Skip to main content
Top
Published in: Pediatric Nephrology 2/2017

01-02-2017 | Review

Pronephric tubule formation in zebrafish: morphogenesis and migration

Authors: Richard W. Naylor, Alan J. Davidson

Published in: Pediatric Nephrology | Issue 2/2017

Login to get access

Abstract

The nephron is the functional subunit of the vertebrate kidney and plays important osmoregulatory and excretory roles during embryonic development and in adulthood. Despite its central role in kidney function, surprisingly little is known about the molecular and cellular processes that control nephrogenesis. The zebrafish pronephric kidney, comprising two nephrons, provides a visually accessible and genetically tractable model system for a better understanding of nephron formation. Using this system, various developmental processes, including the commitment of mesoderm to a kidney fate, renal tubule proliferation, and migration, can be studied during nephrogenesis. Here, we discuss some of these processes in zebrafish with a focus on the pathways that influence renal tubule cell morphogenesis.
Literature
1.
go back to reference Wingert RA, Davidson AJ (2008) The zebrafish pronephros: a model to study nephron segmentation. Kidney Int 73:1120–1127CrossRefPubMed Wingert RA, Davidson AJ (2008) The zebrafish pronephros: a model to study nephron segmentation. Kidney Int 73:1120–1127CrossRefPubMed
2.
go back to reference Gerlach GF, Wingert RA (2013) Kidney organogenesis in the zebrafish: insights into vertebrate nephrogenesis and regeneration. Wiley Interdiscip Rev Dev Biol 2:559–585CrossRefPubMed Gerlach GF, Wingert RA (2013) Kidney organogenesis in the zebrafish: insights into vertebrate nephrogenesis and regeneration. Wiley Interdiscip Rev Dev Biol 2:559–585CrossRefPubMed
3.
go back to reference Wingert RA, Selleck R, Yu J, Song HD, Chen Z, Song A, Zhou Y, Thisse B, Thisse C, McMahon AP, Davidson AJ (2007) The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet 3:1922–1938CrossRefPubMed Wingert RA, Selleck R, Yu J, Song HD, Chen Z, Song A, Zhou Y, Thisse B, Thisse C, McMahon AP, Davidson AJ (2007) The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet 3:1922–1938CrossRefPubMed
4.
go back to reference Mudumana SP, Hentschel D, Liu Y, Vasilyev A, Drummond IA (2008) odd skipped related1 reveals a novel role for endoderm in regulating kidney versus vascular cell fate. Development 135:3355–3367CrossRefPubMedPubMedCentral Mudumana SP, Hentschel D, Liu Y, Vasilyev A, Drummond IA (2008) odd skipped related1 reveals a novel role for endoderm in regulating kidney versus vascular cell fate. Development 135:3355–3367CrossRefPubMedPubMedCentral
5.
go back to reference Pfeffer PL, Gerster T, Lun K, Brand M, Busslinger M (1998) Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development 125:3063–3074PubMed Pfeffer PL, Gerster T, Lun K, Brand M, Busslinger M (1998) Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development 125:3063–3074PubMed
7.
go back to reference Naylor RW, Przepiorski A, Ren Q, Yu J, Davidson AJ (2013) HNF1β is essential for nephron segmentation during nephrogenesis. J Am Soc Nephrol 24:77–87CrossRefPubMed Naylor RW, Przepiorski A, Ren Q, Yu J, Davidson AJ (2013) HNF1β is essential for nephron segmentation during nephrogenesis. J Am Soc Nephrol 24:77–87CrossRefPubMed
8.
go back to reference Zhou X, Vize PD (2004) Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev Biol 271:322–338CrossRefPubMed Zhou X, Vize PD (2004) Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev Biol 271:322–338CrossRefPubMed
9.
go back to reference Raciti D, Reggiani L, Geffers L, Jiang Q, Bacchion F, Subrizi AE, Clements D, Tindal C, Davidson DR, Kaissling B, Brandli AW (2008) Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biol 9:R84CrossRefPubMedPubMedCentral Raciti D, Reggiani L, Geffers L, Jiang Q, Bacchion F, Subrizi AE, Clements D, Tindal C, Davidson DR, Kaissling B, Brandli AW (2008) Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biol 9:R84CrossRefPubMedPubMedCentral
10.
