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Advances in Pluripotent and Adult Stem Cells for Eye Research

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Regenerative Biology of the Eye

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

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Abstract

Blindness is one of the most feared disabilities and many common causes of blindness are currently untreatable. Currently, the World Health Organization estimates that around 285 million people are visually impaired. Regenerative medicine using stem cells offers a new avenue for medical treatment by replacing cells and tissues lost during ocular disease progression. Here we provide an overview of research of pluripotent stem cells as well as adult stem cells in the eye and highlight their potentials for eye research.

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Abbreviations

ALS:

Amyotrophic lateral sclerosis

CEnC:

Corneal endothelial cell

CEpSC:

Corneal epithelial stem cell

CSSC:

Corneal stromal stem cell

ESC:

Embryonic stem cell

FD:

Familial dysautonomia

iPSC:

Induced pluripotent stem cell

LESC:

Limbal epithelial stem cell

miRNA:

Micro RNA

MSC:

Mesenchymal stem cell

NuRD:

Nucleosome remodelling and deacetylase

SP:

Side population

SSEA4:

Stage-specific embryonic antigen-4

TDP-43:

Tar DNA binding protein-43

TM-MSC:

Trabecular meshwork mesenchymal stem cell

References

  1. Smith A (1998) Cell therapy: in search of pluripotency. Curr Biol 8(22):R802–R804

    CAS  PubMed  Google Scholar 

  2. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18(4):399–404

    CAS  PubMed  Google Scholar 

  3. Thomson JA et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147

    CAS  PubMed  Google Scholar 

  4. Ogawa M, Porter PN, Nakahata T (1983) Renewal and commitment to differentiation of hemopoietic stem cells (an interpretive review). Blood 61(5):823–829

    CAS  PubMed  Google Scholar 

  5. Temple S (2001) The development of neural stem cells. Nature 414(6859):112–117

    CAS  PubMed  Google Scholar 

  6. Caplan AI (2005) Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng 11(7–8):1198–1211

    CAS  PubMed  Google Scholar 

  7. Zuk PA et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13(12):4279–4295

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Erices A, Conget P, Minguell JJ (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 109(1):235–242

    CAS  PubMed  Google Scholar 

  9. Arriero M, Brodsky SV, Gealekman O, Lucas PA, Goligorsky MS (2004) Adult skeletal muscle stem cells differentiate into endothelial lineage and ameliorate renal dysfunction after acute ischemia. Am J Physiol Renal Physiol 287(4):F621–F627

    CAS  PubMed  Google Scholar 

  10. Lavker RM, Sun TT (1983) Epidermal stem cells. J Invest Dermatol 81(1 suppl):121s–127s

    CAS  PubMed  Google Scholar 

  11. Inoue M et al (1988) Macroscopic intestinal colonies of mice as a tool for studying differentiation of multipotential intestinal stem cells. Am J Pathol 132(1):49–58

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Tseng SC (1989) Concept and application of limbal stem cells. Eye (Lond) 3(pt 2):141–157

    Google Scholar 

  13. Bianco P, Gehron Robey P (2000) Marrow stromal stem cells. J Clin Invest 105(12):1663–1668

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Friedenstein AJ et al (1974) Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 2(2):83–92

    CAS  PubMed  Google Scholar 

  15. Shamblott MJ et al (1998) Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci U S A 95(23):13726–13731

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Andrews PW (2002) From teratocarcinomas to embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 357(1420):405–417

    PubMed Central  PubMed  Google Scholar 

  17. Chung Y et al (2008) Human embryonic stem cell lines generated without embryo destruction. Cell Stem Cell 2(2):113–117

    CAS  PubMed  Google Scholar 

  18. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676

    CAS  PubMed  Google Scholar 

  19. Takahashi K et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872

    CAS  PubMed  Google Scholar 

  20. Yu J et al (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920

    CAS  PubMed  Google Scholar 

  21. Muller FJ et al (2008) Regulatory networks define phenotypic classes of human stem cell lines. Nature 455(7211):401–405

