The number of fetal nephron progenitor cells limits ureteric branching and adult nephron endowment

Cell Reports

Volumn 7, Issue 1, 2014, Pages 127-137

  Cebrian, Cristina ^a   Asai, Naoya ^a   D'Agati, Vivette ^b   Costantini, Frank ^a  

^a Department of Genetics and Development Columbia University ^*  (United States)

^b Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; SPROUTY PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRANCHING MORPHOGENESIS; CAP MESENCHYME; CELL COUNT; CELL RENEWAL; CONTROLLED STUDY; FETUS DEVELOPMENT; GROWTH RATE; INFANT; KIDNEY AGENESIS; KIDNEY DEVELOPMENT; KIDNEY HYPOPLASIA; KIDNEY INTERSTITIUM; KIDNEY SIZE; MOUSE; NEPHRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; URETER; URETER BUD; ANIMAL; CYTOLOGY; EMBRYOLOGY; FEMALE; KIDNEY; MORPHOGENESIS; PREGNANCY;

ANIMALS; FEMALE; KIDNEY; MICE; MORPHOGENESIS; NEPHRONS; PREGNANCY; STEM CELLS;

EID: 84898028444     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.02.033     Document Type: Article

References (68)

1. Basson M.A., Watson-Johnson J., Shakya R., Akbulut S., Hyink D., Costantini F.D., Wilson P.D., Mason I.J., Licht J.D. Branching morphogenesis of the ureteric epithelium during kidney development is coordinated by the opposing functions of GDNF and Sprouty1. Dev. Biol. 2006, 299:466-477.
2. Benz K., Campean V., Cordasic N., Karpe B., Neuhuber W., Mall G., Hartner A., Hilgers K.F., Amann K. Early glomerular alterations in genetically determined low nephron number. Am. J. Physiol. Renal Physiol. 2011, 300:F521-F530.
3. Bertram J.F., Douglas-Denton R.N., Diouf B., Hughson M.D., Hoy W.E. Human nephron number: implications for health and disease. Pediatr. Nephrol. 2011, 26:1529-1533.
4. Boyle S., Misfeldt A., Chandler K.J., Deal K.K., Southard-Smith E.M., Mortlock D.P., Baldwin H.S., de Caestecker M. Fate mapping using Cited1-CreERT2 mice demonstrates that the cap mesenchyme contains self-renewing progenitor cells and gives rise exclusively to nephronic epithelia. Dev. Biol. 2008, 313:234-245.
5. Brunskill E.W., Aronow B.J., Georgas K., Rumballe B., Valerius M.T., Aronow J., Kaimal V., Jegga A.G., Yu J., Grimmond S., et al. Atlas of gene expression in the developing kidney at microanatomic resolution. Dev. Cell 2008, 15:781-791.
6. Brunskill E.W., Lai H.L., Jamison D.C., Potter S.S., Patterson L.T. Microarrays and RNA-Seq identify molecular mechanisms driving the end of nephron production. BMC Dev. Biol. 2011, 11:15.
7. Burn S.F. Detection of β-galactosidase activity: X-gal staining. Methods Mol. Biol. 2012, 886:241-250.
8. Byun J., Verardo M.R., Sumengen B., Lewis G.P., Manjunath B.S., Fisher S.K. Automated tool for the detection of cell nuclei in digital microscopic images: application to retinal images. Mol. Vis. 2006, 12:949-960.
9. Cacalano G., Fariñas I., Wang L.C., Hagler K., Forgie A., Moore M., Armanini M., Phillips H., Ryan A.M., Reichardt L.F., et al. GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 1998, 21:53-62.
10. Cain J.E., Di Giovanni V., Smeeton J., Rosenblum N.D. Genetics of renal hypoplasia: insights into the mechanisms controlling nephron endowment. Pediatr. Res. 2010, 68:91-98.
11. Carroll T.J., Park J.S., Hayashi S., Majumdar A., McMahon A.P. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev. Cell 2005, 9:283-292.
12. Costantini F. Renal branching morphogenesis: concepts, questions, and recent advances. Differentiation 2006, 74:402-421.
13. Costantini F. Genetic controls and cellular behaviors in branching morphogenesis of the renal collecting system. Wiley Interdiscip. Rev. Dev. Biol. 2012, 1:693-713.
14. Costantini F., Kopan R. Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev. Cell 2010, 18:698-712.
15. Costantini F., Shakya R. GDNF/Ret signaling and the development of the kidney. Bioessays 2006, 28:117-127.
16. Costantini F., Watanabe T., Lu B., Chi X., Srinivas S. Dissection of embryonic mouse kidney, culture invitro, and imaging of the developing organ. Cold Spring Harb. Protoc. 2011, 2011. pdb.prot5613.
17. Cullen-McEwen L.A., Drago J., Bertram J.F. Nephron endowment in glial cell line-derived neurotrophic factor (GDNF) heterozygous mice. Kidney Int. 2001, 60:31-36.