go back to reference Majumdar A, Lun K, Brand M, Drummond IA (2000) Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia. Development 127:2089–2098PubMed Majumdar A, Lun K, Brand M, Drummond IA (2000) Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia. Development 127:2089–2098PubMed
11.
go back to reference Perner B, Englert C, Bollig F (2007) The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev Biol 309:87–96CrossRefPubMed Perner B, Englert C, Bollig F (2007) The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev Biol 309:87–96CrossRefPubMed
12.
go back to reference Tomar R, Mudumana SP, Pathak N, Hukriede NA, Drummond IA (2014) osr1 is required for podocyte development downstream of wt1a. J Am Soc Nephrol 25:2539–2545CrossRefPubMedPubMedCentral Tomar R, Mudumana SP, Pathak N, Hukriede NA, Drummond IA (2014) osr1 is required for podocyte development downstream of wt1a. J Am Soc Nephrol 25:2539–2545CrossRefPubMedPubMedCentral
13.
go back to reference Gerlach GF, Wingert RA (2014) Zebrafish pronephros tubulogenesis and epithelial identity maintenance are reliant on the polarity proteins Prkc iota and zeta. Dev Biol 396:183–200CrossRefPubMedPubMedCentral Gerlach GF, Wingert RA (2014) Zebrafish pronephros tubulogenesis and epithelial identity maintenance are reliant on the polarity proteins Prkc iota and zeta. Dev Biol 396:183–200CrossRefPubMedPubMedCentral
14.
go back to reference Miceli R, Kroeger P, Wingert R (2014) Molecular mechanisms of podocyte development revealed by zebrafish kidney research. Cell Dev Biol 3 Miceli R, Kroeger P, Wingert R (2014) Molecular mechanisms of podocyte development revealed by zebrafish kidney research. Cell Dev Biol 3
15.
go back to reference O'Brien LL, Grimaldi M, Kostun Z, Wingert RA, Selleck R, Davidson AJ (2011) Wt1a, Foxc1a, and the Notch mediator Rbpj physically interact and regulate the formation of podocytes in zebrafish. Dev Biol 358:318–330CrossRefPubMedPubMedCentral O'Brien LL, Grimaldi M, Kostun Z, Wingert RA, Selleck R, Davidson AJ (2011) Wt1a, Foxc1a, and the Notch mediator Rbpj physically interact and regulate the formation of podocytes in zebrafish. Dev Biol 358:318–330CrossRefPubMedPubMedCentral
16.
go back to reference Cheng CN, Wingert RA (2015) Nephron proximal tubule patterning and corpuscles of Stannius formation are regulated by the sim1a transcription factor and retinoic acid in zebrafish. Dev Biol 399:100–116CrossRefPubMed Cheng CN, Wingert RA (2015) Nephron proximal tubule patterning and corpuscles of Stannius formation are regulated by the sim1a transcription factor and retinoic acid in zebrafish. Dev Biol 399:100–116CrossRefPubMed
17.
go back to reference Li Y, Cheng CN, Verdun VA, Wingert RA (2014) Zebrafish nephrogenesis is regulated by interactions between retinoic acid, mecom, and Notch signaling. Dev Biol 386:111–122CrossRefPubMed Li Y, Cheng CN, Verdun VA, Wingert RA (2014) Zebrafish nephrogenesis is regulated by interactions between retinoic acid, mecom, and Notch signaling. Dev Biol 386:111–122CrossRefPubMed
20.
go back to reference Vize PD, Jones EA, Pfister R (1995) Development of the Xenopus pronephric system. Dev Biol 171:531–540CrossRefPubMed Vize PD, Jones EA, Pfister R (1995) Development of the Xenopus pronephric system. Dev Biol 171:531–540CrossRefPubMed
21.
go back to reference Zhang J, Yuan S, Vasilyev A, Amin Arnaout M (2015) The transcriptional coactivator Taz regulates proximodistal patterning of the pronephric tubule in zebrafish. Mech Dev 138(Pt 3):328–325CrossRefPubMed Zhang J, Yuan S, Vasilyev A, Amin Arnaout M (2015) The transcriptional coactivator Taz regulates proximodistal patterning of the pronephric tubule in zebrafish. Mech Dev 138(Pt 3):328–325CrossRefPubMed
22.
