Skip to main content
Erschienen in: Pediatric Nephrology 9/2011

01.09.2011 | Review

The role of proton transporters in epithelial Wnt signaling pathways

verfasst von: Tobias Hermle, Astrid G. Petzoldt, Matias Simons

Erschienen in: Pediatric Nephrology | Ausgabe 9/2011

Einloggen, um Zugang zu erhalten

Abstract

The planar cell polarity (PCP) pathway polarizes epithelia in the plane of a tissue. It regulates form and function of tissues and manifests itself by the polarized formation of cellular appendages such as epidermal hairs and cilia. Defects in the pathway are often associated with organ malformation and disease. In the kidney, the molecular events leading to cyst formation in polycystic kidney disease involve the PCP pathway. PCP is, however, best understood in Drosophila where genetic screens have identified a group of PCP core proteins including the Wnt receptor Frizzled (Fz), Dishevelled (Dsh), and Flamingo (Fmi). These proteins can localize to opposite parts of the plasma membrane in response to a poorly understood symmetry breaking event. Recent evidence suggests that proton transporters may play a role in regulating the asymmetric localization of PCP core proteins. Several papers have reported that the (pro)renin receptor, which is an associated subunit of the proton pumping V-ATPase, is required for PCP, but also for canonical Wnt signaling. Here, we discuss the implications of these findings for diverse developmental settings.
Literatur
1.
Zurück zum Zitat Simons M, Mlodzik M (2008) Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42:518–540CrossRef Simons M, Mlodzik M (2008) Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42:518–540CrossRef
3.
Zurück zum Zitat Gubb D, Garcia-Bellido A (1982) A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J Embryol Exp Morphol 68:37–57PubMed Gubb D, Garcia-Bellido A (1982) A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J Embryol Exp Morphol 68:37–57PubMed
4.
Zurück zum Zitat Vinson CR, Adler PN (1987) Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329:549–551PubMedCrossRef Vinson CR, Adler PN (1987) Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329:549–551PubMedCrossRef
5.
Zurück zum Zitat Seifert JR, Mlodzik M (2007) Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet 8:126–138PubMedCrossRef Seifert JR, Mlodzik M (2007) Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet 8:126–138PubMedCrossRef
7.
Zurück zum Zitat Song H, Hu J, Chen W, Elliott G, Andre P, Gao B, Yang Y (2010) Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466:378–382PubMedPubMedCentralCrossRef Song H, Hu J, Chen W, Elliott G, Andre P, Gao B, Yang Y (2010) Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466:378–382PubMedPubMedCentralCrossRef
8.
Zurück zum Zitat Wang Y, Nathans J (2007) Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134:647–658PubMedCrossRef Wang Y, Nathans J (2007) Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134:647–658PubMedCrossRef
9.
Zurück zum Zitat Simons M, Walz G (2006) Polycystic kidney disease: cell division without a c(l)ue? Kidney Int 70:854–864PubMedCrossRef Simons M, Walz G (2006) Polycystic kidney disease: cell division without a c(l)ue? Kidney Int 70:854–864PubMedCrossRef
10.
Zurück zum Zitat Fischer E, Legue E, Doyen A, Nato F, Nicolas JF, Torres V, Yaniv M, Pontoglio M (2006) Defective planar cell polarity in polycystic kidney disease. Nat Genet 38:21–23PubMedCrossRef Fischer E, Legue E, Doyen A, Nato F, Nicolas JF, Torres V, Yaniv M, Pontoglio M (2006) Defective planar cell polarity in polycystic kidney disease. Nat Genet 38:21–23PubMedCrossRef
12.
