Functional endothelial progenitor cells selectively recruit neurovascular protective monocyte-derived F4/80+/Ly6c+ macrophages in a mouse model of retinal degeneration

Stem Cells

Volumn 31, Issue 10, 2013, Pages 2149-2161

  Fukuda, Shinichi ^a   Nagano, Masumi ^a,b   Yamashita, Toshiharu ^a   Kimura, Kenichi ^a   Tsuboi, Ikki ^a   Salazar, Georgina ^a   Ueno, Shinji ^c   Kondo, Mineo ^d   Kunath, Tilo ^a   Oshika, Tetsuro ^a   Ohneda, Osamu ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Endothelial progenitor cell transplantation; Monocyte derived macrophages; Neurovascular protection; Residual microglia

Indexed keywords

ALDEHYDE DEHYDROGENASE; CHEMOKINE RECEPTOR CCR2; CYCLOSPORIN A; INTERLEUKIN 10; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVITY; MACROPHAGE; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; RETINITIS PIGMENTOSA; STEM CELL GENE THERAPY;

ENDOTHELIAL PROGENITOR CELL TRANSPLANTATION; MONOCYTE DERIVED MACROPHAGES; NEUROVASCULAR PROTECTION; RESIDUAL MICROGLIA;

ANIMALS; ANTIGENS, DIFFERENTIATION; ANTIGENS, LY; BONE MARROW CELLS; CELLS, CULTURED; CHEMOKINES; CHEMOTAXIS; ENDOTHELIAL CELLS; GENE EXPRESSION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; INSULIN-LIKE GROWTH FACTOR I; MACROPHAGES; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICROGLIA; NERVE DEGENERATION; RETINA; RETINAL NEURONS; RETINAL VESSELS; RETINITIS PIGMENTOSA; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84887922477     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1469     Document Type: Article

References (50)

