APOE isoforms control pathogenic subretinal inflammation in age-related macular degeneration

Journal of Neuroscience

Volumn 35, Issue 40, 2015, Pages 13568-13576

  Levy, Olivier ^a,b,c   Lavalette, Sophie ^a,b,c   Hu, Shulong J ^a,b,c   Housset, Michael ^a,b,c   Raoul, William ^a,b,c   Eandi, Chiara ^e   Sahel, José Alain ^a,b,c,d   Sullivan, Patrick M ^f   Guillonneau, Xavier ^a,b,c   Sennlaub, Florian ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DE LA VISION   (France)

^d CENTRE HOSPITALIER NATIONAL D OPHTALMOLOGIE DES QUINZE VINGTS   (France)

^e UNIVERSITY OF TURIN   (Italy)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apolipoprotein E; Mononuclear phagocyte; Neurodegeneration; Neuroinflammation

Indexed keywords

APOLIPOPROTEIN E; CHEMOKINE RECEPTOR CX3CR1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; CHEMOKINE RECEPTOR; CRB1 PROTEIN, HUMAN; CX3CR1 PROTEIN, HUMAN; CYTOKINE; EYE PROTEIN; ISOPROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN;

AGE RELATED MACULAR DEGENERATION; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE FREQUENCY; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC PREDISPOSITION; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MALE; MOUSE; NERVE DEGENERATION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINA DEGENERATION; RETINITIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBRETINAL NEOVASCULARIZATION; ADVERSE EFFECTS; AGING; ANIMAL; CELL CULTURE; COMPLICATION; CYTOLOGY; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INFLAMMATION; LASER; MACULAR DEGENERATION; METABOLISM; RETINA; TRANSGENIC MOUSE;

AGING; ANIMALS; APOLIPOPROTEINS E; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LASERS; MACULAR DEGENERATION; MALE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; PROTEIN ISOFORMS; RECEPTORS, CHEMOKINE; RETINA;

EID: 84944039457     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2468-15.2015     Document Type: Article

References (43)