go back to reference Wingert RA, Davidson AJ (2011) Zebrafish nephrogenesis involves dynamic spatiotemporal expression changes in renal progenitors and essential signals from retinoic acid and irx3b. Dev Dyn 240:2011–2027CrossRefPubMed Wingert RA, Davidson AJ (2011) Zebrafish nephrogenesis involves dynamic spatiotemporal expression changes in renal progenitors and essential signals from retinoic acid and irx3b. Dev Dyn 240:2011–2027CrossRefPubMed
23.
go back to reference De Groh ED, Swanhart LM, Cosentino CC, Jackson RL, Dai W, Kitchens CA, Day BW, Smithgall TE, Hukriede NA (2010) Inhibition of histone deacetylase expands the renal progenitor cell population. J Am Soc Nephrol 21:794–802 De Groh ED, Swanhart LM, Cosentino CC, Jackson RL, Dai W, Kitchens CA, Day BW, Smithgall TE, Hukriede NA (2010) Inhibition of histone deacetylase expands the renal progenitor cell population. J Am Soc Nephrol 21:794–802
24.
go back to reference Lienkamp SS, Liu K, Karner CM, Carroll TJ, Ronneberger O, Wallingford JB, Walz G (2012) Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat Genet 44:1382–1387CrossRefPubMedPubMedCentral Lienkamp SS, Liu K, Karner CM, Carroll TJ, Ronneberger O, Wallingford JB, Walz G (2012) Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat Genet 44:1382–1387CrossRefPubMedPubMedCentral
25.
go back to reference Lienkamp S, Ganner A, Boehlke C, Schmidt T, Arnold SJ, Schafer T, Romaker D, Schuler J, Hoff S, Powelske C, Eifler A, Kronig C, Bullerkotte A, Nitschke R, Kuehn EW, Kim E, Burkhardt H, Brox T, Ronneberger O, Gloy J, Walz G (2010) Inversin relays Frizzled-8 signals to promote proximal pronephros development. Proc Natl Acad Sci U S A 107:20388–20393CrossRefPubMedPubMedCentral Lienkamp S, Ganner A, Boehlke C, Schmidt T, Arnold SJ, Schafer T, Romaker D, Schuler J, Hoff S, Powelske C, Eifler A, Kronig C, Bullerkotte A, Nitschke R, Kuehn EW, Kim E, Burkhardt H, Brox T, Ronneberger O, Gloy J, Walz G (2010) Inversin relays Frizzled-8 signals to promote proximal pronephros development. Proc Natl Acad Sci U S A 107:20388–20393CrossRefPubMedPubMedCentral
26.
27.
go back to reference Van Itallie CM, Anderson JM (2014) Architecture of tight junctions and principles of molecular composition. Semin Cell Dev Biol 36:157–165CrossRefPubMed Van Itallie CM, Anderson JM (2014) Architecture of tight junctions and principles of molecular composition. Semin Cell Dev Biol 36:157–165CrossRefPubMed
28.
go back to reference Li WY, Huey CL, Yu AS (2004) Expression of claudin-7 and -8 along the mouse nephron. Am J Physiol Ren Physiol 286:F1063–F1071CrossRef Li WY, Huey CL, Yu AS (2004) Expression of claudin-7 and -8 along the mouse nephron. Am J Physiol Ren Physiol 286:F1063–F1071CrossRef
29.
go back to reference Yu AS, Enck AH, Lencer WI, Schneeberger EE (2003) Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 278:17350–17359CrossRefPubMed Yu AS, Enck AH, Lencer WI, Schneeberger EE (2003) Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 278:17350–17359CrossRefPubMed
30.
go back to reference Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S (2002) Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875–886PubMed Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S (2002) Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875–886PubMed
31.
go back to reference Thisse B, Pflumio S, Fürthauer M, Loppin B, Heyer V, Degrave A, Woehl R, Lux A, Steffan T, Charbonnier XQ, Thisse C (2001) Expression of the zebrafish genome during embryogenesis. ZFIN Direct Data Submission (http://zfin.org) Thisse B, Pflumio S, Fürthauer M, Loppin B, Heyer V, Degrave A, Woehl R, Lux A, Steffan T, Charbonnier XQ, Thisse C (2001) Expression of the zebrafish genome during embryogenesis. ZFIN Direct Data Submission (http://​zfin.​org)
32.
