Embryonic Stem Cell-Derived Microvesicles Induce Gene Expression Changes in Müller Cells of the Retina

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Katsman, Diana ^a,b   Stackpole, Emma J ^a   Domin, Daniel R ^a   Farber, Debora B ^a,b  

^a JULES STEIN EYE INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VACUOLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; GANGLION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MICROARRAY ANALYSIS; MORPHOLOGY; MOUSE; MUELLER CELL; NONHUMAN; PHOTORECEPTOR; RETINA AMACRINE CELL; RETINA CELL; RETINA ROD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELL SHAPE; CYTOPLASMIC VESICLES; EMBRYONIC STEM CELLS; EYE PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICRORNAS; OCTAMER TRANSCRIPTION FACTOR-3; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTORECEPTOR CELLS, VERTEBRATE; PLURIPOTENT STEM CELLS; RETINA; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS;

EID: 84870603236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050417     Document Type: Article

References (77)

1. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L, (2010) Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 78: 838-848.
2. Deregibus MC, Tetta C, Camussi G, (2010) The dynamic stem cell microenvironment is orchestrated by microvesicle-mediated transfer of genetic information. Histol Histopathol 25: 397-404.
3. Wolf P, (1967) The nature and significance of platelet products in human plasma. Br J Haematol 13: 269-288.
4. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ, (1999) Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94: 3791-3799.
5. Cocucci E, Racchetti G, Meldolesi J, (2009) Shedding microvesicles: artefacts no more. Trends in Cell Biology 19: 43-51.
6. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, et al. (2009) Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4: e4722.
7. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, et al. (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20: 847-856.
8. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, et al. (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110: 2440-2448.
9. Herrera MB, Fonsato V, Gatti S, Deregibus MC, Sordi A, et al. (2010) Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. J Cell Mol Med 14: 1605-1618.
10. Quesenberry PJ, Dooner MS, Aliotta JM, (2010) Stem cell plasticity revisited: the continuum marrow model and phenotypic changes mediated by microvesicles. Exp Hematol 38: 581-592.
11. Tetta C, Bruno S, Fonsato V, Deregibus MC, Camussi G, (2011) The role of microvesicles in tissue repair. Organogenesis 7: 105-115.
12. Bruno S, Grange C, Collino F, Deregibus MC, Cantaluppi V, et al. (2012) Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PLoS One 7: e33115.
13. Wang YM, Blelloch R, (2009) Cell Cycle Regulation by MicroRNAs in Embryonic Stem Cells. Cancer Research 69: 4093-4096.
14. Turner DL, Cepko CL, (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328: 131-136.
15. Jadhav AP, Roesch K, Cepko CL, (2009) Development and neurogenic potential of Müller glial cells in the vertebrate retina. Prog Retin Eye Res 28: 249-262.
16. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, et al. (2004) Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 101: 13654-13659.
17. Bernardos RL, Barthel LK, Meyers JR, Raymond PA, (2007) Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 27: 7028-7040.
18. Das AV, Mallya KB, Zhao X, Ahmad F, Bhattacharya S, et al. (2006) Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 299: 283-302.
19. Hollborn M, Ulbricht E, Rillich K, Dukic-Stefanovic S, Wurm A, et al. (2011) The human Müller cell line MIO-M1 expresses opsins. Mol Vis 17: 2738-2750.
20. Dyer MA, Cepko CL, (2000) Control of Müller glial cell proliferation and activation following retinal injury. Nat Neurosci 3: 873-880.
21. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, et al. (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25: 397-424.
22. Fischer AJ, Reh TA, (2003) Potential of Müller glia to become neurogenic retinal progenitor cells. Glia 43: 70-76.
23. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, et al. (2008) Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A 105: 19508-19513.