Zurück zum Zitat Veeman MT, Axelrod JD, Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5:367–377PubMedCrossRef Veeman MT, Axelrod JD, Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5:367–377PubMedCrossRef
13.
Zurück zum Zitat Wolff T, Rubin GM (1998) Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125:1149–1159PubMedCrossRef Wolff T, Rubin GM (1998) Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125:1149–1159PubMedCrossRef
14.
Zurück zum Zitat Jenny A, Darken RS, Wilson PA, Mlodzik M (2003) Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J 22:4409–4420PubMedPubMedCentralCrossRef Jenny A, Darken RS, Wilson PA, Mlodzik M (2003) Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J 22:4409–4420PubMedPubMedCentralCrossRef
15.
Zurück zum Zitat Tree DR, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD (2002) Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109:371–381PubMedCrossRef Tree DR, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD (2002) Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109:371–381PubMedCrossRef
16.
Zurück zum Zitat Wu J, Mlodzik M (2008) The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev Cell 15:462–469PubMedPubMedCentralCrossRef Wu J, Mlodzik M (2008) The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev Cell 15:462–469PubMedPubMedCentralCrossRef
17.
Zurück zum Zitat Singh J, Yanfeng WA, Grumolato L, Aaronson SA, Mlodzik M (2010) Abelson family kinases regulate Frizzled planar cell polarity signaling via Dsh phosphorylation. Genes Dev 24:2157–2168PubMedPubMedCentralCrossRef Singh J, Yanfeng WA, Grumolato L, Aaronson SA, Mlodzik M (2010) Abelson family kinases regulate Frizzled planar cell polarity signaling via Dsh phosphorylation. Genes Dev 24:2157–2168PubMedPubMedCentralCrossRef
18.
Zurück zum Zitat Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, Koshida I, Suzuki K, Yamada G, Schwabe GC, Mundlos S, Shibuya H, Takada S, Minami Y (2003) The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8:645–654PubMedCrossRef Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, Koshida I, Suzuki K, Yamada G, Schwabe GC, Mundlos S, Shibuya H, Takada S, Minami Y (2003) The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8:645–654PubMedCrossRef
19.
20.
Zurück zum Zitat Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, Niehrs C (2007) Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316:1619–1622PubMedCrossRef Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, Niehrs C (2007) Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316:1619–1622PubMedCrossRef
21.
Zurück zum Zitat Simons M, Gault WJ, Gotthardt D, Rohatgi R, Klein TJ, Shao Y, Lee HJ, Wu AL, Fang Y, Satlin LM, Dow JT, Chen J, Zheng J, Boutros M, Mlodzik M (2009) Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat Cell Biol 11:286–294PubMedPubMedCentralCrossRef Simons M, Gault WJ, Gotthardt D, Rohatgi R, Klein TJ, Shao Y, Lee HJ, Wu AL, Fang Y, Satlin LM, Dow JT, Chen J, Zheng J, Boutros M, Mlodzik M (2009) Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat Cell Biol 11:286–294PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C (2010) Requirement of prorenin receptor and vacuolar H+−ATPase-mediated acidification for Wnt signaling. Science 327:459–463PubMedCrossRef Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C (2010) Requirement of prorenin receptor and vacuolar H+−ATPase-mediated acidification for Wnt signaling. Science 327:459–463PubMedCrossRef
23.
Zurück zum Zitat Buechling T, Bartscherer K, Ohkawara B, Chaudhary V, Spirohn K, Niehrs C, Boutros M (2010) Wnt/Frizzled signaling requires dPRR, the Drosophila homolog of the prorenin receptor. Curr Biol 20:1263–1268PubMedCrossRef Buechling T, Bartscherer K, Ohkawara B, Chaudhary V, Spirohn K, Niehrs C, Boutros M (2010) Wnt/Frizzled signaling requires dPRR, the Drosophila homolog of the prorenin receptor. Curr Biol 20:1263–1268PubMedCrossRef