go back to reference Thisse B, Thisse C (2004) Fast release clones: a high throughput expression analysis. ZFIN Direct Data Submission (http://zfin.org) Thisse B, Thisse C (2004) Fast release clones: a high throughput expression analysis. ZFIN Direct Data Submission (http://​zfin.​org)
33.
go back to reference Thisse C, Thisse B (2005) High throughput expression analysis of ZF-models consortium clones. ZFIN Direct Data Submission (http://zfin.org) Thisse C, Thisse B (2005) High throughput expression analysis of ZF-models consortium clones. ZFIN Direct Data Submission (http://​zfin.​org)
34.
go back to reference Rauch GJ, Lyons DA, Middendorf I, Friedlander B, Arana N, Reyes T, Talbot WS (2003) Submission and curation of gene expression data. ZFIN Direct Data Submission (http://zfin.org) Rauch GJ, Lyons DA, Middendorf I, Friedlander B, Arana N, Reyes T, Talbot WS (2003) Submission and curation of gene expression data. ZFIN Direct Data Submission (http://​zfin.​org)
35.
go back to reference McKee R, Gerlach GF, Jou J, Cheng CN, Wingert RA (2014) Temporal and spatial expression of tight junction genes during zebrafish pronephros development. Gene Expr Patterns 16:104–113CrossRefPubMedPubMedCentral McKee R, Gerlach GF, Jou J, Cheng CN, Wingert RA (2014) Temporal and spatial expression of tight junction genes during zebrafish pronephros development. Gene Expr Patterns 16:104–113CrossRefPubMedPubMedCentral
36.
go back to reference Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, Furuse K, Sasaki H, Fujimura A, Imai M, Kusano E, Tsukita S, Furuse M (2010) Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci U S A 107:8011–8016CrossRefPubMedPubMedCentral Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, Furuse K, Sasaki H, Fujimura A, Imai M, Kusano E, Tsukita S, Furuse M (2010) Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci U S A 107:8011–8016CrossRefPubMedPubMedCentral
37.
go back to reference Gonzalez-Mariscal L, Namorado MC, Martin D, Luna J, Alarcon L, Islas S, Valencia L, Muriel P, Ponce L, Reyes JL (2000) Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int 57:2386–2402CrossRefPubMed Gonzalez-Mariscal L, Namorado MC, Martin D, Luna J, Alarcon L, Islas S, Valencia L, Muriel P, Ponce L, Reyes JL (2000) Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int 57:2386–2402CrossRefPubMed
38.
go back to reference Siliciano JD, Goodenough DA (1988) Localization of the tight junction protein, ZO-1, is modulated by extracellular calcium and cell-cell contact in Madin-Darby canine kidney epithelial cells. J Cell Biol 107:2389–2399CrossRefPubMed Siliciano JD, Goodenough DA (1988) Localization of the tight junction protein, ZO-1, is modulated by extracellular calcium and cell-cell contact in Madin-Darby canine kidney epithelial cells. J Cell Biol 107:2389–2399CrossRefPubMed
40.
go back to reference Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M (2010) Alpha-catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12:533–542CrossRefPubMed Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M (2010) Alpha-catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12:533–542CrossRefPubMed
41.
go back to reference Horsfield J, Ramachandran A, Reuter K, LaVallie E, Collins-Racie L, Crosier K, Crosier P (2002) Cadherin-17 is required to maintain pronephric duct integrity during zebrafish development. Mech Dev 115:15–26CrossRefPubMed Horsfield J, Ramachandran A, Reuter K, LaVallie E, Collins-Racie L, Crosier K, Crosier P (2002) Cadherin-17 is required to maintain pronephric duct integrity during zebrafish development. Mech Dev 115:15–26CrossRefPubMed
42.
go back to reference Vestweber D, Kemler R, Ekblom P (1985) Cell-adhesion molecule uvomorulin during kidney development. Dev Biol 112:213–221CrossRefPubMed Vestweber D, Kemler R, Ekblom P (1985) Cell-adhesion molecule uvomorulin during kidney development. Dev Biol 112:213–221CrossRefPubMed
45.