1. Anderson DH, Ozaki S, Nealon M, Neitz J, Mullins RF, Hageman GS, Johnson LV (2001) Local cellular sources of apolipoprotein E in the human retina and retinal pigmented epithelium: implications for the process of drusen formation. Am J Ophthalmol 131:767-781. CrossRef Medline
2. Bales KR, Liu F, Wu S, Lin S, Koger D, DeLong C, Hansen JC, Sullivan PM, Paul SM (2009) Human APOE isoform-dependent effects on brain beta-amyloid levels in PDAPP transgenic mice. J Neurosci 29:6771-6779. CrossRef Medline
3. Chalam KV, Grover S, Sambhav K, Balaiya S, Murthy RK (2014) Aqueous interleukin-6 levels are superior to vascular endothelial growth factor in predicting therapeutic response to bevacizumab in age-related macular degeneration. J Ophthalmol 2014:502174. CrossRef Medline
4. Chen M, Luo C, Penalva R, XuH (2013) Paraquat-induced retinal degeneration is exaggerated in CX3CR1-deficient mice and is associated with increased retinal inflammation. Invest Ophthalmol Vis Sci 54:682-690. CrossRef Medline
5. Chen W, Stambolian D, Edwards AO, Branham KE, Othman M, Jakobsdottir J, Tosakulwong N, Pericak-Vance MA, Campochiaro PA, Klein ML, Tan PL, Conley YP, Kanda A, Kopplin L, Li Y, Augustaitis KJ, Karoukis AJ, Scott WK, Agarwal A, Kovach JL, et al. (2010) Genetic variants near TIMP3 and high-density lipoprotein-associated loci influence susceptibility to age-related macular degeneration. Proc Natl Acad Sci U S A 107: 7401-7406. CrossRef Medline
6. Chinnery HR, McLenachan S, Humphries T, Kezic JM, Chen X, Ruitenberg MJ, McMenamin PG (2011) Accumulation of murine subretinal macrophages: effects of age, pigmentation and CX(3)CR1. Neurobiol Aging 33:1769-1776. CrossRef Medline
7. Combadière C, Feumi C, Raoul W, Keller N, RodéroM, Pézard A, Lavalette S, Houssier M, Jonet L, Picard E, Debré P, Sirinyan M, Deterre P, Ferroukhi T, Cohen SY, Chauvaud D, Jeanny JC, Chemtob S, Behar-Cohen F, Sennlaub F (2007) CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest 117:2920-2928. CrossRef Medline
8. Dong LM, Weisgraber KH (1996) Human apolipoprotein E4 domain interaction: arginine 61 and glutamic acid 255 interact to direct the preference for very low density lipoproteins. J Biol Chem 271:19053-19057. CrossRef Medline
9. Fryer JD, Demattos RB, McCormick LM, O'Dell MA, Spinner ML, Bales KR, Paul SM, Sullivan PM, Parsadanian M, Bu G, HoltzmanDM (2005) The low density lipoprotein receptor regulates the level of central nervous system human and murine apolipoprotein E but does not modify amyloid plaque pathology in PDAPP mice. J Biol Chem 280:25754-25759. CrossRef Medline
10. Guo C, Otani A, Oishi A, Kojima H, Makiyama Y, Nakagawa S, Yoshimura N (2012) Knockout of ccr2 alleviates photoreceptor cell death in a model of retinitis pigmentosa. Exp Eye Res 104:39-47. CrossRef Medline
11. Gupta N, Brown KE, Milam AH (2003) Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res 76:463-471. CrossRef Medline
12. Heeren J, Grewal T, Laatsch A, Becker N, Rinninger F, Rye KA, Beisiegel U (2004) Impaired recycling of apolipoprotein E4 is associated with intracellular cholesterol accumulation. J Biol Chem 279:55483-55492. CrossRef Medline
13. Hu SJ, Calippe B, Lavalette S, Roubeix C, Montassar F, Housset M, Levy O, Delarasse C, Paques M, Sahel JA, Sennlaub F, Guillonneau X (2015) Upregulation of P2RX7 in Cx3cr1-deficient mononuclear phagocytes leads to increased interleukin-1beta secretion and photoreceptor neurodegeneration. J Neurosci 35:6987-6996. CrossRef Medline
14. Jonas JB, Tao Y, Neumaier M, Findeisen P (2010) Monocyte chemoattractant protein 1, intercellular adhesion molecule 1, and vascular cell adhesion molecule 1 in exudative age-related macular degeneration. Arch Ophthalmol 128:1281-1286. CrossRef Medline
15. Kezic JM, Chen X, Rakoczy EP, McMenamin PG (2013) The effects of age and Cx3cr1 deficiency on retinal microglia in the Ins2Akita diabetic mouse. Invest Ophthalmol Vis Sci 54:854-863. CrossRef Medline
16. Klaver CC, Kliffen M, van Duijn CM, Hofman A, Cruts M, Grobbee DE, van Broeckhoven C, de Jong PT (1998) Genetic association of apolipoprotein E with age-related macular degeneration. Am J Hum Genet 63:200-206. CrossRef Medline
17. Kohno H, Chen Y, Kevany BM, Pearlman E, Miyagi M, Maeda T, Palczewski K, Maeda A (2013) Photoreceptor proteins initiate microglial activation via Toll-like receptor 4 in retinal degeneration mediated by all-transretinal. J Biol Chem 288:15326-15341. CrossRef Medline
18. KossMJ, HoffmannJ, NguyenN, PfisterM, MischakH, MullenW, HusiH, RejdakR, Koch F, Jankowski J, Krueger K, Bertelmann T, Klein J, Schanstra JP, Siwy J (2014) Proteomics of vitreous humor of patients with exudative age-related macular degeneration. PLoS One 9:e96895. CrossRef Medline
19. Lee S, Varvel NH, Konerth ME, Xu G, Cardona AE, Ransohoff RM, Lamb BT (2010) CX3CR1 deficiency alters microglial activation and reduces betaamyloid deposition in two Alzheimer's disease mouse models. Am J Pathol 177:2549-2562. CrossRef Medline
20. Levy O, Calippe B, Lavalette S, Hu SJ, Raoul W, Dominguez E, Housset M, Paques M, Sahel JA, Bemelmans AP, Combadière C, Guillonneau X, Sennlaub F (2015) Apolipoprotein E promotes subretinal mononuclear phagocyte survival and chronic inflammation in age-related macular degeneration. EMBO Mol Med 7:211-226. CrossRef Medline
