturia Pathosystem. PLoS One 8: e78457.
77. Rowley JW, Weyrich AS (2013) Coordinate expression of transcripts and proteins in platelets. Blood 121: 5255-5256.
78. Dabney A, Storey JD qvalue: Q-value estimation for false discovery rate control. R package version 1.36.0.
79. Folkersen L, Kyriakou T, Goel A, Peden J, Malarstig A, et al. (2009) Relationship between CAD risk genotype in the chromosome 9p21 locus and gene expression. Identification of eight new ANRIL splice variants. PLoS One 4: e7677.