In vivo maturation of functional renal organoids formed from embryonic cell suspensions

Journal of the American Society of Nephrology

Volumn 23, Issue 11, 2012, Pages 1857-1868

  Xinaris, Christodoulos ^a   Benedetti, Valentina ^a   Rizzo, Paola ^a   Abbate, Mauro ^a   Corna, Daniela ^a   Azzollini, Nadia ^a   Conti, Sara ^a   Unbekandt, Mathieu ^b   Davies, Jamie A ^b   Morigi, Marina ^a   Benigni, Ariela ^a   Remuzzi, Giuseppe ^a,c  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c OSPEDALI RIUNITI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL SUSPENSION; CYTOPLASM; EMBRYO CELL; GLOMERULUS; GLOMERULUS FILTRATION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KIDNEY PARENCHYMA; KIDNEY TUBULE ABSORPTION; MOUSE; NEPHRON; NONHUMAN; PRIORITY JOURNAL; RAT; TISSUE ENGINEERING; VASCULARIZATION;

EID: 84868622745     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012050505     Document Type: Article

References (48)

1. Yokoo T, Ohashi T, Shen JS, Sakurai K, Miyazaki Y, Utsunomiya Y, Takahashi M, Terada Y, Eto Y, Kawamura T, Osumi N, Hosoya T:Humanmesenchymal stem cells in rodent whole-embryo culture are reprogrammed to contribute to kidney tissues. Proc Natl Acad Sci U S A 102: 3296-3300, 2005
2. Song B, Niclis JC, Alikhan MA, Sakkal S, Sylvain A, Kerr PG, Laslett AL, Bernard CA, Ricardo SD: Generation of induced pluripotent stem cells from human kidney mesangial cells. J Am Soc Nephrol 22: 1213-1220, 2011
3. Thatava T, Armstrong AS, De Lamo JG, Edukulla R, Khan YK, Sakuma T, Ohmine S, Sundsbak JL, Harris PC, Kudva YC, Ikeda Y: Successful disease-specific induced pluripotent stemcell generation frompatients with kidney transplantation. Stem Cell Res Ther 2: 48, 2011
4. Unbekandt M, Davies JA: Dissociation of embryonic kidneys followed by reaggregation allows the formation of renal tissues. Kidney Int 77: 407-416, 2010
5. Ganeva V, Unbekandt M, Davies JA: An improved kidney dissociation and reaggregation culture system results in nephrons arranged organotypically around a single collecting duct system. Organogenesis 7: 83-87, 2011
6. Saxén L, Sariola H: Early organogenesis of the kidney. Pediatr Nephrol 1: 385-392, 1987
7. Vainio S, Lin Y: Coordinating early kidney development: Lessons from gene targeting. Nat Rev Genet 3: 533-543, 2002
8. Dressler GR: The cellular basis of kidney development. Annu Rev Cell Dev Biol 22: 509-529, 2006
9. Nigam SK, Shah MM: How does the ureteric bud branch? J Am Soc Nephrol 20: 1465-1469, 2009
10. Velagapudi C, Nilsson RP, Lee MJ, Burns HS, Ricono JM, Arar M, Barnes VL, Abboud HE, Barnes JL: Reciprocal induction of simple organogenesis by mouse kidney progenitor cells in three-dimensional coculture. Am J Pathol 180: 819-830, 2012
11. Bard JB, Gordon A, Sharp L, Sellers WI: Early nephron formation in the developing mouse kidney. J Anat 199: 385-392, 2001
12. Kitamoto Y, Tokunaga H, Miyamoto K, Tomita K: VEGF is an essential molecule for glomerular structuring. Nephrol Dial Transplant 17[Suppl 9]: 25-27, 2002
13. Kitamoto Y, Tokunaga H, Tomita K: Vascular endothelial growth factor is an essential molecule for mouse kidney development: Glomerulogenesis and nephrogenesis. J Clin Invest 99: 2351-2357, 1997
14. Tufro A, Norwood VF, Carey RM, Gomez RA: Vascular endothelial growth factor induces nephrogenesis and vasculogenesis. J Am Soc Nephrol 10: 2125-2134, 1999
15. Guan F, Villegas G, Teichman J, Mundel P, Tufro A: Autocrine VEGF-A system in podocytes regulates podocin and its interaction with CD2AP. Am J Physiol Renal Physiol 291: F422-F428, 2006
16. Quaggin SE, Kreidberg JA: Development of the renal glomerulus: Good neighbors and good fences. Development 135: 609-620, 2008
17. Rogers SA, Lowell JA, Hammerman NA, Hammerman MR: Transplantation of developing metanephroi into adult rats. Kidney Int 54: 27-37, 1998
18. Yokote S, Yokoo T, Matsumoto K, Utsunomiya Y, Kawamura T, Hosoya T: The effect of metanephros transplantation on blood pressure in anephric rats with induced acute hypotension [published online ahead of print April 18, 2012]. Nephrol Dial Transplant doi:10.1093/ndt/ gfs006
19. Matsumoto K, Yokoo T, Yokote S, Utsunomiya Y, Ohashi T, Hosoya T: Functional development of a transplanted embryonic kidney: Effect of transplantation site. J Nephrol 25: 50 - 55, 2012
20. Dilworth MR, Clancy MJ, Marshall D, Bravery CA, Brenchley PE, Ashton N: Development and functional capacity of transplanted rat metanephroi. Nephrol Dial Transplant 23: 871-879, 2008
21. Woolf AS, Palmer SJ, Snow ML, Fine LG: Creation of a functioning chimeric mammalian kidney. Kidney Int 38: 991-997, 1990
