Recreating kidney progenitors from pluripotent cells

Pediatric Nephrology

Volumn 29, Issue 4, 2014, Pages 543-552

  Takasato, Minoru ^a   Maier, Barbara ^a   Little, Melissa H ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Directed differentiation; Embryonic stem cell; Kidney development; Kidney progenitor

Indexed keywords

ACTIVIN A; OSTEOGENIC PROTEIN 1; TRANSCRIPTION FACTOR PAX2;

CELL DIFFERENTIATION; CONFERENCE PAPER; EMBRYONIC STEM CELL; GENE EXPRESSION; HUMAN; INNER CELL MASS; KIDNEY CELL; KIDNEY DEVELOPMENT; KIDNEY PROXIMAL TUBULE; MESENCHYMAL STEM CELL; MESODERM; MONOLAYER CULTURE; NEPHRON; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIMITIVE STREAK; PRIORITY JOURNAL; REGENERATIVE MEDICINE; STROMA CELL;

ANIMALS; CELL DIFFERENTIATION; HUMANS; KIDNEY; ORGANOGENESIS; PLURIPOTENT STEM CELLS; TISSUE ENGINEERING;

EID: 84896696490     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-013-2592-7     Document Type: Conference Paper

References (84)

1. Bertram JF, Douglas-Denton RN, Diouf B, Hughson MD, Hoy WE (2011) Human nephron number: implications for health and disease. Pediatr Nephrol 26(9):1529-1533
2. Rumballe BA, Georgas KM, Combes A, Ju A, Gilbert T, Little MH (2011) Nephron formation adopts a novel spatial topology at cessation of nephrogenesis. Dev Biol 360(1):110-122
3. Chang CC, Boland ED, Williams SK, Hoying JB (2011) Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J Biomed Mater Res B Appl Biomater 98(1):160-170
4. Mironov V, Drake C, Wen X (2006) Research project: Charleston Bioengineered Kidney Project. Biotechnol J 1(9):903-905
5. Skardal A, Zhang JX, Prestwich GD (2010) Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 31:6173-6181
6. Reiffel AJ, Kafka C, Hernandez KA, Popa S, Perez JL, Zhou S, Pramanik S, Brown BN, Ryu WS, Bonassar LJ, Spector JA (2013) High-fidelity tissue engineering of patient-specific auricles for reconstruction of pediatric microtia and other auricular deformities. PLoS One 8(2):e56506
7. Badylak SF (2007) The extracellular matrix as a biologic scaffold material. Biomaterials 28(25):3587-3593
8. Song JJ, Guyette JP, Gilpin SE, Gonzalez G, Vacanti JP, Ott HC (2013) Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med 19(5):646-651
9. Okita K, Yamanaka S (2011) Induced pluripotent stem cells: opportunities and challenges. Philos Trans R Soc Lond B Biol Sci 366(1575):2198-2207
10. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27(3):275-280
11. Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, Henckaerts E, Bonham K, Abbott GW, Linden RM, Field LJ, Keller GM (2008) Human cardiovascular progenitor cells develop from a KDR + embryonic-stem-cell-derived population. Nature 453(7194):524-528
12. Chen S, Borowiak M, Fox JL, Maehr R, Osafune K, Davidow L, Lam K, Peng LF, Schreiber SL, Rubin LL, Melton D (2009) A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat Chem Biol 4:258-265
13. Davis RP, Ng ES, Costa M, Mossman AK, Sourris K, Elefanty AG, Stanley EG (2007) Targeting a GFP reporter gene to the MIXL1 locus of human embryonic stem cells identifies human primitive streak-like cells and enables isolation of primitive hematopoietic precursors. Blood 111(4):1876-1884
14. 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
15. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861-872
16. Collin J, Lako M (2011) Concise review: putting a finger on stem cell biology: zinc finger nuclease-driven targeted genetic editing in human pluripotent stem cells. Stem Cells 29(7):1021-1033
17. Sachinidis A, Sotiriadou I, Seelig B, Berkessel A, Hescheler J (2008) A chemical genetics approach for specific differentiation of stem cells to somatic cells: a new promising therapeutical approach. Comb Chem High Throughput Screen 11(1):70-82
18. Zhu S, Wurdak H, Schultz PG (2010) Directed embryonic stem cell differentiation with small molecules. Future Med Chem 2(6):965-973
19. Daley GQ (2003) From embryos to embryoid bodies: generating blood from embryonic stem cells. Ann N Y Acad Sci 996:122-131