24.
Zurück zum Zitat Hermle T, Saltukoglu D, Grunewald J, Walz G, Simons M (2010) Regulation of Frizzled-dependent planar polarity signaling by a V-ATPase subunit. Curr Biol 20:1269–1276PubMedCrossRef Hermle T, Saltukoglu D, Grunewald J, Walz G, Simons M (2010) Regulation of Frizzled-dependent planar polarity signaling by a V-ATPase subunit. Curr Biol 20:1269–1276PubMedCrossRef
25.
Zurück zum Zitat Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V (2006) V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8:124–136PubMedCrossRef Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V (2006) V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8:124–136PubMedCrossRef
26.
Zurück zum Zitat Kinouchi K, Ichihara A, Sano M, Sun-Wada GH, Wada Y, Kurauchi-Mito A, Bokuda K, Narita T, Oshima Y, Sakoda M, Tamai Y, Sato H, Fukuda K, Itoh H (2010) The (Pro)renin receptor/ATP6AP2 is essential for vacuolar H+−ATPase assembly in murine cardiomyocytes. Circ Res 107:30–34PubMedCrossRef Kinouchi K, Ichihara A, Sano M, Sun-Wada GH, Wada Y, Kurauchi-Mito A, Bokuda K, Narita T, Oshima Y, Sakoda M, Tamai Y, Sato H, Fukuda K, Itoh H (2010) The (Pro)renin receptor/ATP6AP2 is essential for vacuolar H+−ATPase assembly in murine cardiomyocytes. Circ Res 107:30–34PubMedCrossRef
27.
Zurück zum Zitat Nguyen G, Muller DN (2010) The biology of the (pro)renin receptor. J Am Soc Nephrol 21:18–23PubMedCrossRef Nguyen G, Muller DN (2010) The biology of the (pro)renin receptor. J Am Soc Nephrol 21:18–23PubMedCrossRef
28.
Zurück zum Zitat Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD (2002) Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109:1417–1427PubMedPubMedCentralCrossRef Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD (2002) Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109:1417–1427PubMedPubMedCentralCrossRef
29.
Zurück zum Zitat Ramser J, Abidi FE, Burckle CA, Lenski C, Toriello H, Wen G, Lubs HA, Engert S, Stevenson RE, Meindl A, Schwartz CE, Nguyen G (2005) A unique exonic splice enhancer mutation in a family with X-linked mental retardation and epilepsy points to a novel role of the renin receptor. Hum Mol Genet 14:1019–1027PubMedCrossRef Ramser J, Abidi FE, Burckle CA, Lenski C, Toriello H, Wen G, Lubs HA, Engert S, Stevenson RE, Meindl A, Schwartz CE, Nguyen G (2005) A unique exonic splice enhancer mutation in a family with X-linked mental retardation and epilepsy points to a novel role of the renin receptor. Hum Mol Genet 14:1019–1027PubMedCrossRef
30.
Zurück zum Zitat Nguyen G, Contrepas A (2008) Physiology and pharmacology of the (pro)renin receptor. Curr Opin Pharmacol 8:127–132PubMedCrossRef Nguyen G, Contrepas A (2008) Physiology and pharmacology of the (pro)renin receptor. Curr Opin Pharmacol 8:127–132PubMedCrossRef
31.
Zurück zum Zitat Shimada Y, Yonemura S, Ohkura H, Strutt D, Uemura T (2006) Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev Cell 10:209–222PubMedCrossRef Shimada Y, Yonemura S, Ohkura H, Strutt D, Uemura T (2006) Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev Cell 10:209–222PubMedCrossRef
32.
Zurück zum Zitat Yan Y, Denef N, Schupbach T (2009) The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking in Drosophila. Dev Cell 17:387–402PubMedPubMedCentralCrossRef Yan Y, Denef N, Schupbach T (2009) The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking in Drosophila. Dev Cell 17:387–402PubMedPubMedCentralCrossRef
33.