24. Bhatia B, Singhal S, Jayaram H, Khaw PT, Limb GA, (2010) Adult retinal stem cells revisited. Open Ophthalmol J 4: 30-38.
25. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, et al. (2001) Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105: 43-55.
26. Mathers PH, Jamrich M, (2000) Regulation of eye formation by the Rx and Pax6 homeobox genes. Cellular and Molecular Life Sciences 57: 186-194.
27. Mallanna SK, Rizzino A, (2010) Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev Biol 344: 16-25.
28. Zovoilis A, Pantazi A, Smorag L, Opitz L, Riester GS, et al. (2010) Embryonic stem cell-related miRNAs are involved in differentiation of pluripotent cells originating from the germ line. Mol Hum Reprod 16: 793-803.
29. Guo L, Zhao RCH, Wu YJ, (2011) The role of microRNAs in self-renewal and differentiation of mesenchymal stem cells. Exp Hematol 39: 608-616.
30. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
31. Roesch K, Jadhav AP, Trimarchi JM, Stadler MB, Roska B, et al. (2008) The transcriptome of retinal Müller glial cells. J Comp Neurol 509: 225-238.
32. Lamba D, Karl M, Reh T, (2008) Neural regeneration and cell replacement: a view from the eye. Cell Stem Cell 2: 538-549.
33. Duester G, (2009) Keeping an eye on retinoic acid signaling during eye development. Chem Biol Interact 178: 178-181.
34. Sappington RM, Chan M, Calkins DJ, (2006) Interleukin-6 protects retinal ganglion cells from pressure-induced death. Invest Ophthalmol Vis Sci 47: 2932-2942.
35. Bermingham-McDonogh O, McCabe KL, Reh TA, (1996) Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina. Development 122: 1427-1438.
36. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
37. Kinouchi R, Takeda M, Yang L, Wilhelmsson U, Lundkvist A, et al. (2003) Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nat Neurosci 6: 863-868.
38. Tucker B, Klassen H, Yang L, Chen DF, Young MJ, (2008) Elevated MMP Expression in the MRL Mouse Retina Creates a Permissive Environment for Retinal Regeneration. Invest Ophthalmol Vis Sci 49: 1686-1695.
39. Chong DY, Boehlke CS, Zheng QD, Zhang L, Han Y, et al. (2008) Interleukin-6 as a photoreceptor neuroprotectant in an experimental model of retinal detachment. Invest Ophthalmol Vis Sci 49: 3193-3200.
40. Domowicz MS, Sanders TA, Ragsdale CW, Schwartz NB, (2008) Aggrecan is expressed by embryonic brain glia and regulates astrocyte development. Developmental biology315: 114-124.
41. Decembrini S, Bressan D, Vignali R, Pitto L, Mariotti S, et al. (2009) MicroRNAs couple cell fate and developmental timing in retina. Proc Natl Acad Sci U S A 106: 21179-21184.
42. Judson RL, Babiarz JE, Venere M, Blelloch R, (2009) Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 27: 459-461.
43. Peter ME, (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8: 843-852.
44. Li X, Carthew RW, (2005) A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123: 1267-1277.
45. Arora A, Guduric-Fuchs J, Harwood L, Dellett M, Cogliati T, et al. (2010) Prediction of microRNAs affecting mRNA expression during retinal development. BMC Dev Biol 10: 1-15.
46. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, et al. (2009) miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460: 705-U780.
47. Letzen BS, Liu C, Thakor NV, Gearhart JD, All AH, et al. (2010) MicroRNA expression profiling of oligodendrocyte differentiation from human embryonic stem cells. PLoS One 5: e10480.
48. Fischer AJ, Reh TA, (2001) Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 4: 247-252.
49. Wu DM, Schneiderman T, Burgett J, Gokhale P, Barthel L, et al. (2001) Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Invest Ophthalmol Vis Sci 42: 2115-2124.
50. Nickerson PE, Da Silva N, Myers T, Stevens K, Clarke DB, (2008) Neural progenitor potential in cultured Müller glia: effects of passaging and exogenous growth factor exposure. Brain Res 1230: 1-12.
51. Giannelli SG, Demontis GC, Pertile G, Rama P, Broccoli V, (2011) Adult human Müller glia cells are a highly efficient source of rod photoreceptors. Stem Cells 29: 344-356.
52. Gnecchi M, Zhang Z, Ni A, Dzau VJ, (2008) Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 103: 1204-1219.