20. Bradley A, Evans M, Kaufman MH, Robertson E (1984) Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309(5965):255-256
21. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145-1147
22. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, de Sousa C, Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448(7150):191-195
23. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448(7150):196-199
24. Schier AF (2003) Nodal signaling in vertebrate development. Ann Rev Cell Dev Biol 19:589-621
25. Shen MM (2007) Nodal signaling: developmental roles and regulation. Development 134:1023-1034
26. Pereira LA, Wong MS, Mei Lim S, Stanley EG, Elefanty AG (2012) The Mix family of homeobox genes-key regulators of mesendoderm formation during vertebrate development. Dev Biol 367:163-177
27. Wilson V, Manson L, Skarnes WC, Beddington RS (1995) The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation. Development 121:877-886
28. Hart AH, Hartley L, Sourris K, Stadler ES, Li R, Stanley EG, Tam PP, Elefanty AG, Robb L (2002) Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development 129(15):3597-3608
29. Sumi T, Tsuneyoshi N, Nakatsuji N, Suemori H (2008) Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135(17):2969-2979
30. Zhang P, Li J, Tan Z, Wang C, Liu T, Chen L, Yong J, Jiang W, Sun X, Du L, Ding M, Deng H (2008) Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood 111:1933-1941
31. Winnier G, Blessing M, Labosky PA, Hogan BL (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9:2105-2116
32. Kimelman D (2006) Mesoderm induction: from caps to chips. Nat Rev Genet 7:360-372
33. Beppu H, Kawabata M, Hamamoto T, Chytil A, Minowa O, Noda T, Miyazono K (2000) BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol 221:249-258
34. James RG, Schultheiss TM (2003) Patterning of the avian intermediate mesoderm by lateral plate and axial tissues. Dev Biol 253:109-124
35. Wijgerde M, Karp S, McMahon J, McMahon AP (2005) Noggin antagonism of BMP4 signaling controls development of the axial skeleton in the mouse. Dev Biol 286(1):149-157
36. James R, Schultheiss T (2005) Bmp signaling promotes intermediate mesoderm gene expression in a dose-dependent, cell-autonomous and translation-dependent manner. Dev Biol 288:113-125
37. Obara-Ishihara T, Kuhlman J, Niswander L, Herzlinger D (1999) The surface ectoderm is essential for nephric duct formation in intermediate mesoderm. Development 126(6):1103-1108
38. Sakai T, Larsen M, Yamada KM (2003) Fibronectin requirement in branching morphogenesis. Nature 423(6942):876-881
39. Abu-Abed S, Dollé P, Metzger D, Beckett B, Chambon P, Petkovich M (2001) The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15(2):226-240
40. Wellik DM, Hawkes PJ, Capecchi MR (2002) Hox11 paralogous genes are essential for metanephric kidney induction. Genes Dev 16(11):1423-1432
41. Niederreither K, Subbarayan V, Dollé P, Chambon P (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21(4):444-448
42. Serluca FC, Fishman MC (2001) Pre-pattern in the pronephric kidney field of zebrafish. Development 128:2233-2241
43. Cartry J, Nichane M, Ribes V, Colas A, Riou JF, Pieler T, Dollé P, Bellefroid EJ, Umbhauer M (2006) Retinoic acid signalling is required for specification of pronephric cell fate. Dev Biol 299:35-51
44. Osafune K, Nishinakamura R, Komazaki S, Asashima M (2002) In vitro induction of the pronephric duct in Xenopus explants. Dev Growth Differ 44:161-167
45. Wingert RA, Davidson AJ (2008) The zebrafish pronephros: a model to study nephron segmentation. Kidney Int 73:1120-1127
46. Little MH, McMahon AP (2012) Mammalian kidney development: principles, progress and projections. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a008300
47. Dudley AT, Godin RE, Robertson EJ (1999) Interaction between FGF and BMP signaling pathways regulates development of metanephric mesenchyme. Genes Dev 13(12):1601-1613
