Sialoadhesin expression in intact degenerating retinas and following transplantation

Investigative Ophthalmology and Visual Science

Volumn 49, Issue 12, 2008, Pages 5602-5610

  Sancho Pelluz, Javier ^a,b,c   Wunderlich, Kirsten A ^a   Rauch, Uwe ^a   Romero, F Javier ^b   Van Veen, Theo ^a,c   Limb, G Astrid ^d   Crocker, Paul R ^e   Perez, Maria Thereza ^a,f  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SIALOADHESIN; ERYTHROCYTE RECEPTOR; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; N ACETYLNEURAMINIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVATION; CHOROID; CILIARY BODY; CONTROLLED STUDY; CORNEA; GRAFT SURVIVAL; GRAFT VERSUS HOST REACTION; MACROPHAGE; MACROPHAGE ACTIVATION; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEGENERATION; SCLERA; SURVIVAL TIME; TISSUE TRANSPLANTATION; VITREOUS BODY; ANIMAL; C3H MOUSE; C57BL MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GENE; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; RETINA; TRANSGENIC MOUSE; TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD; ANTIGENS, CD11B; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENES, MHC CLASS II; GREEN FLUORESCENT PROTEINS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MICROGLIA; N-ACETYLNEURAMINIC ACID; RECEPTORS, IMMUNOLOGIC; RETINA; RETINAL DEGENERATION;

EID: 58149241252     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-2117     Document Type: Article

References (75)

1. Kennan A, Aherne A, Humphries P. Light in retinitis pigmentosa. Trends Genet. 2005;21(2):103-110.
2. Daiger SP, Bowne SJ, Sullivan LS. Perspective on genes and mutations causing retinitis pigmentosa. Arch Ophthalmol. 2007;125(2):151-158. (Pubitemid 46256517)
3. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet. 2006;368(9549):1795-1809.
4. Chang GQ, Hao Y, Wong F. Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron. 1993;11(4):595-605. (Pubitemid 23321770)
5. Portera-Cailliau C, Sung CH, Nathans J, Adler R. Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. Proc Natl Acad Sci U S A. 1994;91:974-978. (Pubitemid 24048491)
6. Xu GZ, Li WW, Tso MO. Apoptosis in human retinal degenerations. Trans Am Ophthalmol Soc. 1996;94:411-430.
7. Sanges D, Comitato A, Tammaro R, Marigo V. Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. Proc Natl Acad Sci U S A. 2006;103(46):17366-17371. (Pubitemid 44788975)
8. Huang PC, Gaitan AE, Hao Y, Petters RM, Wong F. Cellular interactions implicated in the mechanism of photoreceptor degeneration in transgenic mice expressing a mutant rhodopsin gene. Proc Natl Acad Sci U S A. 1993;90(18):8484-8488. (Pubitemid 23277693)
9. Adler R, Curcio C, Hicks D, Price D, Wong F. Cell death in ARMD. Mol Vis. 1999;5:31-42.
10. Sahel JA, Mohand-Said S, Leveillard T, Hicks D, Picaud S, Dreyfus H. Rod-cone interdependence: implications for therapy of photoreceptor cell diseases. Prog Brain Res. 2001;131:649-661. (Pubitemid 33733853)
11. Jones BW, Marc RE. Retinal remodeling during retinal degeneration. Exp Eye Res. 2005;81(2):123-137.
12. Delyfer MN, Forster V, Neveux N, Picaud S, Leveillard T, Sahel JA. Evidence for glutamate-mediated excitotoxic mechanisms during photoreceptor degeneration in the rd1 mouse retina. Mol Vis. 2005;11:688-696. (Pubitemid 41410205)