18. Douglas-Denton R., Moritz K.M., Bertram J.F., Wintour E.M. Compensatory renal growth after unilateral nephrectomy in the ovine fetus. J.Am. Soc. Nephrol. 2002, 13:406-410.
19. Duffield J.S. Macrophages in kidney repair and regeneration. J.Am. Soc. Nephrol. 2011, 22:199-201.
20. Durbec P., Marcos-Gutierrez C.V., Kilkenny C., Grigoriou M., Wartiowaara K., Suvanto P., Smith D., Ponder B., Costantini F., Saarma M., et al. GDNF signalling through the Ret receptor tyrosine kinase. Nature 1996, 381:789-793.
21. Enomoto H., Araki T., Jackman A., Heuckeroth R.O., Snider W.D., Johnson E.M., Milbrandt J. GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 1998, 21:317-324.
22. Feil R., Wagner J., Metzger D., Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 1997, 237:752-757.
23. Georgas K., Rumballe B., Valerius M.T., Chiu H.S., Thiagarajan R.D., Lesieur E., Aronow B.J., Brunskill E.W., Combes A.N., Tang D., et al. 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. 2009, 332:273-286.
24. Grobstein C. Inductive tissue interaction in development. Adv. Cancer Res. 1956, 4:187-236.
25. Gu G., Dubauskaite J., Melton D.A. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002, 129:2447-2457.
26. Hartman H.A., Lai H.L., Patterson L.T. Cessation of renal morphogenesis in mice. Dev. Biol. 2007, 310:379-387.
27. Hayashi S., McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 2002, 244:305-318.
28. Hellmich H.L., Kos L., Cho E.S., Mahon K.A., Zimmer A. Embryonic expression of glial cell-line derived neurotrophic factor (GDNF) suggests multiple developmental roles in neural differentiation and epithelial-mesenchymal interactions. Mech. Dev. 1996, 54:95-105.
29. Hendry C., Rumballe B., Moritz K., Little M.H. Defining and redefining the nephron progenitor population. Pediatr. Nephrol. 2011, 26:1395-1406.
30. Honjo T., Nishizuka Y., Kato I., Hayaishi O. Adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis by diphtheria toxin. J.Biol. Chem. 1971, 246:4251-4260.
31. Hoy W.E., Hughson M.D., Singh G.R., Douglas-Denton R., Bertram J.F. Reduced nephron number and glomerulomegaly in Australian Aborigines: a group at high risk for renal disease and hypertension. Kidney Int. 2006, 70:104-110.
32. Humphreys B.D., Valerius M.T., Kobayashi A., Mugford J.W., Soeung S., Duffield J.S., McMahon A.P., Bonventre J.V. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008, 2:284-291.
33. Humphreys B.D., Lin S.L., Kobayashi A., Hudson T.E., Nowlin B.T., Bonventre J.V., Valerius M.T., McMahon A.P., Duffield J.S. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 2010, 176:85-97.
34. Ishibe S., Karihaloo A., Ma H., Zhang J., Marlier A., Mitobe M., Togawa A., Schmitt R., Czyczk J., Kashgarian M., et al. Met and the epidermal growth factor receptor act cooperatively to regulate final nephron number and maintain collecting duct morphology. Development 2009, 136:337-345.
35. Keller G., Zimmer G., Mall G., Ritz E., Amann K. Nephron number in patients with primary hypertension. N.Engl. J. Med. 2003, 348:101-108.
36. Kobayashi A., Valerius M.T., Mugford J.W., Carroll T.J., Self M., Oliver G., McMahon A.P. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 2008, 3:169-181.
37. Kopan R., Cheng H.T., Surendran K. Molecular insights into segmentation along the proximal-distal axis of the nephron. J.Am. Soc. Nephrol. 2007, 18:2014-2020.
38. LeBleu V.S., Taduri G., O'Connell J., Teng Y., Cooke V.G., Woda C., Sugimoto H., Kalluri R. Origin and function of myofibroblasts in kidney fibrosis. Nat. Med. 2013, 19:1047-1053.
39. Lefevre J., Marshall D.J., Combes A.N., Ju A.L., Little M.H., Hamilton N.A. Modelling cell turnover in a complex tissue during development. J.Theor. Biol. 2013, 338:66-79.
40. Little M.H., McMahon A.P. Mammalian kidney development: principles, progress, and projections. Cold Spring Harb. Perspect. Biol. 2012, 4. pii: a008300.
41. Luyckx V.A., Brenner B.M. Low birth weight, nephron number, and kidney disease. Kidney Int. Suppl. 2005, S68-S77.
42. MacKay K., Striker L.J., Pinkert C.A., Brinster R.L., Striker G.E. Glomerulosclerosis and renal cysts in mice transgenic for the early region of SV40. Kidney Int. 1987, 32:827-837.
