Human induced pluripotent stem cell-derived podocytes mature into vascularized glomeruli upon experimental transplantation

Journal of the American Society of Nephrology

Volumn 27, Issue 6, 2016, Pages 1778-1791

  Sharmin, Sazia ^a   Taguchi, Atsuhiro ^a   Kaku, Yusuke ^a   Yoshimura, Yasuhiro ^a   Ohmori, Tomoko ^a   Sakuma, Tetsushi ^b   Mukoyama, Masashi ^a   Yamamoto, Takashi ^b   Kurihara, Hidetake ^c   Nishinakamura, Ryuichi ^a,d  

^a KUMAMOTO UNIVERSITY   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; GREEN FLUORESCENT PROTEIN; NEPHRIN; PODOCALYXIN; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UVOMORULIN;

ADULT; ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; CELL ISOLATION; CELL MATURATION; CELL SELECTION; CELL SURFACE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; EXPERIMENTAL TRANSPLANTATION; GENE EXPRESSION; GLOMERULUS; HISTOLOGY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INDUCED PLURIPOTENT STEM CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PODOCYTE; PRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SCANNING ELECTRON MICROSCOPY; START CODON; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CELL CULTURE; CELL TRANSPLANTATION; CYTOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; VASCULARIZATION;

ANIMALS; CELL TRANSPLANTATION; CELLS, CULTURED; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KIDNEY GLOMERULUS; MICE; PODOCYTES;

EID: 85016960125     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015010096     Document Type: Article

References (57)

