Derivation of mesenchymal stromal cells from pluripotent stem cells through a neural crest lineage using small molecule compounds with defined media

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Fukuta, Makoto ^a,b,c   Nakai, Yoshinori ^d   Kirino, Kosuke ^b   Nakagawa, Masato ^b   Sekiguchi, Kazuya ^a,b,e   Nagata, Sanae ^b   Matsumoto, Yoshihisa ^a,b,c   Yamamoto, Takuya ^b,f   Umeda, Katsutsugu ^e   Heike, Toshio ^e   Okumura, Naoki ^g   Koizumi, Noriko ^g   Sato, Takahiko ^d   Nakahata, Tatsutoshi ^b   Saito, Megumu ^b   Otsuka, Takanobu ^c   Kinoshita, Shigeru ^d   Ueno, Morio ^d   Ikeya, Makoto ^b   Toguchida, Junya ^a,b,e  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^d KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f KYOTO UNIVERSITY   (Japan)

^g DOSHISHA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOGEN SYNTHASE KINASE 3BETA INHIBITOR; GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA INHIBITOR; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN; CULTURE MEDIUM; INSULIN;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MIGRATION; CELL POPULATION; CELL THERAPY; CELL TYPE; CONTROLLED STUDY; CORNEA ENDOTHELIUM; CULTURE MEDIUM; DNA MICROARRAY; EMBRYONIC STEM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION PROFILING; GLIA; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MELANOCYTE; MESENCHYMAL STROMA CELL; NERVE CELL; NEURAL CREST CELL; PLURIPOTENT STEM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BONE DEVELOPMENT; CARTILAGE CELL; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; CORNEA; CYTOLOGY; ENDOTHELIUM CELL; FIBROBLAST; FLOW CYTOMETRY; METABOLISM; NEURAL CREST;

BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CORNEA; CULTURE MEDIA; DNA, COMPLEMENTARY; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; FIBROBLASTS; FLOW CYTOMETRY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INSULIN; MELANOCYTES; MESENCHYMAL STROMAL CELLS; NEURAL CREST; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOGENESIS; PLURIPOTENT STEM CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84914674829     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112291     Document Type: Article

References (53)

