Modeling Neural Crest Induction, Melanocyte Specification, and Disease-Related Pigmentation Defects in hESCs and Patient-Specific iPSCs

Cell Reports

Volumn 3, Issue 4, 2013, Pages 1140-1152

  Mica, Yvonne ^a   Lee, Gabsang ^a,b   Chambers, Stuart M ^a   Tomishima, Mark J ^a   Studer, Lorenz ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; ENDOTHELIN 3; GLYCOGEN SYNTHASE KINASE 3BETA; WNT PROTEIN;

ARTICLE; CELL ISOLATION; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; CELL ULTRASTRUCTURE; CHEDIAK HIGASHI SYNDROME; CONTROLLED STUDY; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MELANOBLAST; MELANOCYTE; MELANOSOME; NEURAL CREST; OCULAR ALBINISM; PIGMENT DISORDER; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CHEDIAK-HIGASHI SYNDROME; EMBRYONIC STEM CELLS; ENDOTHELIN-3; GLYCOGEN SYNTHASE KINASE 3; GREEN FLUORESCENT PROTEINS; HERMANSKI-PUDLAK SYNDROME; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MELANOCYTES; MODELS, BIOLOGICAL; NEURAL CREST; PIGMENTATION; SIGNAL TRANSDUCTION; SOXE TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84876959225     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.03.025     Document Type: Article

References (62)