13. Yu DY, Cringle SJ. Retinal degeneration and local oxygen metabolism. Exp Eye Res. 2005;80(6):745-751.
14. Milam AH, Li ZY, Fariss RN. Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res. 1998;17(2):175-205. (Pubitemid 28339912)
15. Wang S, Villegas-Perez MP, Vidal-Sanz M, Lund RD. Progressive optic axon dystrophy and vascular changes in rd mice. Invest Ophthalmol Vis Sci. 2000;41(2):537-545. (Pubitemid 30080459)
16. Bringmann A, Pannicke T, Grosche J, et al. Muller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25(4):397-424. (Pubitemid 44038611)
17. Gehrs KM, Anderson DH, Johnson LV, Hageman GS. Age-related macular degeneration: emerging pathogenetic and therapeutic concepts. Ann Med. 2006;38(7):450-471. (Pubitemid 44767496)
18. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004;18(12):1450-1452. (Pubitemid 39561611)
19. Nakazawa T, Matsubara A, Noda K, et al. Characterization of cytokine responses to retinal detachment in rats. Mol Vis. 2006;12:867-878. (Pubitemid 44184719)
20. Tezel G, Yang X, Luo C, Peng Y, Sun SL, Sun D. Mechanisms of immune system activation in glaucoma: oxidative stress-stimulated antigen presentation by the retina and optic nerve head glia. Invest Ophthalmol Vis Sci. 2007;48(2):705-714. (Pubitemid 351260704)
21. Langmann T. Microglia activation in retinal degeneration. J Leukoc Biol. 2007;81(6):1345-1351.
22. Aramant RB, Seiler MJ. Progress in retinal sheet transplantation. Prog Retin Eye Res. 2004;23(5):475-494.
23. Limb GA, Daniels JT, Cambrey AD, et al. Current prospects for adult stem cell-based therapies in ocular repair and regeneration. Curr Eye Res. 2006;31(5):381-390.
24. MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature. 2006;444(7116):203-207. (Pubitemid 44722060)
25. Canola K, Angénieux B, Tekaya M, et al. Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Invest Ophthalmol Vis Sci. 2007;48(1):446-454. (Pubitemid 47251436)
26. McGill TJ, Lund RD, Douglas RM, et al. Syngeneic Schwann cell transplantation preserves vision in RCS rat without immunosuppression. Invest Ophthalmol Vis Sci. 2007;48(4):1906-1912.
27. Ma N, Streilein JW. Contribution of microglia as passenger leukocytes to the fate of intraocular neuronal retinal grafts. Invest Ophthalmol Vis Sci. 1998;39(12):2384-2393. (Pubitemid 28485650)
28. Larsson J, Juliusson B, Holmdahl R, Ehinger B. MHC expression in syngeneic and allogeneic retinal cell transplants in the rat. Graefes Arch Clin Exp Ophthalmol. 1999;237(1):82-85. (Pubitemid 29134871)
29. Anosova NG, Illigens B, Boisgérault F, Fedoseyeva EV, Young MJ, Benichou G. Antigenicity and immunogenicity of allogeneic retinal transplants. J Clin Invest. 2001;108(8):1175-1183. (Pubitemid 32995376)
30. Crocker PR, Gordon S. Properties and distribution of a lectin-like hemagglutinin differentially expressed by murine stromal tissue macrophages. J Exp Med. 1986;164:1862-1875. (Pubitemid 17217969)
31. Crocker PR, Kelm S, Dubois C, et al. Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages. EMBO J. 1991;10(7):1661-1669. (Pubitemid 21905632)
32. Crocker PR, Paulson JC, Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol. 2007;7(4):255-266. (Pubitemid 46480955)
33. Crocker PR, Freeman S, Gordon S, Kelm S. Sialoadhesin binds preferentially to cells of the granulocytic lineage. J Clin Invest. 1995;95(2):635-643.
34. Jiang HR, Lumsden L, Forrester JV. Macrophages and dendritic cells in IRBP-induced experimental autoimmune uveoretinitis in B10RIII mice. Invest Ophthalmol Vis Sci. 1999;40(13):3177-3185.
35. Jiang HR, Hwenda L, Makinen K, Oetke C, Crocker PR, Forrester JV. Sialoadhesin promotes the inflammatory response in experimental autoimmune uveoretinitis. J Immunol. 2006;177(4):2258-2264. (Pubitemid 44200985)
36. Hughes EH, Schlichtenbrede FC, Murphy CC, et al. Generation of activated sialoadhesin-positive microglia during retinal degeneration. Invest Ophthalmol Vis Sci. 2003;44(5):2229-2234. (Pubitemid 36520321)
37. Farber DB, Lolley RN. Enzymic basis for cyclic GMP accumulation in degenerative photoreceptor cells of mouse retina. J Cyclic Nucleotide Res. 1976;2(3):139-148.