22. Dekel B, Burakova T, Arditti FD, Reich-Zeliger S, Milstein O, Aviel- Ronen S, Rechavi G, Friedman N, Kaminski N, Passwell JH, Reisner Y: Human and porcine early kidney precursors as a new source for transplantation. Nat Med 9: 53-60, 2003
23. Loughna S, Hardman P, Landels E, Jussila L, Alitalo K, Woolf AS: A molecular and genetic analysis of renalglomerular capillary development. Angiogenesis 1: 84-101, 1997
24. Robert B, St John PL, Hyink DP, Abrahamson DR: Evidence that embryonic kidney cells expressing flk-1 are intrinsic, vasculogenic angioblasts. Am J Physiol 271: F744-F753, 1996
25. Rosines E, Sampogna RV, Johkura K, Vaughn DA, Choi Y, Sakurai H, Shah MM, Nigam SK: Staged in vitro reconstitution and implantation of engineered rat kidney tissue. Proc Natl Acad Sci U S A 104: 20938-20943, 2007
26. Tufro-McReddie A, Norwood VF, Aylor KW, Botkin SJ, Carey RM, Gomez RA: Oxygen regulates vascular endothelial growth factormediated vasculogenesis and tubulogenesis. Dev Biol 183: 139-149, 1997
27. Loughna S, Yuan HT, Woolf AS: Effects of oxygen on vascular patterning in Tie1/LacZ metanephric kidneys in vitro. Biochem Biophys Res Commun 247: 361-366, 1998
28. 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
29. Abbate M, Brown D, Bonventre JV: Expression of NCAM recapitulates tubulogenic development in kidneys recovering from acute ischemia. Am J Physiol 277: F454-F463, 1999
30. Benigni A, Morigi M, Rizzo P, Gagliardini E, Rota C, Abbate M, Ghezzi S, Remuzzi A, Remuzzi G: Inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am J Pathol 179: 628-638, 2011
31. Ohse T, Pippin JW, Vaughan MR, Brinkkoetter PT, Krofft RD, Shankland SJ: Establishment of conditionally immortalized mouse glomerular parietal epithelial cells in culture. J Am Soc Nephrol 19: 1879-1890, 2008
32. Dressler GR, Deutsch U, Chowdhury K, Nornes HO, Gruss P: Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system. Development 109: 787-795, 1990
33. Laitinen L, Virtanen I, Saxén L: Changes in the glycosylation pattern during embryonic development of mouse kidney as revealed with lectin conjugates. J Histochem Cytochem 35: 55-65, 1987
34. Armstrong JF, Pritchard-Jones K, Bickmore WA, Hastie ND, Bard JB: The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech Dev 40: 85-97, 1993
35. Saxen L: Organogenesis of the Kidney , New York, Cambridge University Press, 1987
36. Davies JA, Garrod DR: Induction of early stages of kidney tubule differentiation by lithium ions. Dev Biol 167: 50-60, 1995
37. Yokoo T, Fukui A, Ohashi T, Miyazaki Y, Utsunomiya Y, Kawamura T, Hosoya T, Okabe M, Kobayashi E: Xenobiotic kidney organogenesis fromhumanmesenchymal stem cells using a growing rodent embryo. J Am Soc Nephrol 17: 1026-1034, 2006
38. Steer DL, Bush KT, Meyer TN, Schwesinger C, Nigam SK: A strategy for in vitro propagation of rat nephrons. Kidney Int 62: 1958 -1965, 2002
39. Osafune K, Takasato M, Kispert A, Asashima M, Nishinakamura R: Identification of multipotent progenitors in the embryonic mouse kidney by a novel colony-forming assay. Development 133: 151-161, 2006
40. Auerbach R, Grobstein C: Inductive interaction of embryonic tissues after dissociation and reaggregation. Exp Cell Res 15: 384-397, 1958
41. Coles HS, Burne JF, Raff MC: Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor. Development 118: 777-784, 1993
42. Giuliani S, Perin L, Sedrakyan S, Kokorowski P, Jin D, De Filippo R: Ex vivo whole embryonic kidney culture: A novel method for research in development, regeneration and transplantation. J Urol 179: 365-370, 2008
43. Ekblom P, Sariola H, Karkinen-Jääskeläinen M, Saxén L: The origin of the glomerular endothelium. Cell Differ 11: 35-39, 1982
44. Akimoto T, Hammerman MR: Microvessel formation from mouse aorta is stimulated in vitro by secreted VEGF and extracts from metanephroi. Am J Physiol Cell Physiol 284: C1625-C1632, 2003
45. Akimoto T, Liapis H, Hammerman MR: Microvessel formation from mouse embryonic aortic explants is oxygen and VEGF dependent. Am J Physiol Regul Integr Comp Physiol 283: R487-R495, 2002
46. De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A: Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25: 100-106, 2007
47. Siegel N, Rosner M, Unbekandt M, Fuchs C, Slabina N, Dolznig H, Davies JA, Lubec G, Hengstschläger M: Contribution of human amniotic fluid stem cells to renal tissue formation depends on mTOR. Hum Mol Genet 19: 3320-3331, 2010
48. Yokoo T, Fukui A, Matsumoto K, Ohashi T, Sado Y, Suzuki H, Kawamura T, Okabe M, Hosoya T, Kobayashi E: Generation of a transplantable erythropoietin-producer derived fromhumanmesenchymal stemcells. Transplantation 85: 1654-1658, 2008