48. Barasch J, Qiao J, McWilliams G, Chen D, Oliver JA, Herzlinger D (1997) Ureteric bud cells secrete multiple factors, including bFGF, which rescue renal progenitors from apoptosis. Am J Physiol 273:F757-F767
49. Brown AC, Adams D, de Caestecker M, Yang X, Friesel R, Oxburgh L (2011) FGF/EGF signaling regulates the renewal of early nephron progenitors during embryonic development. Development 138(23):5099-5112
50. Barak H, Huh SH, Chen S, Jeanpierre C, Martinovic J, Parisot M, Bole-Feysot C, Nitschké P, Salomon R, Antignac C, Ornitz DM, Kopan R (2013) FGF9 and FGF20 maintain the stemness of nephron progenitors in mice and man. Dev Cell 22(6):1191-1207
51. Brown AC, Muthukrishnan SD, Guay JA, Adams DC, Schafer DA, Fetting JL, Oxburgh L (2013) Role for compartmentalization in nephron progenitor differentiation. Proc Natl Acad Sci USA 110(12):4640-4645
52. Blank U, Brown A, Adams DC, Karolak MJ, Oxburgh L (2009) BMP7 promotes proliferation of nephron progenitor cells via a JNK-dependent mechanism. Development 136(21):3557-3566
53. So PL, Danielian PS (1999) Cloning and expression analysis of a mouse gene related to Drosophila odd-skipped. Mech Dev 84:157-160
54. Cirio MC, Hui Z, Haldin CE, Cosentino CC, Stuckenholz C, Chen X, Hong SK, Dawid IB, Hukriede NA (2011) Lhx1 is required for specification of the renal progenitor cell field. PLoS One 6:e18858
55. Burgess R, Cserjesi P, Ligon KL, Olson EN (1995) Paraxis: a basic helix-loop-helix protein expressed in paraxial mesoderm and developing somites. Dev Biol 168(2):296-306
56. Chapman DL, Agulnik I, Hancock S, Silver LM, Papaioannou VE (1996) Tbx6, a mouse T-Box gene implicated in paraxial mesoderm formation at gastrulation. Dev Biol 180(2):534-542
57. Mahlapuu M, Ormestad M, Enerbäck S, Carlsson P (2001) The forkhead transcription factor Foxf1 is required for differentiation of extra-embryonic and lateral plate mesoderm. Development 128(2):155-166
58. James RG, Kamei CN, Wang Q, Jiang R, Schultheiss TM (2006) Odd-skipped related 1 is required for development of the metanephric kidney and regulates formation and differentiation of kidney precursor cells. Development 133:2995-3004
59. Dressler GR, Deutsch U, Chowdhury K, Nornes HO, Gruss P (1990) Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109:787-795
60. Mugford JW, Yu J, Kobayashi A, McMahon AP (2009) High-resolution gene expression analysis of the developing mouse kidney defines novel cellular compartments within the nephron progenitor population. Dev Biol 333(2):312-323
61. Georgas KM, Rumballe BA, Valerius MT, Chiu HS, Thiagarajan RD, Lesieur E, Aronow BJ, Brunskill EW, Combes AN, Tang D, Taylor D, Grimmond SM, Potter SS, McMahon AP, Little MH (2009) Analysis of early nephron patterning reveals a role for distal RV proliferation in fusion to the ureteric tip via a cap mesenchyme-derived connecting segment. Dev Biol 332(2):273-286
62. Thiagarajan R, Georgas K, Rumballe B, Lesieur E, Chiu H, Taylor D, Tang D, Grimmond SM, Little MH (2011) Identification of anchor genes during kidney development defines ontological relationships, molecular subcompartments and regulatory pathways. PLoS One 6(2):e17286
63. Brunskill EW, Georgas K, Rumballe B, Little MH, Potter SS (2011) Defining the molecular character of the developing and adult kidney podocyte. PLoS One 6(9):e24640
64. Georgas K, Rumballe B, Wilkinson L, Chiu HS, Lesieur E, Gilbert T, Little MH (2008) Use of dual section mRNA in situ hybridisation/immunohistochemistry to clarify gene expression patterns during the early stages of nephron development in the embryo and in the mature nephron of the adult mouse kidney. Histochem Cell Biol 130(5):927-942
65. Yamamoto M, Cui L, Johkura K, Asanuma K, Okouchi Y, Ogiwara N, Sasaki K (2005) Branching ducts similar to mesonephric ducts or ureteric buds in teratomas originating from mouse embryonic stem cells. Am J Physiol Renal Physiol 290(1):F52-F60
66. Steenhard B, Isom K, Cazcarro P, Dunmore J, Godwin A, St John P, Abrahamson D (2005) Integration of embryonic stem cells in metanephric kidney organ culture. J Am Soc Nephrol 16:1623-1631