    PubMed Central  PubMed  Google Scholar 

  22. Maherali N et al (2007) Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1(1):55–70

    CAS  PubMed  Google Scholar 

  23. Zhao XY et al (2009) iPS cells produce viable mice through tetraploid complementation. Nature 461(7260):86–88

    CAS  PubMed  Google Scholar 

  24. Nakagawa M et al (2008) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26(1):101–106

    CAS  PubMed  Google Scholar 

  25. Feng B et al (2009) Reprogramming of fibroblasts into induced pluripotent stem cells with orphan nuclear receptor Esrrb. Nat Cell Biol 11(2):197–203

    CAS  PubMed  Google Scholar 

  26. Blelloch R, Venere M, Yen J, Ramalho-Santos M (2007) Generation of induced pluripotent stem cells in the absence of drug selection. Cell Stem Cell 1(3):245–247

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Tsubooka N et al (2009) Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells 14(6):683–694

    CAS  PubMed  Google Scholar 

  28. Park IH et al (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451(7175):141–146

    CAS  PubMed  Google Scholar 

  29. Mali P et al (2008) Improved efficiency and pace of generating induced pluripotent stem cells from human adult and fetal fibroblasts. Stem Cells 26(8):1998–2005

    CAS  PubMed  Google Scholar 

  30. Heng JC et al (2010) The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 6(2):167–174

    CAS  PubMed  Google Scholar 

  31. Wang W et al (2011) Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1. Proc Natl Acad Sci U S A 108(45):18283–18288

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Maekawa M et al (2011) Direct reprogramming of somatic cells is promoted by maternal transcription factor Glis1. Nature 474(7350):225–229

    CAS  PubMed  Google Scholar 

  33. Hirata T et al (2012) Zscan4 transiently reactivates early embryonic genes during the generation of induced pluripotent stem cells. Sci Rep 2:208

    PubMed Central  PubMed  Google Scholar 

  34. Judson RL, Babiarz JE, Venere M, Blelloch R (2009) Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 27(5):459–461

    CAS  PubMed Central  PubMed  Google Scholar 

  35. Lin SL et al (2008) Mir-302 reprograms human skin cancer cells into a pluripotent ES-cell-like state. RNA 14(10):2115–2124

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Anokye-Danso F et al (2011) Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8(4):376–388

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Miyoshi N et al (2011) Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8(6):633–638

    CAS  PubMed  Google Scholar 

  38. Marion RM et al (2009) A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460(7259):1149–1153

    CAS  PubMed Central  PubMed  Google Scholar 

  39. Utikal J et al (2009) Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460(7259):1145–1148

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Banito A et al (2009) Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 23(18):2134–2139

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Hanna J et al (2007) Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318(5858):1920–1923

    CAS  PubMed  Google Scholar 

  42. Hong H et al (2009) Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460(7259):1132–1135

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Kawamura T et al (2009) Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460(7259):1140–1144

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Zhao Y et al (2008) Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell 3(5):475–479

    CAS  PubMed  Google Scholar 

  45. Okita K et al (2011) A more efficient method to generate integration-free human iPS cells. Nat Methods 8(5):409–412

    CAS  PubMed  Google Scholar 

  46. Papp B, Plath K (2013) Epigenetics of reprogramming to induced pluripotency. Cell 152(6):1324–1343

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Yildirim O et al (2011) Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 147(7):1498–1510

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Kaji K et al (2006) The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 8(3):285–292

    CAS  PubMed  Google Scholar 

  49. Zhu D, Fang J, Li Y, Zhang J (2009) Mbd3, a component of NuRD/Mi-2 complex, helps maintain pluripotency of mouse embryonic stem cells by repressing trophectoderm differentiation. PLoS One 4(11):e7684

    PubMed Central  PubMed  Google Scholar 

  50. Rais Y et al (2013) Deterministic direct reprogramming of somatic cells to pluripotency. Nature 502(7469):65–70

    CAS  PubMed  Google Scholar 

  51. Luo M et al (2013) NuRD blocks reprogramming of mouse somatic cells into pluripotent stem cells. Stem Cells 31(7):1278–1286

    CAS  PubMed  Google Scholar 

  52. Brambrink T et al (2008) Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2(2):151–159

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Maherali N et al (2008) A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell 3(3):340–345