1. Adameyko I., Lallemend F., Aquino J.B., Pereira J.A., Topilko P., Müller T., Fritz N., Beljajeva A., Mochii M., Liste I., et al. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 2009, 139:366-379.
2. Baynash A.G., Hosoda K., Giaid A., Richardson J.A., Emoto N., Hammer R.E., Yanagisawa M. Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons. Cell 1994, 79:1277-1285.
3. Betters E., Liu Y., Kjaeldgaard A., Sundström E., García-Castro M.I. Analysis of early human neural crest development. Dev. Biol. 2010, 344:578-592.
4. Braun M.M., Etheridge A., Bernard A., Robertson C.P., Roelink H. Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development 2003, 130:5579-5587.
5. Chambers S.M., Fasano C.A., Papapetrou E.P., Tomishima M., Sadelain M., Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 2009, 27:275-280.
6. Chambers S.M., Mica Y., Studer L., Tomishima M.J. Converting human pluripotent stem cells to neural tissue and neurons to model neurodegeneration. Methods Mol. Biol. 2011, 793:87-97.
7. Chambers S.M., Qi Y., Mica Y., Lee G., Zhang X.-J., Niu L., Bilsland J., Cao L., Stevens E., Whiting P., et al. Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat. Biotechnol. 2012, 30:715-720.
8. Colombo S., Champeval D., Rambow F., Larue L. Transcriptomic analysis of mouse embryonic skin cells reveals previously unreported genes expressed in melanoblasts. J. Invest. Dermatol. 2012, 132:170-178.
9. Creuzet S., Couly G., Le Douarin N.M. Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J. Anat. 2005, 207:447-459.
10. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., Croft G.F., Saphier G., Leibel R., Goland R., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
11. Dupin E., Le Douarin N.M. Development of melanocyte precursors from the vertebrate neural crest. Oncogene 2003, 22:3016-3023.
12. Dupin E., Glavieux C., Vaigot P., Le Douarin N.M. Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc. Natl. Acad. Sci. USA 2000, 97:7882-7887.
13. Ebert A.D., Yu J., Rose F.F., Mattis V.B., Lorson C.L., Thomson J.A., Svendsen C.N. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009, 457:277-280.
14. Elkabetz Y., Panagiotakos G., Al Shamy G., Socci N.D., Tabar V., Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 2008, 22:152-165.
15. Fang D., Leishear K., Nguyen T.K., Finko R., Cai K., Fukunaga M., Li L., Brafford P.A., Kulp A.N., Xu X., et al. Defining the conditions for the generation of melanocytes from human embryonic stem cells. Stem Cells 2006, 24:1668-1677.
16. Fasano C.A., Chambers S.M., Lee G., Tomishima M.J., Studer L. Efficient derivation of functional floor plate tissue from human embryonic stem cells. Cell Stem Cell 2010, 6:336-347.
17. Friedmann P.S., Gilchrest B.A. Ultraviolet radiation directly induces pigment production by cultured human melanocytes. J. Cell. Physiol. 1987, 133:88-94.
18. Fujimura N., Vacik T., Machon O., Vlcek C., Scalabrin S., Speth M., Diep D., Krauss S., Kozmik Z. Wnt-mediated down-regulation of Sp1 target genes by a transcriptional repressor Sp5. J. Biol. Chem. 2007, 282:1225-1237.
19. García-Castro M.I., Marcelle C., Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science 2002, 297:848-851.
20. Hari L., Miescher I., Shakhova O., Suter U., Chin L., Taketo M., Richardson W.D., Kessaris N., Sommer L. Temporal control of neural crest lineage generation by Wnt/β-catenin signaling. Development 2012, 139:2107-2117.
21. Huizing M., Scher C.D., Strovel E., Fitzpatrick D.L., Hartnell L.M., Anikster Y., Gahl W.A. Nonsense mutations in ADTB3A cause complete deficiency of the beta3A subunit of adaptor complex-3 and severe Hermansky-Pudlak syndrome type 2. Pediatr. Res. 2002, 51:150-158.
22. Introne W., Boissy R.E., Gahl W.A. Clinical, molecular, and cell biological aspects of Chediak-Higashi syndrome. Mol. Genet. Metab. 1999, 68:283-303.
23. Karim M.A., Nagle D.L., Kandil H.H., Bürger J., Moore K.J., Spritz R.A. Mutations in the Chediak-Higashi syndrome gene (CHS1) indicate requirement for the complete 3801 amino acid CHS protein. Hum. Mol. Genet. 1997, 6:1087-1089.
24. Kléber M., Lee H.-Y., Wurdak H., Buchstaller J., Riccomagno M.M., Ittner L.M., Suter U., Epstein D.J., Sommer L. Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. J. Cell Biol. 2005, 169:309-320.
25. Kriks S., Shim J.-W., Piao J., Ganat Y.M., Wakeman D.R., Xie Z., Carrillo-Reid L., Auyeung G., Antonacci C., Buch A., et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011, 480:547-551.
26. Kunisada T., Yoshida H., Yamazaki H., Miyamoto A., Hemmi H., Nishimura E., Shultz L.D., Nishikawa S., Hayashi S. Transgene expression of steel factor in the basal layer of epidermis promotes survival, proliferation, differentiation and migration of melanocyte precursors. Development 1998, 125:2915-2923.
27. LaBonne C., Bronner-Fraser M. Neural crest induction in Xenopus: evidence for a two-signal model. Development 1998, 125:2403-2414.
28. Lagutin O.V., Zhu C.C., Kobayashi D., Topczewski J., Shimamura K., Puelles L., Russell H.R.C., McKinnon P.J., Solnica-Krezel L., Oliver G. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 2003, 17:368-379.
29. Lahav R., Ziller C., Dupin E., Le Douarin N.M. Endothelin 3 promotes neural crest cell proliferation and mediates a vast increase in melanocyte number in culture. Proc. Natl. Acad. Sci. USA 1996, 93:3892-3897.
30. Lavado A., Lagutin O.V., Oliver G. Six3 inactivation causes progressive caudalization and aberrant patterning of the mammalian diencephalon. Development 2008, 135:441-450.
31. Le Douarin N.M., Creuzet S., Couly G., Dupin E. Neural crest cell plasticity and its limits. Development 2004, 131:4637-4650.