1. Hartong DT, Berson EL, Dryja TP Retinitis pigmentosa. Lancet 2006; 368:1795-1809.
2. Humphries P, Kenna P, Farrar GJ On the molecular genetics of retinitis pigmentosa. Science 1992;256:804-808.
3. Bramall AN, Wright AF, Jacobson SG et al. The genomic, biochemical, and cellular responses of the retina in inherited photoreceptor degenerations and prospects for the treatment of these disorders. Annu Rev Neurosci 2010;33:441-472.
4. Cideciyan AV. Leber congenital amaurosis due to RPE65 mutations and its treatment with gene therapy. Prog Retin Eye Res 2010;29:398-427.
5. Frasson M, Picaud S, Leveillard T et al. Glial cell line-derived neuro-trophic factor induces histologic and functional protection of rod pho-toreceptors in the rd/rd mouse. Invest Ophthalmol Vis Sci 1999;40: 2724-2734.
6. LaVail MM, Yasumura D, Matthes MT et al. Protection of mouse photoreceptors by survival factors in retinal degenerations. Invest Oph-thalmol Vis Sci 1998;39:592-602.
7. Inoue Y, Iriyama A, Ueno S et al. Subretinal transplantation of bone marrow mesenchymal stem cells delays retinal degeneration in the RCS rat model of retinal degeneration. Exp Eye Res 2007;85:234-241.
8. MacLaren RE, Pearson RA, MacNeil A et al. Retinal repair by transplantation of photoreceptor precursors. Nature 2006;444:203-207.
9. Otani A, Dorrell MI, Kinder K et al. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J Clin Invest 2004;114:765-774.
10. Meyer JS, Katz ML, Maruniak JA et al. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells 2006;24:274-283.
11. Yang P, Seiler MJ, Aramant RB et al. Differential lineage restriction of rat retinal progenitor cells in vitro and in vivo. J Neurosci Res 2002;69:466-476.
12. Asahara T, Murohara T, Sullivan A et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967.
13. Gehling UM, Ergun S, Schumacher U et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 2000;95: 3106-3112.
14. Peichev M, Naiyer AJ, Pereira D et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000;95:952-958.
15. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003;9:702-712.
16. Murohara T, Ikeda H, Duan J et al. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 2000;105:1527-1536.
17. Shi Q, Rafii S, Wu MH et al. Evidence for circulating bone marrow-derived endothelial cells. Blood 1998;92:362-367.
18. Hristov M, Erl W, Weber PC Endothelial progenitor cells: Mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 2003; 23:1185-1189.
19. Nagano M, Yamashita T, Hamada H et al. Identification of functional endothelial progenitor cells suitable for the treatment of ischemic tissue using human umbilical cord blood. Blood 2007;110:151-160.
20. Nakamura K, Tsurushima H, Marushima A et al. A subpopulation of endothelial progenitor cells with low aldehyde dehydrogenase activity attenuates acute ischemic brain injury in rats. Biochem Biophys Res Commun 2012;418:87-92.
21. Fan Y, Shen F, Frenzel T et al. Endothelial progenitor cell transplantation improves long-term stroke outcome in mice. Ann Neurol 2010;67: 488-497.
22. Ohta T, Kikuta K, Imamura H et al. Administration of ex vivo-expanded bone marrow-derived endothelial progenitor cells attenuates focal cerebral ischemia-reperfusion injury in rats. Neurosurgery 2006;59:679-686.
23. Jeong JO, Kim MO, Kim H et al. Dual angiogenic and neurotrophic effects of bone marrow-derived endothelial progenitor cells on diabetic neuropathy. Circulation 2009;119:699-708.
24. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
25. Ueno S, Kondo M, Miyata K et al. Physiological function of S-cone system is not enhanced in rd7 mice. Exp Eye Res 2005;81:751-758.
26. van Rooijen N., Sanders A, van den Berg TK. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodro-nate and propamidine. J Immunol Methods 1996;193:93-99.
27. Sasahara M, Otani A, Oishi A et al. Activation of bone marrow-derived microglia promotes photoreceptor survival in inherited retinal degeneration. Am J Pathol 2008;172:1693-1703.
28. Xu G, Nagano M, Kanezaki R et al. Frequent mutations in the GATA-1 gene in the transient myeloproliferative disorder of Down syndrome. Blood 2003;102:2960-2968.
29. Bowes C, Li T, Danciger M et al. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phospho-diesterase. Nature 1990;347:677-680.
30. Pittler SJ, Baehr W. Identification of a nonsense mutation in the rod photoreceptor cGMP phosphodiesterase beta-subunit gene of the rd mouse. Proc Natl Acad Sci USA 1991;88:8322-8326.
31. Kaneko H, Nishiguchi KM, Nakamura M et al. Retardation of photore-ceptor degeneration in the detached retina of rd1 mouse. Invest Oph-thalmol Vis Sci 2008;49:781-787.
32. Chang B, Hawes NL, Hurd RE et al. Retinal degeneration mutants in the mouse. Vision Res 2002;42:517-525.
33. Zhang Y, Ingram DA, Murphy MP et al. Release of proinflammatory mediators and expression of proinflammatory adhesion molecules by endothelial progenitor cells. Am J Physiol Heart Circ Physiol 2009; 296:H1675-1682.
34. Zeng HY, Zhu XA, Zhang C et al. Identification of sequential events and factors associated with microglial activation, migration, and cyto-toxicity in retinal degeneration in rd mice. Invest Ophthalmol Vis Sci 2005;46:2992-2999.
35. Harrison JK, Jiang Y, Chen S et al. Role for neuronally derived frac-talkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 1998;95:10896-10901.
36. London A, Itskovich E, Benhar I et al. Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages. J Exp Med 2011;208:23-39.
37. Leenen PJ, Melis M, Slieker WA et al. Murine macrophage precursor characterization. II. Monoclonal antibodies against macrophage precursor antigens. Eur J Immunol 1990;20:27-34.
38. Geissmann F, Jung S, Littman DR Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003;19: 71-82.
39. Ingram DA, Mead LE, Tanaka H et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004;104:2752-2760.
40. van der Strate BW, Popa ER, Schipper M et al. Circulating human CD34+ progenitor cells modulate neovascularization and inflammation in a nude mouse model. J Mol Cell Cardiol 2007;42:1086-1097.
41. Suh W, Kim KL, Kim JM et al. Transplantation of endothelial progenitor cells accelerates dermal wound healing with increased recruitment of monocytes/macrophages and neovascularization. Stem Cells 2005; 23:1571-1578.
42. Yoder MC, Mead LE, Prater D et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007;109:1801-1809.
43. Chen L, Wu W, Dentchev T et al. Light damage induced changes in mouse retinal gene expression. Exp Eye Res 2004;79: 239-247.
44. Jo N, Wu GS, Rao NA Upregulation of chemokine expression in the retinal vasculature in ischemia-reperfusion injury. Invest Ophthalmol Vis Sci 2003;44:4054-4060.
45. Nakazawa T, Hisatomi T, Nakazawa C et al. Monocyte chemoattrac-tant protein 1 mediates retinal detachment-induced photoreceptor apo-ptosis. Proc Natl Acad Sci USA 2007;104:2425-2430.
46. Abu El-Asrar AM, Van Damme J, Put W et al. Monocyte chemotactic protein-1 in proliferative vitreoretinal disorders. Am J Ophthalmol 1997;123:599-606.
47. Lu H, Huang D, Saederup N et al. Macrophages recruited via CCR2 produce insulin-like growth factor-1 to repair acute skeletal muscle injury. FASEB J 2011;25:358-369.
48. Lu H, Huang D, Ransohoff RM et al. Acute skeletal muscle injury: CCL2 expression by both monocytes and injured muscle is required for repair. FASEB J 2011;25:3344-3355.
49. Shechter R, London A, Varol C et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009;6:e1000113.
50. García J.E., López AM, de Cabo MR et al. Cyclosporin A decreases human macrophage interleukin-6 synthesis at post-transcriptional level. Mediators Inflamm 1999;8:253-259.