1. Quaggin SE, Kreidberg JA: Development of the renal glomerulus: Good neighbors and good fences. Development 135: 609-620, 2008
2. Schell C,Wanner N, Huber TB: Glomerular development-shaping the multi-cellular filtration unit. Semin Cell Dev Biol 36: 39-49, 2014
3. Kestilä M, Lenkkeri U,MännikköM, Lamerdin J,McCready P, Putaala H, Ruotsalainen V,Morita T, NissinenM, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K: Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1: 575-582, 1998
4. Ruotsalainen V, Ljungberg P, Wartiovaara J, Lenkkeri U, Kestilä M, JalankoH,HolmbergC, Tryggvason K:Nephrin is specifically located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci U S A 96: 7962-7967, 1999
5. Patrakka J, Tryggvason K: Nephrin-a unique structural and signaling protein of the kidney filter. Trends Mol Med 13: 396-403, 2007
6. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C: NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroidresistant nephrotic syndrome. Nat Genet 24: 349-354, 2000
7. Donoviel DB, Freed DD, Vogel H, Potter DG, Hawkins E, Barrish JP, Mathur BN, Turner CA, Geske R, Montgomery CA, Starbuck M, Brandt M, Gupta A, Ramirez-Solis R, Zambrowicz BP, Powell DR: Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol Cell Biol 21: 4829-4836, 2001
8. Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP: Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3: 169-181, 2008
9. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP: Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 9: 283-292, 2005
10. Guo G,Morrison DJ, Licht JD,Quaggin SE:WT1 activates a glomerularspecific enhancer identified from the human nephrin gene. J Am Soc Nephrol 15: 2851-2856, 2004
11. Lindenmeyer MT, Eichinger F, Sen K, Anders H-J, Edenhofer I, Mattinzoli D, Kretzler M, Rastaldi MP, Cohen CD: Systematic analysis of a novel human renal glomerulus-enriched gene expression dataset. PLoS One 5: e11545, 2010
12. Naruse K, Fujieda M, Miyazaki E, Hayashi Y: An immunohistochemical study of developing glomeruli in human fetal kidneys. Kidney Int 57: 1836-1846, 2000
13. Taguchi A, Kaku Y, Ohmori T, Sharmin S, Ogawa M, Sasaki H, Nishinakamura R: Redefining the in vivo origin ofmetanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell 14: 53-67, 2014
14. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y,Miller JC, Zeitler B, Cherone JM,Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R: Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29: 731-734, 2011
15. Ruotsalainen V, Patrakka J, Tissari P, Reponen P, Hess M, Kestilä M, Holmberg C, Salonen R, Heikinheimo M, Wartiovaara J, Tryggvason K, Jalanko H: Role of nephrin in cell junction formation in human nephrogenesis. Am J Pathol 157: 1905-1916, 2000
16. Bariety J, Mandet C, Hill GS, Bruneval P: Parietal podocytes in normal human glomeruli. J AmSoc Nephrol 17: 2770-2780, 2006
17. Brièare N, Magny P: Scanning electron microscopic observations of human fetal kidney maturing in vivo and in serum-free organ culture. Anat Rec 235: 461-474, 1993
18. Hyodo T, Naguro T, Kameie T, Iino A, Miyagawa I: Scanning and transmission electron-microscopic study of the development of the podocyte in the human fetus. Pediatr Nephrol 11: 133-139, 1997
19. Ruotsalainen V, Reponen P, Khoshnoodi J, Kilpeläinen P, Tryggvason K: Monoclonal antibodies to human nephrin. Hybrid Hybridomics 23: 55-63, 2004
20. She X, RohlCA, Castle JC, Kulkarni AV, JohnsonJM,Chen R:Definition, conservation and epigenetics of housekeeping and tissue-enriched genes. BMC Genomics 10: 269, 2009
21. Brunskill EW, Georgas K, Rumballe B, Little MH, Potter SS: Defining the molecular character of the developing and adult kidney podocyte. PLoS One 6: e24640, 2011
22. Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, Kanagawa O, Miner JH, Shaw AS: Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 286: 312-315, 1999
23. Pierchala BA, Muñoz MR, Tsui CC: Proteomic analysis of the slit diaphragm complex: CLIC5 is a protein critical for podocyte morphology and function. Kidney Int 78: 868-882, 2010
24. Asanuma K, Campbell KN, Kim K, Faul C, Mundel P: Nuclear relocation of the nephrin and CD2AP-binding protein dendrin promotes apoptosis of podocytes. Proc Natl Acad Sci U S A 104: 10134-10139, 2007
25. Xiao Z, Rodriguez PQ, He L, Betsholtz C, Tryggvason K, Patrakka J: Wtip-and gadd45a-interacting protein dendrin is not crucial for the development or maintenance of the glomerular filtration barrier. PLoS One 8: e83133, 2013
26. Has C, Spartà G, Kiritsi D, Weibel L, Moeller A, Vega-Warner V,Waters A, He Y, Anikster Y, Esser P, Straub B, Hausser I, Bockenhauer D, Dekel B, Hildebrandt F, Bruckner-Tuderman L, Laube G: Integrin a3 mutations with kidney, lung, and skin disease. N Engl J Med 366: 1508-1514, 2012
27. Shukrun R, Vivante A, PleniceanuO, Vax E, Anikster Y, Dekel B, LotanD: A human integrin-a3 mutation confers major renal developmental defects. PLoS One 9: e90879, 2014
28. Hinkes B, Wiggins RC, Gbadegesin R, Vlangos CN, Seelow D, Nürnberg G, Garg P, Verma R, Chaib H, Hoskins BE, Ashraf S, Becker C, Hennies HC, Goyal M, Wharram BL, Schachter AD, Mudumana S, Drummond I, Kerjaschki D, Waldherr R, Dietrich A, Ozaltin F, Bakkaloglu A, Cleper R, Basel-Vanagaite L, Pohl M, Griebel M, Tsygin AN, Soylu A,Müller D, Sorli CS, Bunney TD, KatanM, Liu J, Attanasio M, O'toole JF,Hasselbacher K,Mucha B,Otto EA, Airik R, Kispert A, Kelley GG, Smrcka AV, Gudermann T, Holzman LB, Nürnberg P, Hildebrandt F: Positional cloning uncovers mutations in PLCE1 responsible for a nephrotic syndrome variant that may be reversible. Nat Genet 38: 1397-1405, 2006
29. TheMay-Hegglin/Fechtner Syndrome Consortium:Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes. Nat Genet 26: 103-105, 2000