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Stadtfeld M, Maherali N, Breault DT, Hochedlinger K (2008) Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2(3):230–240

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Sommer CA et al (2009) Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27(3):543–549

    CAS  PubMed  Google Scholar 

  56. Carey BW et al (2009) Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc Natl Acad Sci U S A 106(1):157–162

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Shao LJ et al (2009) Generation of iPS cells using defined factors linked via the self-cleaving 2A sequences in a single open reading frame. Cell Res 19(3):296–306

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Chang CW et al (2009) Polycistronic lentiviral vector for “hit and run” reprogramming of adult skin fibroblasts to induced pluripotent stem cells. Stem Cells 27(5):1042–1049

    CAS  PubMed  Google Scholar 

  59. Soldner F et al (2009) Parkinson’s disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136(5):964–977

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Woltjen K et al (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458(7239):766–770

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Kaji K et al (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458(7239):771–775

    CAS  PubMed Central  PubMed  Google Scholar 

  62. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322(5903):945–949

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Okita K, Nakagawa M, Hong HJ, Ichisaka T, Yamanaka S (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322(5903):949–953

    CAS  PubMed  Google Scholar 

  64. Ban H et al (2011) Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc Natl Acad Sci U S A 108(34):14234–14239

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M (2009) Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad B Phys Biol Sci 85(8):348–362

    CAS  Google Scholar 

  66. Yu J et al (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324(5928):797–801

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Okita K et al (2013) An efficient nonviral method to generate integration-free human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells 31(3):458–466

    CAS  PubMed  Google Scholar 

  68. Dowey SN, Huang X, Chou BK, Ye Z, Cheng L (2012) Generation of integration-free human induced pluripotent stem cells from postnatal blood mononuclear cells by plasmid vector expression. Nat Protoc 7(11):2013–2021

    CAS  PubMed Central  PubMed  Google Scholar 

  69. Yakubov E, Rechavi G, Rozenblatt S, Givol D (2010) Reprogramming of human fibroblasts to pluripotent stem cells using mRNA of four transcription factors. Biochem Biophys Res Commun 394(1):189–193

    CAS  PubMed  Google Scholar 

  70. Warren L et al (2010) Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7(5):618–630

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Yoshioka N et al (2013) Efficient generation of human iPSCs by a synthetic self-replicative RNA. Cell Stem Cell 13(2):246–254

    CAS  PubMed  Google Scholar 

  72. Kim D et al (2009) Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4(6):472–476

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Zhou HY et al (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4(5):381–384

    CAS  PubMed  Google Scholar 

  74. Lee J et al (2012) Activation of innate immunity is required for efficient nuclear reprogramming. Cell 151(3):547–558

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Hou P et al (2013) Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341(6146):651–654

    CAS  PubMed  Google Scholar 

  76. Lee G et al (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461(7262):402–406

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Lee G et al (2012) Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat Biotechnol 30(12):1244–1248

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Dimos JT et al (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321(5893):1218–1221

    CAS  PubMed  Google Scholar 

  79. Egawa N et al (2012) Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci Transl Med 4(145):145ra104

    PubMed  Google Scholar 

  80. Bilican B et al (2012) Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci U S A 109(15):5803–5808

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Burkhardt MF et al (2013) A cellular model for sporadic ALS using patient-derived induced pluripotent stem cells. Mol Cell Neurosci 56:355–364

    CAS  PubMed  Google Scholar 

  82. Gipson IK (2007) The ocular surface: the challenge to enable and protect vision: the Friedenwald lecture. Invest Ophthalmol Vis Sci 48(10):4390, 4391–4398

    PubMed Central  PubMed  Google Scholar 

  83. Kinoshita S et al (2001) Characteristics of the human ocular surface epithelium. Prog Retin Eye Res 20(5):639–673

    CAS  PubMed  Google Scholar 

  84. Wilson SE, Hong JW (2000) Bowman’s layer structure and function: critical or dispensable to corneal function? A hypothesis. Cornea 19(4):417–420

    CAS  PubMed  Google Scholar 

  85. Germundsson J, Karanis G, Fagerholm P, Lagali N (2013) Age-related thinning of Bowman’s layer in the human cornea in vivo. Invest Ophthalmol Vis Sci 54(9):6143–6149