38. Bowes C, Li T, Danciger M, Baxter LC, Applebury ML, Farber DB. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature. 1990;347:677-680. (Pubitemid 20356246)
39. Zhang Y, Kardaszewska AK, van Veen T, Rauch U, Perez MT. Integration between abutting retinas: role of glial structures and associated molecules at the interface. Invest Ophthalmol Vis Sci. 2004;45(12):4440-4449. (Pubitemid 39564670)
40. Zhang Y, Klassen HJ, Tucker BA, Perez MT, Young MJ. CNS progenitor cells promote a permissive environment for neurite outgrowth via a matrix metalloproteinase-2-dependent mechanism. J Neurosci. 2007;27(17):4499-4506. (Pubitemid 46663570)
41. Crocker PR, Gordon S. Mouse macrophage hemagglutinin (sheep erythrocyte receptor) with specificity for sialylated glycoconjugates characterized by a monoclonal antibody. J Exp Med. 1989;169(4):1333-1346. (Pubitemid 19104966)
42. Oetke C, Kraal G, Crocker PR. The antigen recognized by MOMA-I is sialoadhesin. Immunol Lett. 2006;106(1):96-98.
43. Thanos S. Sick photoreceptors attract activated microglia from the ganglion cell layer: a model to study the inflammatory cascades in rats with inherited retinal dystrophy. Brain Res. 1992;588(1):21-28.
44. Thanos S, Richter W. The migratory potential of vitally labelled microglial cells within the retina of rats with hereditary photoreceptor dystrophy. Int J Dev Neurosci. 1993;11(5):671-680. (Pubitemid 23352354)
45. Ng TF, Streilein JW. Light-induced migration of retinal microglia into the subretinal space. Invest Ophthalmol Vis Sci. 2001;42(13):3301-3310.
46. Hughes EH, Schlichtenbrede FC, Murphy CC, et al. Minocycline delays photoreceptor death in the rds mouse through a microglia independent mechanism. Exp Eye Res. 2004;78(6):1077-1084.
47. Zeiss CJ, Johnson EA. Proliferation of microglia, but not photoreceptors, in the outer nuclear layer of the rd-1 mouse. Invest Ophthalmol Vis Sci. 2004;45(3):971-976.
48. Zeng HY, Zhu XA, Zhang C, Yang LP, Wu LM, Tso MO. Identification of sequential events and factors associated with microglial activation, migration, and cytotoxicity in retinal degeneration in rd mice. Invest Ophthalmol Vis Sci. 2005;46(8):2992-2999. (Pubitemid 43086724)
49. Yang LP, Zhu XA, Tso MO. A possible mechanism of microglia-photoreceptor crosstalk. Mol Vis. 2007;13:2048-2057.
50. Yang LP, Li Y, Zhu XA, Tso MO. Minocycline delayed photoreceptor death in rds mice through iNOS-dependent mechanism. Mol Vis. 2007;13:1073-1082. (Pubitemid 47064331)
51. Perry VH, Crocker PR, Gordon S. The blood-brain barrier regulates the expression of a macrophage sialic acid-binding receptor on microglia. J Cell Sci. 1992;101:201-207.
52. Xu H, Chen M, Mayer EJ, Forrester JV, Dick AD. Turnover of resident retinal microglia in the normal adult mouse. Glia. 2007;55(11):1189-1198. (Pubitemid 47204210)
53. Blanks JC, Johnson LV. Vascular atrophy in the retinal degenerative rd mouse. J Comp Neurol. 1986;254(4):543-553.
54. Fitzgerald ME, Slapnick SM, Caldwell RB. Alterations in lectin binding accompany increased permeability in the dystrophic rat model for proliferative retinopathy. Prog Clin Biol Res. 1989;314:409-425.
55. Vinores SA, Küchle M, Derevjanik NL, et al. Blood-retinal barrier breakdown in retinitis pigmentosa: light and electron microscopic immunolocalization. Histol Histopathol. 1995;10(4):913-923.