43. Marrable A.W. The counting of cells and nuclei in microtome sections. Q.J. Microsc. Sci. 1962, s3:331-347.
44. Mason J.M., Morrison D.J., Basson M.A., Licht J.D. Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 2006, 16:45-54.
45. Michos O., Cebrian C., Hyink D., Grieshammer U., Williams L., D'Agati V., Licht J.D., Martin G.R., Costantini F. Kidney development in the absence of Gdnf and Spry1 requires Fgf10. PLoS Genet. 2010, 6:e1000809.
46. Mitamura T., Higashiyama S., Taniguchi N., Klagsbrun M., Mekada E. Diphtheria toxin binds to the epidermal growth factor (EGF)-like domain of human heparin-binding EGF-like growth factor/diphtheria toxin receptor and inhibits specifically its mitogenic activity. J.Biol. Chem. 1995, 270:1015-1019.
47. Moore M.W., Klein R.D., Fariñas I., Sauer H., Armanini M., Phillips H., Reichardt L.F., Ryan A.M., Carver-Moore K., Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature 1996, 382:76-79.
48. Moritz K.M., Singh R.R., Probyn M.E., Denton K.M. Developmental programming of a reduced nephron endowment: more than just a baby's birth weight. Am. J. Physiol. Renal Physiol. 2009, 296:F1-F9.
49. Mugford J.W., Sipilä P., McMahon J.A., McMahon A.P. Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev. Biol. 2008, 324:88-98.
50. Mugford J.W., Yu J., Kobayashi A., McMahon A.P. High-resolution gene expression analysis of the developing mouse kidney defines novel cellular compartments within the nephron progenitor population. Dev. Biol. 2009, 333:312-323.
51. Nakamura E., Nguyen M.T., Mackem S. Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreER(T) to assay temporal activity windows along the proximodistal limb skeleton. Dev. Dyn. 2006, 235:2603-2612.
52. Ohuchi H., Hori Y., Yamasaki M., Harada H., Sekine K., Kato S., Itoh N. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem. Biophys. Res. Commun. 2000, 277:643-649.
53. Pachnis V., Mankoo B., Costantini F. Expression of the c-ret proto-oncogene during mouse embryogenesis. Development 1993, 119:1005-1017.
54. Pichel J.G., Shen L., Sheng H.Z., Granholm A.C., Drago J., Grinberg A., Lee E.J., Huang S.P., Saarma M., Hoffer B.J., et al. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996, 382:73-76.
55. Rumballe B.A., Georgas K.M., Combes A.N., Ju A.L., Gilbert T., Little M.H. Nephron formation adopts a novel spatial topology at cessation of nephrogenesis. Dev. Biol. 2011, 360:110-122.
56. Sánchez M.P., Silos-Santiago I., Frisén J., He B., Lira S.A., Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 1996, 382:70-73.
57. Saxén L. Organogenesis of the Kidney 1987, Cambridge University Press, Cambridge/New York.
58. Schreuder M.F. Safety in glomerular numbers. Pediatr. Nephrol. 2012, 27:1881-1887.
59. Schuchardt A., D'Agati V., Larsson-Blomberg L., Costantini F., Pachnis V. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 1994, 367:380-383.
60. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
61. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
62. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
63. Stanger B.Z., Tanaka A.J., Melton D.A. Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver. Nature 2007, 445:886-891.
64. Treanor J.J., Goodman L., de Sauvage F., Stone D.M., Poulsen K.T., Beck C.D., Gray C., Armanini M.P., Pollock R.A., Hefti F., et al. Characterization of a multicomponent receptor for GDNF. Nature 1996, 382:80-83.
65. Vega Q.C., Worby C.A., Lechner M.S., Dixon J.E., Dressler G.R. Glial cell line-derived neurotrophic factor activates the receptor tyrosine kinase RET and promotes kidney morphogenesis. Proc. Natl. Acad. Sci. USA 1996, 93:10657-10661.
66. Vogetseder A., Karadeniz A., Kaissling B., Le Hir M. Tubular cell proliferation in the healthy rat kidney. Histochem. Cell Biol. 2005, 124:97-104.
67. Yamaizumi M., Mekada E., Uchida T., Okada Y. One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell. Cell 1978, 15:245-250.
68. Zhao H., Kegg H., Grady S., Truong H.T., Robinson M.L., Baum M., Bates C.M. Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev. Biol. 2004, 276:403-415.