    PubMed  Google Scholar 

  86. Radner W, Zehetmayer M, Aufreiter R, Mallinger R (1998) Interlacing and cross-angle distribution of collagen lamellae in the human cornea. Cornea 17(5):537–543

    CAS  PubMed  Google Scholar 

  87. Rada JA, Cornuet PK, Hassell JR (1993) Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp Eye Res 56(6):635–648

    CAS  PubMed  Google Scholar 

  88. Muller LJ, Pels L, Vrensen GF (1995) Novel aspects of the ultrastructural organization of human corneal keratocytes. Invest Ophthalmol Vis Sci 36(13):2557–2567

    CAS  PubMed  Google Scholar 

  89. Johnson DH, Bourne WM, Campbell RJ (1982) The ultrastructure of Descemet’s membrane. I. Changes with age in normal corneas. Arch Ophthalmol 100(12):1942–1947

    CAS  PubMed  Google Scholar 

  90. Stiemke MM, McCartney MD, Cantu-Crouch D, Edelhauser HF (1991) Maturation of the corneal endothelial tight junction. Invest Ophthalmol Vis Sci 32(10):2757–2765

    CAS  PubMed  Google Scholar 

  91. Fischbarg J, Lim JJ (1974) Role of cations, anions and carbonic anhydrase in fluid transport across rabbit corneal endothelium. J Physiol 241(3):647–675

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Maurice DM (1972) The location of the fluid pump in the cornea. J Physiol 221(1):43–54

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Tan DT, Dart JK, Holland EJ, Kinoshita S (2012) Corneal transplantation. Lancet 379(9827):1749–1761

    PubMed  Google Scholar 

  94. Peh GS, Beuerman RW, Colman A, Tan DT, Mehta JS (2011) Human corneal endothelial cell expansion for corneal endothelium transplantation: an overview. Transplantation 91(8):811–819

    PubMed  Google Scholar 

  95. Davanger M, Evensen A (1971) Role of the pericorneal papillary structure in renewal of corneal epithelium. Nature 229(5286):560–561

    CAS  PubMed  Google Scholar 

  96. Dua HS, Forrester JV (1990) The corneoscleral limbus in human corneal epithelial wound healing. Am J Ophthalmol 110(6):646–656

    CAS  PubMed  Google Scholar 

  97. Majo F, Rochat A, Nicolas M, Jaoude GA, Barrandon Y (2008) Oligopotent stem cells are distributed throughout the mammalian ocular surface. Nature 456(7219):250–254

    CAS  PubMed  Google Scholar 

  98. Barbaro V et al (2007) C/EBPdelta regulates cell cycle and self-renewal of human limbal stem cells. J Cell Biol 177(6):1037–1049

    CAS  PubMed Central  PubMed  Google Scholar 

  99. Dua HS, Shanmuganathan VA, Powell-Richards AO, Tighe PJ, Joseph A (2005) Limbal epithelial crypts: a novel anatomical structure and a putative limbal stem cell niche. Br J Ophthalmol 89(5):529–532

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Pellegrini G et al (2001) p63 identifies keratinocyte stem cells. Proc Natl Acad Sci U S A 98(6):3156–3161

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Cotsarelis G, Cheng SZ, Dong G, Sun TT, Lavker RM (1989) Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57(2):201–209

    CAS  PubMed  Google Scholar 

  102. Di Iorio E et al (2005) Isoforms of DeltaNp63 and the migration of ocular limbal cells in human corneal regeneration. Proc Natl Acad Sci U S A 102(27):9523–9528

    PubMed Central  PubMed  Google Scholar 

  103. Figueira EC, Di Girolamo N, Coroneo MT, Wakefield D (2007) The phenotype of limbal epithelial stem cells. Invest Ophthalmol Vis Sci 48(1):144–156

    PubMed  Google Scholar 

  104. Watanabe K et al (2004) Human limbal epithelium contains side population cells expressing the ATP-binding cassette transporter ABCG2. FEBS Lett 565(1–3):6–10