56. Zhang Y, Rauch U, Perez MT. Accumulation of neurocan, a brain chondroitin sulfate proteoglycan, in association with the retinal vasculature in RCS rats. Invest Ophthalmol Vis Sci. 2003;44(3):1252-1261. (Pubitemid 36297847)
57. Hackam AS, Strom R, Liu D, et al. Identification of gene expression changes associated with the progression of retinal degeneration in the rd1 mouse. Invest Ophthalmol Vis Sci. 2004;45(9):2929-2942. (Pubitemid 39121819)
58. Rohrer B, Pinto FR, Hulse KE, Lohr HR, Zhang L, Almeida JS. Multidestructive pathways triggered in photoreceptor cell death of the rd mouse as determined through gene expression profiling. J Biol Chem. 2004;279(40):41903-41910. (Pubitemid 39313639)
59. Nicchia GP, Nico B, Camassa LM, et al. The role of aquaporin-4 in the blood-brain barrier development and integrity: studies in animal and cell culture models. Neuroscience. 2004;129(4):935-945. (Pubitemid 39556245)
60. McMenamin PG. Dendritic cells and macrophages in the uveal tract of the normal mouse eye. Br J Ophthalmol. 1999;83(5):598-604.
61. Chinnery HR, Ruitenberg MJ, Plant GW, Pearlman E, Jung S, McMenamin PG. The chemokine receptor CX3CR1 mediates homing of MHC class II-positive cells to the normal mouse corneal epithelium. Invest Ophthalmol Vis Sci. 2007;48(4):1568-1574. (Pubitemid 351261340)
62. Lazarus HS, Hageman GS. In situ characterization of the human hyalocyte. Arch Ophthalmol. 1994;112(10):1356-1362.
63. Qiao H, Hisatomi T, Sonoda KH, et al. The characterisation of hyalocytes: the origin, phenotype, and turnover. Br J Ophthalmol. 2005;89(4):513-517. (Pubitemid 40469977)
64. Zhang Y, Arnér K, Ehinger B, Perez MT. Limitation of anatomical integration between subretinal transplants and the host retina. Invest Ophthalmol Vis Sci. 2003;44(1):324-331. (Pubitemid 36134292)
65. Jiang LQ, Jorquera M, Streilein JW. Subretinal space and vitreous cavity as immunologically privileged sites for retinal allografts. Invest Ophthalmol Vis Sci. 1993;34(12):3347-3354. (Pubitemid 23346667)
66. Lund RD, Ono SJ, Keegan DJ, Lawrence JM. Retinal transplantation: progress and problems in clinical application. J Leukoc Biol. 2003;74(2):151-160. (Pubitemid 38040410)
67. Al-Amro S, Tang L, Kaplan HJ. Limitations in the study of immune privilege in the subretinal space of the rodent. Invest Ophthalmol Vis Sci. 1999;40(12):3067-3069.
68. Lewis GP, Sethi CS, Carter KM, Charteris DG, Fisher SK. Microglial cell activation following retinal detachment: a comparison between species. Mol Vis. 2005;11:491-500.
69. Sharma RK, Bergström A, Zucker CL, Adolph AR, Ehinger B. Survival of long-term retinal cell transplants. Acta Ophthalmol Scand. 2000;78(4):396-402. (Pubitemid 30608642)
70. Gouras P, Tanabe T. Survival and integration of neural retinal transplants in rd mice. Graefes Arch Clin Exp Ophthalmol. 2003;241(5):403-409. (Pubitemid 36748576)
71. Streilein JW, Ma N, Wenkel H, Ng TF, Zamiri P. Immunobiology and privilege of neuronal retina and pigment epithelium transplants. Vision Res. 2002;42(4):487-495. (Pubitemid 34169706)
72. Xu H, Dawson R, Forrester JV, Liversidge J. Identification of novel dendritic cell populations in normal mouse retina. Invest Ophthalmol Vis Sci. 2007;48(4):1701-1710. (Pubitemid 351261356)
73. Santos AM, Calvente R, Tassi M, et al. Embryonic and postnatal development of microglial cells in the mouse retina. J Comp Neurol. 2008;506(2):224-239.
74. Oishi A, Nagai T, Mandai M, Takahashi M, Yoshimura N. The effect of dendritic cells on the retinal cell transplantation. Biochem Biophys Res Commun. 2007;363(2):292-296. (Pubitemid 47484330)
75. Rohrer B, Demos C, Frigg R, Grimm C. Classical complement activation and acquired immune response pathways are not essential for retinal degeneration in the rd1 mouse. Exp Eye Res. 2007;84(1):82-91. (Pubitemid 44803019)