go back to reference Itano N, Okamoto S, Zhang D, Lipton SA, Ruoslahti E (2003) Cell spreading controls endoplasmic and nuclear calcium: a physical gene regulation pathway from the cell surface to the nucleus. Proc Natl Acad Sci U S A 100:5181–5186CrossRefPubMedPubMedCentral Itano N, Okamoto S, Zhang D, Lipton SA, Ruoslahti E (2003) Cell spreading controls endoplasmic and nuclear calcium: a physical gene regulation pathway from the cell surface to the nucleus. Proc Natl Acad Sci U S A 100:5181–5186CrossRefPubMedPubMedCentral
46.
go back to reference Mammoto A, Connor KM, Mammoto T, Yung CW, Huh D, Aderman CM, Mostoslavsky G, Smith LE, Ingber DE (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457:1103–1108CrossRefPubMedPubMedCentral Mammoto A, Connor KM, Mammoto T, Yung CW, Huh D, Aderman CM, Mostoslavsky G, Smith LE, Ingber DE (2009) A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457:1103–1108CrossRefPubMedPubMedCentral
47.
go back to reference Quaggin SE, Kreidberg JA (2008) Development of the renal glomerulus: good neighbors and good fences. Development 135:609–620CrossRefPubMed Quaggin SE, Kreidberg JA (2008) Development of the renal glomerulus: good neighbors and good fences. Development 135:609–620CrossRefPubMed
48.
go back to reference Schell C, Wanner N, Huber TB (2014) Glomerular development—shaping the multi-cellular filtration unit. Semin Cell Dev Biol 36:39–49CrossRefPubMed Schell C, Wanner N, Huber TB (2014) Glomerular development—shaping the multi-cellular filtration unit. Semin Cell Dev Biol 36:39–49CrossRefPubMed
49.
go back to reference Serluca FC, Drummond IA, Fishman MC (2002) Endothelial signaling in kidney morphogenesis: a role for hemodynamic forces. Curr Biol 12:492–497CrossRefPubMed Serluca FC, Drummond IA, Fishman MC (2002) Endothelial signaling in kidney morphogenesis: a role for hemodynamic forces. Curr Biol 12:492–497CrossRefPubMed
50.
go back to reference Grote D, Souabni A, Busslinger M, Bouchard M (2006) Pax 2/8-regulated Gata 3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney. Development 133:53–61CrossRefPubMed Grote D, Souabni A, Busslinger M, Bouchard M (2006) Pax 2/8-regulated Gata 3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney. Development 133:53–61CrossRefPubMed
51.
go back to reference Stewart K, Bouchard M (2014) Coordinated cell behaviours in early urogenital system morphogenesis. Semin Cell Dev Biol 36:13–20CrossRefPubMed Stewart K, Bouchard M (2014) Coordinated cell behaviours in early urogenital system morphogenesis. Semin Cell Dev Biol 36:13–20CrossRefPubMed
52.
go back to reference Pyati UJ, Webb AE, Kimelman D (2005) Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132:2333–2343CrossRefPubMed Pyati UJ, Webb AE, Kimelman D (2005) Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132:2333–2343CrossRefPubMed
53.
go back to reference Slanchev K, Putz M, Schmitt A, Kramer-Zucker A, Walz G (2011) Nephrocystin-4 is required for pronephric duct-dependent cloaca formation in zebrafish. Hum Mol Genet 20:3119–3128CrossRefPubMed Slanchev K, Putz M, Schmitt A, Kramer-Zucker A, Walz G (2011) Nephrocystin-4 is required for pronephric duct-dependent cloaca formation in zebrafish. Hum Mol Genet 20:3119–3128CrossRefPubMed
54.
go back to reference Burckle C, Gaude HM, Vesque C, Silbermann F, Salomon R, Jeanpierre C, Antignac C, Saunier S, Schneider-Maunoury S (2011) Control of the Wnt pathways by nephrocystin-4 is required for morphogenesis of the zebrafish pronephros. Hum Mol Genet 20:2611–2627CrossRefPubMed Burckle C, Gaude HM, Vesque C, Silbermann F, Salomon R, Jeanpierre C, Antignac C, Saunier S, Schneider-Maunoury S (2011) Control of the Wnt pathways by nephrocystin-4 is required for morphogenesis of the zebrafish pronephros. Hum Mol Genet 20:2611–2627CrossRefPubMed
55.