    CAS  PubMed  Google Scholar 

  105. Di Girolamo N et al (2008) Localization of the low-affinity nerve growth factor receptor p75 in human limbal epithelial cells. J Cell Mol Med 12(6B):2799–2811

    PubMed  Google Scholar 

  106. Chen Z et al (2004) Characterization of putative stem cell phenotype in human limbal epithelia. Stem Cells 22(3):355–366

    PubMed Central  PubMed  Google Scholar 

  107. Chee KY, Kicic A, Wiffen SJ (2006) Limbal stem cells: the search for a marker. Clin Experiment Ophthalmol 34(1):64–73

    PubMed  Google Scholar 

  108. Truong TT, Huynh K, Nakatsu MN, Deng SX (2011) SSEA4 is a potential negative marker for the enrichment of human corneal epithelial stem/progenitor cells. Invest Ophthalmol Vis Sci 52(9):6315–6320

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Draper JS, Pigott C, Thomson JA, Andrews PW (2002) Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat 200(pt 3):249–258

    CAS  PubMed Central  PubMed  Google Scholar 

  110. Pellegrini G et al (1997) Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 349(9057):990–993

    CAS  PubMed  Google Scholar 

  111. Tsubota K et al (1999) Treatment of severe ocular-surface disorders with corneal epithelial stem-cell transplantation. N Engl J Med 340(22):1697–1703

    CAS  PubMed  Google Scholar 

  112. Mariappan I et al (2010) In vitro culture and expansion of human limbal epithelial cells. Nat Protoc 5(8):1470–1479

    CAS  PubMed  Google Scholar 

  113. Rama P et al (2010) Limbal stem-cell therapy and long-term corneal regeneration. N Engl J Med 363(2):147–155

    CAS  PubMed  Google Scholar 

  114. Scott JE (1996) Proteodermatan and proteokeratan sulfate (decorin, lumican/fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry 35(27):8795–8799

    CAS  PubMed  Google Scholar 

  115. Chakravarti S et al (1998) Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141(5):1277–1286

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Funderburgh ML, Du Y, Mann MM, SundarRaj N, Funderburgh JL (2005) PAX6 expression identifies progenitor cells for corneal keratocytes. FASEB J 19(10):1371–1373

    CAS  PubMed Central  PubMed  Google Scholar 

  117. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183(4):1797–1806

    CAS  PubMed  Google Scholar 

  118. Pfister O, Oikonomopoulos A, Sereti KI, Liao R (2010) Isolation of resident cardiac progenitor cells by Hoechst 33342 staining. Methods Mol Biol 660:53–63

    CAS  PubMed  Google Scholar 

  119. Motohashi N, Alexander MS, Casar JC, Kunkel LM (2012) Identification of a novel microRNA that regulates the proliferation and differentiation in muscle side population cells. Stem Cells Dev 21(16):3031–3043

    CAS  PubMed Central  PubMed  Google Scholar 

  120. Wang J et al (2010) The presence of a side population and its marker ABCG2 in human deciduous dental pulp cells. Biochem Biophys Res Commun 400(3):334–339

    CAS  PubMed  Google Scholar 

  121. Vieyra DS, Rosen A, Goodell MA (2009) Identification and characterization of side population cells in embryonic stem cell cultures. Stem Cells Dev 18(8):1155–1166

    CAS  PubMed Central  PubMed  Google Scholar 

  122. Du Y, Funderburgh ML, Mann MM, SundarRaj N, Funderburgh JL (2005) Multipotent stem cells in human corneal stroma. Stem Cells 23(9):1266–1275

    PubMed Central  PubMed  Google Scholar 

  123. Chao JR, Bronner ME, Lwigale PY (2013) Human fetal keratocytes have multipotent characteristics in the developing avian embryo. Stem Cells Dev 22(15):2186–2195

    PubMed  Google Scholar 

  124. Doughty MJ (1989) Toward a quantitative analysis of corneal endothelial cell morphology: a review of techniques and their application. Optom Vis Sci 66(9):626–642

    CAS  PubMed  Google Scholar 

  125. Williams K, Watsky M (2002) Gap junctional communication in the human corneal endothelium and epithelium. Curr Eye Res 25(1):29–36