53. Gotz M, Barde YA, (2005) Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 46: 369-372.
54. Muranishi Y, Terada K, Furukawa T, (2012) An essential role for Rax in retina and neuroendocrine system development. Dev Growth Differ 54: 341-348.
55. Wang NK, Tosi J, Kasanuki JM, Chou CL, Kong J, et al. (2010) Transplantation of Reprogrammed Embryonic Stem Cells Improves Visual Function in a Mouse Model for Retinitis Pigmentosa. Transplantation 89: 911-919.
56. Klimanskaya I, Hipp J, Rezai KA, West M, Atala A, et al. (2004) Derivation and comparative assessment of retinal pigment epithelium from human embryonic stem cells using transcriptomics. Cloning Stem Cells 6: 217-245.
57. Yu JY, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
58. Levine EM, Passini M, Hitchcock PF, Glasgow E, Schechter N, (1997) Vsx-1 and Vsx-2: two Chx10-like homeobox genes expressed in overlapping domains in the adult goldfish retina. J Comp Neurol 387: 439-448.
59. Fausett BV, Gumerson JD, Goldman D, (2008) The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. Journal of Neuroscience 28: 1109-1117.
60. Dorsky RI, Chang WS, Rapaport DH, Harris WA, (1997) Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature 385: 67-70.
61. Kelly LE, Nekkalapudi S, El-Hodiri HM, (2007) Expression of the forkhead transcription factor FoxN4 in progenitor cells in the developing Xenopus laevis retina and brain. Gene Expression Patterns 7: 233-238.
62. Cid E, Santos-Ledo A, Parrilla-Monge M, Lillo C, Arevalo R, et al. (2010) Prox1 expression in rod precursors and Müller cells. Exp Eye Res 90: 267-276.
63. Li SG, Mo ZQ, Yang XJ, Price SM, Shen MM, et al. (2004) Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron 43: 795-807.
64. Hufnagel RB, Le TT, Riesenberg AL, Brown NL, (2010) Neurog2 controls the leading edge of neurogenesis in the mammalian retina. Dev Biol 340: 490-503.
65. Sehgal R, Sheibani N, Rhodes SJ, Belecky Adams TL, (2009) BMP7 and SHH regulate Pax2 in mouse retinal astrocytes by relieving TLX repression. Dev Biol 332: 429-443.
66. Nelson BR, Reh TA, (2008) Relationship between delta-like and proneural bHLH genes during chick retinal development. Developmental Dynamics 237: 1565-1580.
67. Yurco P, Cameron DA, (2004) Evidence for multiple roles of Müller glia in the regeneration of adult zebrafish retina. Invest Ophthalmol Vis Sci 45: U636-U636.
68. Dalkara D, Kolstad KD, Guerin KI, Hoffmann NV, Visel M, et al. (2011) AAV mediated GDNF secretion from retinal glia slows down retinal degeneration in a rat model of retinitis pigmentosa. Mol Ther 19: 1602-1608.
69. Ward MS, Khoobehi A, Lavik EB, Langer R, Young MJ, (2007) Neuroprotection of retinal ganglion cells in DBA/2J mice with GDNF-loaded biodegradable microspheres. J Pharm Sci 96: 558-568.
70. Lau D, McGee LH, Zhou SZ, Rendahl KG, Manning WC, et al. (2000) Retinal degeneration is slowed in transgenic rats by AAV-mediated delivery of FGF-2. Invest Ophthalmol Vis Sci 41: 3622-3633.
71. Vergara MN, Del Rio-Tsonis K, (2009) Retinal regeneration in the Xenopus laevis tadpole: a new model system. Mol Vis 15: 1000-1013.
72. Kuffler DP, Sosa IJ, Reyes O, (2009) Schwann cell chondroitin sulfate proteoglycan inhibits dorsal root ganglion neuron neurite outgrowth and substrate specificity via a soma and not a growth cone mechanism. Journal of Neuroscience Research 87: 2863-2871.
73. Gong J, Sagiv O, Cai H, Tsang SH, Del Priore LV, (2008) Effects of extracellular matrix and neighboring cells on induction of human embryonic stem cells into retinal or retinal pigment epithelial progenitors. Exp Eye Res 86: 957-965.
74. Zhao Y, Srivastava D, (2007) A developmental view of microRNA function. Trends in Biochemical Sciences 32: 189-197.
75. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, et al. (2008) Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 40: 1478-1483.
76. Melton C, Judson RL, Blelloch R, (2010) Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463: 621-626.
77. Limb GA, Salt TE, Munro PM, Moss SE, Khaw PT, (2002) In vitro characterization of a spontaneously immortalized human Müller cell line (MIO-M1). Invest Ophthalmol Vis Sci 43: 864-869.