1. Liu Z, Tang Y, Lu S, Zhou J, Du Z, et al. (2013) The tumourigenicity of iPS cells and their differentiated derivates. J Cell Mol Med 17: 782-791.
2. Le Douarin NM, Dupin E (2003) Multipotentiality of the neural crest. Curr Opin Genet Dev 13: 529-536.
3. Sauka-Spengler T, Bronner-Fraser M (2008) A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9: 557-568.
4. Kalcheim C, Burstyn-Cohen T (2005) Early stages of neural crest ontogeny: formation and regulation of cell delamination. Int J Dev Biol 49: 105-116.
5. Kalcheim C (2000) Mechanisms of early neural crest development: from cell specification to migration. Int Rev Cytol 200: 143-196.
6. Vincent SD, Buckingham ME (2010) How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 90: 1-41.
7. Neirinckx V, Coste C, Rogister B, Wislet-Gendebien S (2013) Concise review: adult mesenchymal stem cells, adult neural crest stem cells, and therapy of neurological pathologies: a state of play. Stem Cells Transl Med 2: 284-296.
8. Neirinckx V, Marquet A, Coste C, Rogister B, Wislet-Gendebien S (2013) Adult bone marrow neural crest stem cells and mesenchymal stem cells are not able to replace lost neurons in acute MPTP-lesioned mice. PLoS One 8: e64723.
9. Giuliani M, Oudrhiri N, Noman ZM, Vernochet A, Chouaib S, et al. (2011) Human mesenchymal stem cells derived from induced pluripotent stem cells down-regulate NK-cell cytolytic machinery. Blood 118: 3254-3262.
10. Villa-Diaz LG, Brown SE, Liu Y, Ross AM, Lahann J, et al. (2012) Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells 30: 1174-1181.
11. Liu Q, Spusta SC, Mi R, Lassiter RN, Stark MR, et al. (2012) Human neural crest stem cells derived from human ESCs and induced pluripotent stem cells: induction, maintenance, and differentiation into functional schwann cells. Stem Cells Transl Med 1: 266-278.
12. Chimge NO, Bayarsaihan D (2010) Generation of neural crest progenitors from human embryonic stem cells. J Exp Zool B Mol Dev Evol 314: 95-103.
13. Milet C, Monsoro-Burq AH (2012) Embryonic stem cell strategies to explore neural crest development in human embryos. Dev Biol 366: 96-99.
14. 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: 19240-19245.
15. Mica Y, Lee G, Chambers SM, Tomishima MJ, Studer L (2013) Modeling neural crest induction, melanocyte specification, and disease-related pigmentation defects in hESCs and patient-specific iPSCs. Cell Rep 3: 1140-1152.
16. Suemori H, Yasuchika K, Hasegawa K, Fujioka T, Tsuneyoshi N, et al. (2006) Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochem Biophys Res Commun 345: 926-932.
17. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, et al. (2000) Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227: 271-278.
18. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, et al. (2011) A more efficient method to generate integration-free human iPS cells. Nat Methods 8: 409-412.
19. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
20. McMahon AP, Bradley A (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62: 1073-1085.
21. Nakagawa M, Taniguchi Y, Senda S, Takizawa N, Ichisaka T, et al. (2014) A novel efficient feeder-free culture system for the derivation of human induced pluripotent stem cells. Sci Rep 4: 3594.
22. Nasu A, Ikeya M, Yamamoto T, Watanabe A, Jin Y, et al. (2013) Genetically matched human iPS cells reveal that propensity for cartilage and bone differentiation differs with clones, not cell type of origin. PLoS One 8: e53771.
23. Wataya T, Ando S, Muguruma K, Ikeda H, Watanabe K, et al. (2008) Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation. Proc Natl Acad Sci U S A 105: 11796-11801.
24. Colleoni S, Galli C, Giannelli SG, Armentero MT, Blandini F, et al. (2010) Long-term culture and differentiation of CNS precursors derived from anterior human neural rosettes following exposure to ventralizing factors. Exp Cell Res 316: 1148-1158.
25. James MJ, Jarvinen E, Wang XP, Thesleff I (2006) Different roles of Runx2 during early neural crest-derived bone and tooth development. J Bone Miner Res 21: 1034-1044.
26. Lee G, Chambers SM, Tomishima MJ, Studer L (2010) Derivation of neural crest cells from human pluripotent stem cells. Nat Protoc 5: 688-701.
27. Ohta S, Imaizumi Y, Okada Y, Akamatsu W, Kuwahara R, et al. (2011) Generation of human melanocytes from induced pluripotent stem cells. PLoS One 6: e16182.
28. Fang D, Leishear K, Nguyen TK, Finko R, Cai K, et al. (2006) Defining the conditions for the generation of melanocytes from human embryonic stem cells. Stem Cells 24: 1668-1677.
29. Ju C, Zhang K, Wu X (2012) Derivation of corneal endothelial cell-like cells from rat neural crest cells in vitro. PLoS One 7: e42378.
30. Umeda K, Zhao J, Simmons P, Stanley E, Elefanty A, et al. (2012) Human chondrogenic paraxial mesoderm, directed specification and prospective isolation from pluripotent stem cells. Sci Rep 2: 455.
31. Okamoto T, Aoyama T, Nakayama T, Nakamata T, Hosaka T, et al. (2002) Clonal heterogeneity in differentiation potential of immortalized human mesenchymal stem cells. Biochem Biophys Res Commun 295: 354-361.
32. Kreitzer FR, Salomonis N, Sheehan A, Huang M, Park JS, et al. (2013) A robust method to derive functional neural crest cells from human pluripotent stem cells. Am J Stem Cells 2: 119-131.
33. Lee G, Ramirez CN, Kim H, Zeltner N, Liu B, et al. (2012) Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat Biotechnol 30: 1244-1248.
34. Kimura C, Takeda N, Suzuki M, Oshimura M, Aizawa S, et al. (1997) Cis-acting elements conserved between mouse and pufferfish Otx2 genes govern the expression in mesencephalic neural crest cells. Development 124: 3929-3941.
35. Qiu M, Bulfone A, Ghattas I, Meneses JJ, Christensen L, et al. (1997) Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev Biol 185: 165-184.
36. Manley NR, Capecchi MR (1995) The role of Hoxa-3 in mouse thymus and thyroid development. Development 121: 1989-2003.
37. Liu Z, Yu S, Manley NR (2007) Gcm2 is required for the differentiation and survival of parathyroid precursor cells in the parathyroid/thymus primordia. Dev Biol 305: 333-346.
38. Motohashi T, Aoki H, Yoshimura N, Kunisada T (2006) Induction of melanocytes from embryonic stem cells and their therapeutic potential. Pigment Cell Res 19: 284-289.
39. Johnston MC, Noden DM, Hazelton RD, Coulombre JL, Coulombre AJ (1979) Origins of avian ocular and periocular tissues. Exp Eye Res 29: 27-43.
40. Trainor PA, Tam PP (1995) Cranial paraxial mesoderm and neural crest cells of the mouse embryo: codistribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development 121: 2569-2582.
41. Fitch JM, Birk DE, Linsenmayer C, Linsenmayer TF (1990) The spatial organization of Descemet's membrane-associated type IV collagen in the avian cornea. J Cell Biol 110: 1457-1468.
42. De Schauwer C, Meyer E, Van de Walle GR, Van Soom A (2011) Markers of stemness in equine mesenchymal stem cells: a plea for uniformity. Theriogenology 75: 1431-1443.
43. Lee G, Kim H, Elkabetz Y, Al Shamy G, Panagiotakos G, et al. (2007) Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 25: 1468-1475.
44. Curchoe CL, Maurer J, McKeown SJ, Cattarossi G, Cimadamore F, et al. (2010) Early acquisition of neural crest competence during hESCs neuralization. PLoS One 5: e13890.
45. Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, et al. (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463: 958-962.
46. Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, et al. (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461: 402-406.
47. Jiang M, Stanke J, Lahti JM (2011) The connections between neural crest development and neuroblastoma. Curr Top Dev Biol 94: 77-127.
48. Caplan AI (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213: 341-347.
49. Silva NA, Sousa N, Reis RL, Salgado AJ (2013) From basics to clinical: A comprehensive review on spinal cord injury. Prog Neurobiol.
50. Helms JA, Schneider RA (2003) Cranial skeletal biology. Nature 423: 326-331.
51. Morikawa S, Mabuchi Y, Niibe K, Suzuki S, Nagoshi N, et al. (2009) Development of mesenchymal stem cells partially originate from the neural crest. Biochem Biophys Res Commun 379: 1114-1119.
52. Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, et al. (2007) Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129: 1377-1388.
53. Cai J, Yang M, Poremsky E, Kidd S, Schneider JS, et al. (2010) Dopaminergic neurons derived from human induced pluripotent stem cells survive and integrate into 6-OHDA-lesioned rats. Stem Cells Dev 19: 1017-1023.