    PubMed  Google Scholar 

  126. To CH, Kong CW, Chan CY, Shahidullah M, Do CW (2002) The mechanism of aqueous humour formation. Clin Exp Optom 85(6):335–349

    PubMed  Google Scholar 

  127. Carlson KH, Bourne WM, McLaren JW, Brubaker RF (1988) Variations in human corneal endothelial cell morphology and permeability to fluorescein with age. Exp Eye Res 47(1):27–41

    CAS  PubMed  Google Scholar 

  128. Bourne WM, Nelson LR, Hodge DO (1997) Central corneal endothelial cell changes over a ten-year period. Invest Ophthalmol Vis Sci 38(3):779–782

    CAS  PubMed  Google Scholar 

  129. Joyce NC (2012) Proliferative capacity of corneal endothelial cells. Exp Eye Res 95(1):16–23

    CAS  PubMed Central  PubMed  Google Scholar 

  130. Kaufman HE, Katz JI (1977) Pathology of the corneal endothelium. Invest Ophthalmol Vis Sci 16(4):265–268

    CAS  PubMed  Google Scholar 

  131. Laing RA, Sanstrom MM, Berrospi AR, Leibowitz HM (1976) Changes in the corneal endothelium as a function of age. Exp Eye Res 22(6):587–594

    CAS  PubMed  Google Scholar 

  132. Peh GS, Toh KP, Wu FY, Tan DT, Mehta JS (2011) Cultivation of human corneal endothelial cells isolated from paired donor corneas. PLoS One 6(12):e28310

    CAS  PubMed Central  PubMed  Google Scholar 

  133. Choi JS et al (2010) Bioengineering endothelialized neo-corneas using donor-derived corneal endothelial cells and decellularized corneal stroma. Biomaterials 31(26):6738–6745

    CAS  PubMed  Google Scholar 

  134. Proulx S et al (2009) Transplantation of a tissue-engineered corneal endothelium reconstructed on a devitalized carrier in the feline model. Invest Ophthalmol Vis Sci 50(6):2686–2694

    PubMed  Google Scholar 

  135. Levis HJ et al (2012) Plastic compressed collagen as a novel carrier for expanded human corneal endothelial cells for transplantation. PLoS One 7(11):e50993

    CAS  PubMed Central  PubMed  Google Scholar 

  136. Koizumi N, Okumura N, Kinoshita S (2012) Development of new therapeutic modalities for corneal endothelial disease focused on the proliferation of corneal endothelial cells using animal models. Exp Eye Res 95(1):60–67

    CAS  PubMed  Google Scholar 

  137. Hirata-Tominaga K et al (2013) Corneal endothelial cell fate is maintained by LGR5 through the regulation of hedgehog and Wnt pathway. Stem Cells 31(7):1396–1407

    CAS  PubMed  Google Scholar 

  138. Barker N et al (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449(7165):1003–1007

    CAS  PubMed  Google Scholar 

  139. Jaks V et al (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40(11):1291–1299

    CAS  PubMed  Google Scholar 

  140. Barker N et al (2010) Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6(1):25–36

    CAS  PubMed  Google Scholar 

  141. McGowan SL, Edelhauser HF, Pfister RR, Whikehart DR (2007) Stem cell markers in the human posterior limbus and corneal endothelium of unwounded and wounded corneas. Mol Vis 13:1984–2000

    CAS  PubMed  Google Scholar 

  142. Tripathi RC, Tripathi BJ (1982) Human trabecular endothelium, corneal endothelium, keratocytes, and scleral fibroblasts in primary cell culture. A comparative study of growth characteristics, morphology, and phagocytic activity by light and scanning electron microscopy. Exp Eye Res 35(6):611–624

    CAS  PubMed  Google Scholar 

  143. Grierson I, Marshall J, Robins E (1983) Human trabecular meshwork in primary culture: a morphological and autoradiographic study. Exp Eye Res 37(4):349–365

    CAS  PubMed  Google Scholar 

  144. Stamer WD, Seftor RE, Williams SK, Samaha HA, Snyder RW (1995) Isolation and culture of human trabecular meshwork cells by extracellular matrix digestion. Curr Eye Res 14(7):611–617