21. Liu J, Copland DA, Horie S, WuWK, Chen M, Xu Y, Paul Morgan B, Mack M, Xu H, Nicholson LB, Dick AD (2013) Myeloid cells expressing VEGF and arginase-1 following uptake of damaged retinal pigment epithelium suggests potential mechanism that drives the onset of choroidal angiogenesis in mice. PLoS One 8:e72935. CrossRef Medline
22. Luhmann UF, Carvalho LS, Robbie SJ, Cowing JA, Duran Y, Munro PM, Bainbridge JW, Ali RR (2013) Ccl2, Cx3cr1 and Ccl2/Cx3cr1 chemokine deficiencies are not sufficient to cause age-related retinal degeneration. Exp Eye Res 107:80-87. CrossRef Medline
23. Mahley RW, Rall SC Jr (2000) Apolipoprotein E: far more than a lipid transport protein. Annu Rev GenomicsHumGenet 1:507-537. CrossRef Medline
24. Mahley RW, Weisgraber KH, Huang Y (2009) Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS. J Lipid Res 50 [Suppl]:S183-S188.
25. Malek G, Johnson LV, Mace BE, Saloupis P, Schmechel DE, Rickman DW, Toth CA, Sullivan PM, Bowes Rickman C (2005) Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration. Proc Natl Acad Sci U S A 102:11900-11905. CrossRef Medline
26. Mattapallil MJ, Wawrousek EF, Chan CC, Zhao H, Roychoudhury J, Ferguson TA, CaspiRR (2012) The rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest Ophthalmol Vis Sci 53:2921-2927. CrossRef Medline
27. McKay GJ, Patterson CC, Chakravarthy U, Dasari S, Klaver CC, Vingerling JR, Ho L, de Jong PT, Fletcher AE, Young IS, Seland JH, Rahu M, Soubrane G, Tomazzoli L, Topouzis F, Vioque J, Hingorani AD, Sofat R, Dean M, Sawitzke J, et al. (2011) Evidence of association of APOE with agerelated macular degeneration: a pooled analysis of 15 studies.HumMutat 32:1407-1416. CrossRef Medline
28. Ong JM, Zorapapel NC, Rich KA, Wagstaff RE, Lambert RW, Rosenberg SE, Moghaddas F, Pirouzmanesh A, Aoki AM, KenneyMC (2001) Effects of cholesterol and apolipoprotein E on retinal abnormalities in ApoEdeficient mice. Invest Ophthalmol Vis Sci 42:1891-1900. Medline
29. Penfold PL, Madigan MC, Gillies MC, Provis JM (2001) Immunological and aetiological aspects of macular degeneration. Prog Retin Eye Res 20:385-414. CrossRef Medline
30. Peng B, Xiao J, Wang K, So KF, Tipoe GL, Lin B (2014) Suppression of microglial activation is neuroprotective in a mouse model of human retinitis pigmentosa. J Neurosci 34:8139-8150. CrossRef Medline
31. Peri F, Nüsslein-Volhard C (2008) Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 133:916-927. CrossRef Medline
32. Riddell DR, Zhou H, Atchison K, Warwick HK, Atkinson PJ, Jefferson J, Xu L, Aschmies S, Kirksey Y, HuY, Wagner E, Parratt A, Xu J, Li Z, ZaleskaMM, Jacobsen JS, Pangalos MN, Reinhart PH (2008) Impact of apolipoprotein E (ApoE) polymorphism on brain ApoE levels. J Neurosci 28:11445-11453. CrossRef Medline
33. Rosenfeld ME, Butler S, Ord VA, Lipton BA, Dyer CA, Curtiss LK, Palinski W, Witztum JL (1993) Abundant expression of apoprotein E by macrophages in human and rabbit atherosclerotic lesions. Arterioscler Thromb 13:1382-1389. CrossRef Medline
34. Rutar M, Natoli R, Provis JM (2012) Small interfering RNA-mediated suppression of Ccl2 in Muller cells attenuates microglial recruitment and photoreceptor death following retinal degeneration. J Neuroinflammation 9:221. CrossRef Medline
35. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J (2003) Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44:3578-3585. CrossRef Medline
36. Seddon JM, George S, Rosner B, Rifai N (2005) Progression of age-related macular degeneration: prospective assessment of C-reactive protein, interleukin 6, and other cardiovascular biomarkers. Arch Ophthalmol 123: 774-782. CrossRef Medline
37. Sennlaub F, Auvynet C, Calippe B, Lavalette S, Poupel L, HuSJ, Dominguez E, Camelo S, Levy O, Guyon E, Saederup N, Charo IF, Rooijen NV, Nandrot E, Bourges JL, Behar-Cohen F, Sahel JA, Guillonneau X, Raoul W, Combadière C (2013) CCR2(+) monocytes infiltrate atrophic lesions in agerelated macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice. EMBO Mol Med 5:1775-1793. CrossRef Medline
38. Smoak KA, Aloor JJ, Madenspacher J, Merrick BA, Collins JB, Zhu X, Cavigiolio G, Oda MN, Parks JS, Fessler MB (2010) Myeloid differentiation primary response protein 88 couples reverse cholesterol transport to inflammation. Cell Metab 11:493-502. CrossRef Medline
39. Sullivan PM, Mezdour H, Aratani Y, Knouff C, Najib J, Reddick RL, Quarfordt SH, Maeda N (1997) Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 272: 17972-17980. CrossRef Medline
40. Sullivan PM, Han B, Liu F, Mace BE, Ervin JF, Wu S, Koger D, Paul S, Bales KR (2011) Reduced levels ofhumanapoE4 protein in an animal model of cognitive impairment. Neurobiol Aging 32:791-801. CrossRef Medline
41. SuzukiM, TsujikawaM, ItabeH, DuZJ, XieP, MatsumuraN, FuX, ZhangR, Sonoda KH, Egashira K, Hazen SL, Kamei M (2012) Chronic photo-oxidative stress and subsequent MCP-1 activation as causative factors for age-related macular degeneration. J Cell Sci 125:2407-2415. CrossRef Medline
42. Tsutsumi C, Sonoda KH, Egashira K, Qiao H, Hisatomi T, Nakao S, Ishibashi M, Charo IF, Sakamoto T, Murata T, Ishibashi T (2003) The critical role of ocular-infiltrating macrophages in the development of choroidal neovascularization. J Leukoc Biol 74:25-32. CrossRef Medline
43. Yu CE, Cudaback E, Foraker J, Thomson Z, Leong L, Lutz F, Gill JA, Saxton A, Kraemer B, Navas P, Keene CD, Montine T, Bekris LM (2013) Epigenetic signature and enhancer activity of the human APOE gene.HumMol Genet 22:5036-5047. CrossRef Medline