go back to reference Bastock R, Strutt H, Strutt D (2003) Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130:3007–3014CrossRefPubMed Bastock R, Strutt H, Strutt D (2003) Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130:3007–3014CrossRefPubMed
56.
go back to reference Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Kronig C, Schermer B, Benzing T, Cabello OA, Jenny A, Mlodzik M, Polok B, Driever W, Obara T, Walz G (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37:537–543CrossRefPubMedPubMedCentral Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Kronig C, Schermer B, Benzing T, Cabello OA, Jenny A, Mlodzik M, Polok B, Driever W, Obara T, Walz G (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37:537–543CrossRefPubMedPubMedCentral
57.
go back to reference Baranowska Korberg I, Hofmeister W, Markljung E, Cao J, Nilsson D, Ludwig M, Draaken M, Holmdahl G, Barker G, Reutter H, Vukojevic V, Clementson Kockum C, Lundin J, Lindstrand A, Nordenskjold A (2015) WNT3 involvement in human bladder exstrophy and cloaca development in zebrafish. Hum Mol Genet 24:5069–5078CrossRefPubMed Baranowska Korberg I, Hofmeister W, Markljung E, Cao J, Nilsson D, Ludwig M, Draaken M, Holmdahl G, Barker G, Reutter H, Vukojevic V, Clementson Kockum C, Lundin J, Lindstrand A, Nordenskjold A (2015) WNT3 involvement in human bladder exstrophy and cloaca development in zebrafish. Hum Mol Genet 24:5069–5078CrossRefPubMed
58.
go back to reference Joberty G, Petersen C, Gao L, Macara IG (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531–539CrossRefPubMed Joberty G, Petersen C, Gao L, Macara IG (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531–539CrossRefPubMed
59.
go back to reference Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T (2000) A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2:540–547CrossRefPubMed Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T (2000) A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2:540–547CrossRefPubMed
60.
go back to reference Tabuse Y, Izumi Y, Piano F, Kemphues KJ, Miwa J, Ohno S (1998) Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125:3607–3614PubMed Tabuse Y, Izumi Y, Piano F, Kemphues KJ, Miwa J, Ohno S (1998) Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125:3607–3614PubMed
61.
go back to reference Vasilyev A, Liu Y, Mudumana S, Mangos S, Lam PY, Majumdar A, Zhao J, Poon KL, Kondrychyn I, Korzh V, Drummond IA (2009) Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol 7:e9CrossRefPubMed Vasilyev A, Liu Y, Mudumana S, Mangos S, Lam PY, Majumdar A, Zhao J, Poon KL, Kondrychyn I, Korzh V, Drummond IA (2009) Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol 7:e9CrossRefPubMed
62.
go back to reference Vasilyev A, Liu Y, Hellman N, Pathak N, Drummond IA (2012) Mechanical stretch and PI3K signaling link cell migration and proliferation to coordinate epithelial tubule morphogenesis in the zebrafish pronephros. PLoS One 7:e39992CrossRefPubMedPubMedCentral Vasilyev A, Liu Y, Hellman N, Pathak N, Drummond IA (2012) Mechanical stretch and PI3K signaling link cell migration and proliferation to coordinate epithelial tubule morphogenesis in the zebrafish pronephros. PLoS One 7:e39992CrossRefPubMedPubMedCentral
63.
go back to reference Wang JH, Thampatty BP (2006) An introductory review of cell mechanobiology. Biomech Model Mechanobiol 5:1–16CrossRefPubMed Wang JH, Thampatty BP (2006) An introductory review of cell mechanobiology. Biomech Model Mechanobiol 5:1–16CrossRefPubMed
65.
Metadata
Title
Pronephric tubule formation in zebrafish: morphogenesis and migration
Authors
Richard W. Naylor
Alan J. Davidson
Publication date
01-02-2017
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Nephrology / Issue 2/2017
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-016-3353-1

Other articles of this Issue 2/2017

Pediatric Nephrology 2/2017 Go to the issue