    CAS  PubMed  Google Scholar 

  145. Gonzalez P, Epstein DL, Luna C, Liton PB (2006) Characterization of free-floating spheres from human trabecular meshwork (HTM) cell culture in vitro. Exp Eye Res 82(6):959–967

    CAS  PubMed Central  PubMed  Google Scholar 

  146. Tay CY, Sathiyanathan P, Chu SW, Stanton LW, Wong TT (2012) Identification and characterization of mesenchymal stem cells derived from the trabecular meshwork of the human eye. Stem Cells Dev 21(9):1381–1390

    CAS  PubMed  Google Scholar 

  147. Hatou S et al (2013) Functional corneal endothelium derived from corneal stroma stem cells of neural crest origin by retinoic acid and Wnt/beta-catenin signaling. Stem Cells Dev 22(5):828–839

    CAS  PubMed  Google Scholar 

  148. Gage PJ, Rhoades W, Prucka SK, Hjalt T (2005) Fate maps of neural crest and mesoderm in the mammalian eye. Invest Ophthalmol Vis Sci 46(11):4200–4208

    PubMed  Google Scholar 

  149. Chambers SM et al (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27(3):275–280

    CAS  PubMed Central  PubMed  Google Scholar 

  150. Menendez L, Yatskievych TA, Antin PB, Dalton S (2011) Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc Natl Acad Sci U S A 108(48):19240–19245

    CAS  PubMed Central  PubMed  Google Scholar 

  151. Jin ZB et al (2011) Modeling retinal degeneration using patient-specific induced pluripotent stem cells. PLoS One 6(2):e17084

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Tucker BA et al (2013) Patient-specific iPSC-derived photoreceptor precursor cells as a means to investigate retinitis pigmentosa. Elife 2:e00824

    PubMed Central  PubMed  Google Scholar 

  153. Singh R et al (2013) iPS cell modeling of Best disease: insights into the pathophysiology of an inherited macular degeneration. Hum Mol Genet 22(3):593–607

    CAS  PubMed Central  PubMed  Google Scholar 

  154. Minegishi Y et al (2013) Enhanced optineurin E50K-TBK1 interaction evokes protein insolubility and initiates familial primary open-angle glaucoma. Hum Mol Genet 22(17):3559–3567

    CAS  PubMed  Google Scholar 

  155. Du Y et al (2009) Stem cell therapy restores transparency to defective murine corneas. Stem Cells 27(7):1635–1642

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful for support from National Research Foundation Translational and Clinical Research Programme Grant (R1020/35/2013TCR) (G.S.L. Peh), Biomedical Research Council Translational Clinical Research Partnership Grant (R827/22/2011TCRPA) (G.S.L. Peh), Cranbourne Foundation (R.C.B. Wong), ORIA/RANZCO Eye Foundation Grant (R.C.B. Wong) and the University of Melbourne ECR Grant (R.C.B. Wong). The Centre for Eye Research Australia (R.C.B. Wong) receives operational infrastructure support from the Victorian government.

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Authors and Affiliations

  1. Singapore National Eye Centre, Singapore, Singapore

    Gary S. L. Peh

  2. Centre for Eye Research Australia and the Department of Ophthalmology, Royal Victorian Eye and Ear Hospital, University of Melbourne, Level 1, 32 Gisbourne Street, East Melbourne, VIC, 3002, Australia

    Raymond C. B. Wong

  3. Department of Ophthalmology, University of Melbourne, East Melbourne, VIC, Australia

    Raymond C. B. Wong

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  1. Gary S. L. Peh
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  2. Raymond C. B. Wong
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Correspondence to Raymond C. B. Wong .

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  1. Centre for Eye Research Australia, Royal Victorian Eye and Ear Hospital, Department of Ophthalmology, The University of Melbourne, East Melbourne, Victoria, Australia

    Alice Pébay

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Peh, G.S.L., Wong, R.C.B. (2014). Advances in Pluripotent and Adult Stem Cells for Eye Research. In: Pébay, A. (eds) Regenerative Biology of the Eye. Stem Cell Biology and Regenerative Medicine. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0787-8_5

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