30. Kelley MJ, Jawien W, Ortel TL, Korczak JF: Mutation of MYH9, encoding non-muscle myosin heavy chain A, in May-Hegglin anomaly. Nat Genet 26: 106-108, 2000
31. Sison K, Eremina V, Baelde H,Min W, HirashimaM, Fantus IG,Quaggin SE: Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling. J Am Soc Nephrol 21: 1691-1701, 2010
32. Kazama I, Mahoney Z, Miner JH, Graf D, Economides AN, Kreidberg JA: Podocyte-derived BMP7 is critical for nephron development. J Am Soc Nephrol 19: 2181-2191, 2008
33. Neumann-Haefelin E, Kramer-Zucker A, Slanchev K, Hartleben B, NoutsouF,MartinK,WannerN,Ritter A, GödelM, Pagel P, FuX,Müller A, Baumeister R, Walz G, Huber TB: A model organism approach: Defining the role of Neph proteins as regulators of neuron and kidney morphogenesis. Hum Mol Genet 19: 2347-2359, 2010
34. Takemoto M, He L, Norlin J, Patrakka J, Xiao Z, Petrova T, Bondjers C, Asp J, Wallgard E, Sun Y, Samuelsson T, Mostad P, Lundin S, Miura N, Sado Y, Alitalo K, Quaggin SE, Tryggvason K, Betsholtz C: Large-scale identification of genes implicated in kidney glomerulus development and function. EMBO J 25: 1160-1174, 2006
35. Fan X, Li Q, Pisarek-Horowitz A, Rasouly HM, Wang X, Bonegio RG, Wang H, McLaughlin M, Mangos S, Kalluri R, Holzman LB, Drummond IA, Brown D, Salant DJ, LuW: Inhibitory effects of Robo2 on nephrin: A crosstalk between positive and negative signals regulating podocyte structure. Cell Reports 2: 52-61, 2012
36. Hashimoto T, Karasawa T, Saito A, Miyauchi N, Han GD, Hayasaka K, Shimizu F, Kawachi H: Ephrin-B1 localizes at the slit diaphragm of the glomerular podocyte. Kidney Int 72: 954-964, 2007
37. Suh JH, Miner JH: The glomerular basement membrane as a barrier to albumin. Nat Rev Nephrol 9: 470-477, 2013
38. Takebe T, Sekine K, Enomura M, KoikeH, KimuraM,Ogaeri T, Zhang RR, Ueno Y, Zheng Y-W, Koike N, Aoyama S, Adachi Y, Taniguchi H: Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499: 481-484, 2013
39. Takebe T, Enomura M, Yoshizawa E, Kimura M, Koike H, Ueno Y, Matsuzaki T, Yamazaki T, Toyohara T, Osafune K, Nakauchi H, Yoshikawa HY, Taniguchi H: Vascularized and complex organ buds from diverse tissues via mesenchymal cell-driven condensation. Cell Stem Cell 16: 556-565, 2015
40. Ichimura K, Stan RV, Kurihara H, Sakai T: Glomerular endothelial cells form diaphragms during development and pathologic conditions. J Am Soc Nephrol 19: 1463-1471, 2008
41. TakasatoM, Er PX, BecroftM, Vanslambrouck JM, Stanley EG, Elefanty AG, Little MH: Directing human embryonic stem cell differentiation towards a renal lineage generates a self-organizing kidney. Nat Cell Biol 16: 118-126, 2013
42. Lam AQ, Freedman BS, Morizane R, Lerou PH, Valerius MT, Bonventre JV: Rapid and efficient differentiation of human pluripotent stem cells into intermediate mesoderm that forms tubules expressing kidney proximal tubular markers. J Am SocNephrol 25: 1211-1225, 2014
43. Mae S, Shono A, Shiota F, Yasuno T, KajiwaraM, Gotoda-Nishimura N, Arai S, Sato-Otubo A, Toyoda T, Takahashi K, NakayamaN, Cowan CA, Aoi T,Ogawa S,McMahonAP, Yamanaka S,Osafune K:Monitoring and robust induction of nephrogenic intermediate mesoderm from human pluripotent stem cells. Nat Commun 4: 1367, 2013
44. Humphreys BD, Lin S-L, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176: 85-97, 2010
45. Kobayashi A, Mugford JW, Krautzberger AM, Naiman N, Liao J, McMahon AP: Identification of a multipotent self-renewing stromal progenitor population duringmammalian kidney organogenesis. Stem Cell Reports 3: 650-662, 2014
46. Sariola H: Incomplete fusion of the epithelial and endothelial basement membranes in interspecies hybrid glomeruli. CellDiffer 14: 189-195, 1984
47. Vernier RL, Birch-Andersen A: Studies of the human fetal kidney. J Pediatr 60: 754-768, 1963
48. Lizardo-Daudt HM, Edelweiss MI, Dos Santos FT, Schumacher RCA: Diagnosis of the human fetal age based on the development of the normal kidney. J Bras PatolMed Lab 38: 135-139, 2002
49. Rice WL, Van Hoek AN, Pǎunescu TG, Huynh C, Goetze B, Singh B, Scipioni L, Stern LA, Brown D: High resolution helium ion scanning microscopy of the rat kidney. PLoS One 8: e57051, 2013
50. Sakuma T, Ochiai H, Kaneko T, Mashimo T, Tokumasu D, Sakane Y, Suzuki K, Miyamoto T, Sakamoto N, Matsuura S, Yamamoto T: Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity. Sci Rep 3: 3379, 2013
51. Nakagawa Y, Yamamoto T, Suzuki K-I, Araki K, Takeda N,Ohmuraya M, Sakuma T: Screening methods to identify TALEN-mediated knockout mice. Exp Anim 63: 79-84, 2014
52. 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 131: 861-872, 2007
53. Tucker KL, Wang Y, Dausman J, Jaenisch R: A transgenic mouse strain expressing four drug-selectable marker genes. Nucleic Acids Res 25: 3745-3746, 1997
54. Nakagawa M, Taniguchi Y, Senda S, Takizawa N, Ichisaka T, Asano K, Morizane A, Doi D, Takahashi J, Nishizawa M, Yoshida Y, Toyoda T, Osafune K, Sekiguchi K, Yamanaka S: A novel efficient feeder-free culture system for the derivation of human induced pluripotent stem cells. Sci Rep 4: 3594, 2014
55. Cho EA, Patterson LT, Brookhiser WT, Mah S, Kintner C, Dressler GR: Differential expression and function of cadherin-6 during renal epithelium development. Development 125: 803-812, 1998
56. Brunskill EW, Sequeira-Lopez MLS, Pentz ES, Lin E, Yu J, Aronow BJ, Potter SS, Gomez RA: Genes that confer the identity of the renin cell. J Am Soc Nephrol 22: 2213-2225, 2011
57. Okada S, Harada H, Ito T, Saito T, Suzu S: Early development of human hematopoietic and acquired immune systems in new born NOD/Scid/Jak3null mice intrahepatic engrafted with cord blood-derived CD34 + cells. Int J Hematol 88: 476-482, 2008