32. Lee G., Kim H., Elkabetz Y., Al Shamy G., Panagiotakos G., Barberi T., Tabar V., Studer L. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat. Biotechnol. 2007, 25:1468-1475.
33. Lee G., Papapetrou E.P., Kim H., Chambers S.M., Tomishima M.J., Fasano C.A., Ganat Y.M., Menon J., Shimizu F., Viale A., et al. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 2009, 461:402-406.
34. Lee G., Chambers S.M., Tomishima M.J., Studer L. Derivation of neural crest cells from human pluripotent stem cells. Nat. Protoc. 2010, 5:688-701.
35. Luo R., Gao J., Wehrle-Haller B., Henion P.D. Molecular identification of distinct neurogenic and melanogenic neural crest sublineages. Development 2003, 130:321-330.
36. Marchant L., Linker C., Ruiz P., Guerrero N., Mayor R. The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev. Biol. 1998, 198:319-329.
37. Meier F., Nesbit M., Hsu M.Y., Martin B., Van Belle P., Elder D.E., Schaumburg-Lever G., Garbe C., Walz T.M., Donatien P., et al. Human melanoma progression in skin reconstructs: biological significance of bFGF. Am. J. Pathol. 2000, 156:193-200.
38. Meijer L., Flajolet M., Greengard P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 2004, 25:471-480.
39. Menendez L., Yatskievych T.A., Antin P.B., Dalton S. Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc. Natl. Acad. Sci. USA 2011, 108:19240-19245.
40. Nagle D.L., Karim M.A., Woolf E.A., Holmgren L., Bork P., Misumi D.J., McGrail S.H., Dussault B.J., Perou C.M., Boissy R.E., et al. Identification and mutation analysis of the complete gene for Chediak-Higashi syndrome. Nat. Genet. 1996, 14:307-311.
41. Nissan X., Larribere L., Saidani M., Hurbain I., Delevoye C., Feteira J., Lemaitre G., Peschanski M., Baldeschi C. Functional melanocytes derived from human pluripotent stem cells engraft into pluristratified epidermis. Proc. Natl. Acad. Sci. USA 2011, 108:14861-14866.
42. Oh J., Bailin T., Fukai K., Feng G.H., Ho L., Mao J.I., Frenk E., Tamura N., Spritz R.A. Positional cloning of a gene for Hermansky-Pudlak syndrome, a disorder of cytoplasmic organelles. Nat. Genet. 1996, 14:300-306.
43. Papapetrou E.P., Lee G., Malani N., Setty M., Riviere I., Tirunagari L.M.S., Kadota K., Roth S.L., Giardina P., Viale A., et al. Genomic safe harbors permit high β-globin transgene expression in thalassemia induced pluripotent stem cells. Nat. Biotechnol. 2011, 29:73-78.
44. Park I.-H., Zhao R., West J.A., Yabuuchi A., Huo H., Ince T.A., Lerou P.H., Lensch M.W., Daley G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008, 451:141-146.
45. Park I.H., Arora N., Huo H., Maherali N., Ahfeldt T., Shimamura A., Lensch M.W., Cowan C., Hochedlinger K., Daley G.Q. Disease-specific induced pluripotent stem cells. Cell 2008, 134:877-886.
46. Patthey C., Gunhaga L., Edlund T. Early development of the central and peripheral nervous systems is coordinated by Wnt and BMP signals. PLoS One 2008, 3. e1625.
47. Reid K., Nishikawa S., Bartlett P.F., Murphy M. Steel factor directs melanocyte development in vitro through selective regulation of the number of c-kit+ progenitors. Dev. Biol. 1995, 169:568-579.
48. Reid K., Turnley A.M., Maxwell G.D., Kurihara Y., Kurihara H., Bartlett P.F., Murphy M. Multiple roles for endothelin in melanocyte development: regulation of progenitor number and stimulation of differentiation. Development 1996, 122:3911-3919.
49. Ring D.B., Johnson K.W., Henriksen E.J., Nuss J.M., Goff D., Kinnick T.R., Ma S.T., Reeder J.W., Samuels I., Slabiak T., et al. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 2003, 52:588-595.
50. Selleck M.A., García-Castro M.I., Artinger K.B., Bronner-Fraser M. Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development 1998, 125:4919-4930.
51. Steel K.P., Davidson D.R., Jackson I.J. TRP-2/DT, a new early melanoblast marker, shows that steel growth factor (c-kit ligand) is a survival factor. Development 1992, 115:1111-1119.
52. Steventon B., Araya C., Linker C., Kuriyama S., Mayor R. Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. Development 2009, 136:771-779.
53. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
54. Thomas A.J., Erickson C.A. The making of a melanocyte: the specification of melanoblasts from the neural crest. Pigment Cell Melanoma Res. 2008, 21:598-610.
55. Veeman M.T., Slusarski D.C., Kaykas A., Louie S.H., Moon R.T. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 2003, 13:680-685.
56. Wei M.L. Hermansky-Pudlak syndrome: a disease of protein trafficking and organelle function. Pigment Cell Res. 2006, 19:19-42.
57. Weidinger G., Thorpe C.J., Wuennenberg-Stapleton K., Ngai J., Moon R.T. The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/beta-catenin signaling in mesoderm and neuroectoderm patterning. Curr. Biol. 2005, 15:489-500.
58. Wen-Jun L., Hai-Yan W., Wei L., Ke-Yu W., Rui-Ming W. Evidence that geniposide abrogates norepinephrine-induced hypopigmentation by the activation of GLP-1R-dependent c-kit receptor signaling in melanocyte. J. Ethnopharmacol. 2008, 118:154-158.
59. Xu J., Lamouille S., Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 2009, 19:156-172.
60. Yamane T., Hayashi S., Mizoguchi M., Yamazaki H., Kunisada T. Derivation of melanocytes from embryonic stem cells in culture. Dev. Dyn. 1999, 216:450-458.
61. Yoshida H., Kunisada T., Kusakabe M., Nishikawa S., Nishikawa S.I. Distinct stages of melanocyte differentiation revealed by anlaysis of nonuniform pigmentation patterns. Development 1996, 122:1207-1214.
62. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.