67. Kim D, Dressler GR (2005) Nephrogenic factors promote differentiation of mouse embryonic stem cells into renal epithelia. J Am Soc Nephrol 16(12):3527-3534
68. Kobayashi T, Tanaka H, Kuwana H, Inoshita S, Teraoka H, Sasaki S, Terada Y (2005) Wnt4-transformed mouse embryonic stem cells differentiate into renal tubular cells. Biochem Biophys Res Commun 336:585-595
69. Bruce S, Rea R, Steptoe A, Busslinger M, Bertram J, Perkins A (2007) In vitro differentiation of murine embryonic stem cells toward a renal lineage. Differentiation 75:337-349
70. Vigneau C, Polgar K, Striker G, Elliott J, Hyink D, Weber O, Fehling HJ, Keller G, Burrow C, Wilson P (2007) Mouse embryonic stem cell-derived embryoid bodies generate progenitors that integrate long term into renal proximal tubules in vivo. J Am Soc Nephrol 18:1709-1720
71. Morizane R, Monkawa T, Itoh H (2009) Differentiation of murine embryonic stem and induced pluripotent stem cells to renal lineage in vitro. Biochem Biophys Res Commun 390:1334-1339
72. Ren X, Zhang J, Gong X, Niu X, Zhang X, Chen P, Zhang X (2010) Differentiation of murine embryonic stem cells toward renal lineages by conditioned medium from ureteric bud cells in vitro. Acta Biochim Biophys Sin (Shanghai) 42(7):464-471
73. Nishikawa M, Yanagawa N, Kojima N, Yuri S, Hauser PV, Jo OD, Yanagawa N (2012) Stepwise renal lineage differentiation of mouse embryonic stem cells tracing in vivo development. Biochem Biophys Res Commun 417(2):897-902
74. Mae S, Shirasawa S, Yoshie S, Sato F, Kanoh Y, Ichikawa H, Yokoyama T, Yue F, Tomotsune D, Sasaki K (2010) Combination of small molecules enhances differentiation of mouse embryonic stem cells into intermediate mesoderm through BMP7-positive cells. Biochem Biophys Res Commun 393(4):877-882
75. Karner CM, Das A, Ma Z, Self M, Chen C, Lum L, Oliver G, Carroll TJ (2011) Canonical Wnt9b signaling balances progenitor cell expansion and differentiation during kidney development. Development 138(7):1247-1257
76. Perantoni AO (2003) The ureteric bud. Tissue-culture approaches to branching morphogenesis and inductive signaling. Methods Mol Med 86:179-192
77. Rosselot C, Spraggon L, Chia I, Batourina E, Riccio P, Lu B, Niederreither K, Dolle P, Duester G, Chambon P, Costantini F, Gilbert T, Molotkov A, Mendelsohn C (2011) Non-cell-autonomous retinoid signaling is crucial for renal development. Development 137(2):283-292
78. Lin SA, Kolle G, Grimmond SM, Zhou Q, Doust E, Little MH, Aronow B, Ricardo SD, Pera MF, Bertram JF, Laslett AL (2010) Subfractionation of differentiating human embryonic stem cell populations allows the isolation of a mesodermal population enriched for intermediate mesoderm and putative renal progenitors. Stem Cells Dev 19(10):1637-1648
79. Challen GA, Martinez G, Davis M, Teasdale R, Grimmond S, Little MH (2004) Identifying the molecular phenotype of renal progenitor cells. J Am Soc Nephrol 15(9):2344-2357
80. Mae S, Shono A, Shiota F, Yasuno T, Kajiwara M, Gotoda-Nishimura N, Arai S, Sato-Otubo A, Toyoda T, Takahashi K, Nakayama N, Cowan CA, Aoi T, Ogawa S, McMahon AP, Yamanaka S, Osafune K (2013) Monitoring and robust induction of nephrogenic intermediate mesoderm from human pluripotent stem cells. Nat Commun 4:1367
81. Lusis M, Li J, Ineson J, Christensen ME, Rice A, Little MH (2010) Isolation of clonogenic, long-term self renewing embryonic renal stem cells. Stem Cell Res 5(1):23-39
82. Narayanan K, Schumacher KM, Tasnim F, Kandasamy K, Schumacher A, Ni M, Gao S, Gopalan B, Zink D, Ying JY (2013) Human embryonic stem cells differentiate into functional renal proximal tubular-like cells. Kidney Int 83(4):593-603
83. Song B, Smink AM, Jones CV, Callaghan JM, Firth SD, Bernard CA, Laslett AL, Kerr PG, Ricardo SD (2012) The directed differentiation of human iPS cells into kidney podocytes. PLoS One 7(9):e46453
84. Georgas KM, Chiu HS, Lesieur E, Rumballe BA, Little MH (2011) Expression of metanephric nephron-patterning genes in differentiating mesonephric tubules. Dev Dyn 240(6):1600-1612