Zurück zum Zitat Vaccari T, Duchi S, Cortese K, Tacchetti C, Bilder D (2010) The vacuolar ATPase is required for physiological as well as pathological activation of the Notch receptor. Development 137:1825–1832PubMedPubMedCentralCrossRef Vaccari T, Duchi S, Cortese K, Tacchetti C, Bilder D (2010) The vacuolar ATPase is required for physiological as well as pathological activation of the Notch receptor. Development 137:1825–1832PubMedPubMedCentralCrossRef
34.
Zurück zum Zitat Niehrs C, Boutros M (2010) Trafficking, acidification, and growth factor signaling. Sci Signal 3:pe26PubMedCrossRef Niehrs C, Boutros M (2010) Trafficking, acidification, and growth factor signaling. Sci Signal 3:pe26PubMedCrossRef
35.
Zurück zum Zitat Mahalingam M, Martinez-Mayorga K, Brown MF, Vogel R (2008) Two protonation switches control rhodopsin activation in membranes. Proc Natl Acad Sci USA 105:17795–17800PubMedCrossRefPubMedCentral Mahalingam M, Martinez-Mayorga K, Brown MF, Vogel R (2008) Two protonation switches control rhodopsin activation in membranes. Proc Natl Acad Sci USA 105:17795–17800PubMedCrossRefPubMedCentral
36.
Zurück zum Zitat Denker S, Huang D, Orlowski J, Furthmayr H, Barber D (2000) Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H+ translocation. Mol Cell 6:1425–1436PubMedCrossRef Denker S, Huang D, Orlowski J, Furthmayr H, Barber D (2000) Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H+ translocation. Mol Cell 6:1425–1436PubMedCrossRef
37.
Zurück zum Zitat Frantz C, Karydis A, Nalbant P, Hahn KM, Barber DL (2007) Positive feedback between Cdc42 activity and H+ efflux by the Na-H exchanger NHE1 for polarity of migrating cells. J Cell Biol 179:403–410PubMedPubMedCentralCrossRef Frantz C, Karydis A, Nalbant P, Hahn KM, Barber DL (2007) Positive feedback between Cdc42 activity and H+ efflux by the Na-H exchanger NHE1 for polarity of migrating cells. J Cell Biol 179:403–410PubMedPubMedCentralCrossRef
38.
Zurück zum Zitat Levin M, Thorlin T, Robinson KR, Nogi T, Mercola M (2002) Asymmetries in H+/K+−ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111:77–89PubMedCrossRef Levin M, Thorlin T, Robinson KR, Nogi T, Mercola M (2002) Asymmetries in H+/K+−ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111:77–89PubMedCrossRef
39.
Zurück zum Zitat Shimeld SM, Levin M (2006) Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Dev Dyn 235:1543–1553PubMedCrossRef Shimeld SM, Levin M (2006) Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Dev Dyn 235:1543–1553PubMedCrossRef
40.
Zurück zum Zitat Duboc V, Rottinger E, Lapraz F, Besnardeau L, Lepage T (2005) Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev Cell 9:147–158PubMedCrossRef Duboc V, Rottinger E, Lapraz F, Besnardeau L, Lepage T (2005) Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev Cell 9:147–158PubMedCrossRef
41.
Zurück zum Zitat Adams DS, Robinson KR, Fukumoto T, Yuan S, Albertson RC, Yelick P, Kuo L, McSweeney M, Levin M (2006) Early, H+−V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133:1657–1671PubMedCrossRef Adams DS, Robinson KR, Fukumoto T, Yuan S, Albertson RC, Yelick P, Kuo L, McSweeney M, Levin M (2006) Early, H+−V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133:1657–1671PubMedCrossRef
Metadaten
Titel
The role of proton transporters in epithelial Wnt signaling pathways
verfasst von
Tobias Hermle
Astrid G. Petzoldt
Matias Simons
Publikationsdatum
01.09.2011
Verlag
Springer Berlin Heidelberg
Erschienen in
Pediatric Nephrology / Ausgabe 9/2011
Print ISSN: 0931-041X
Elektronische ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-011-1823-z

Weitere Artikel der Ausgabe 9/2011

Pediatric Nephrology 9/2011 Zur Ausgabe

Program

Program

Kinder mit anhaltender Sinusitis profitieren häufig von Antibiotika

30.04.2024 Rhinitis und Sinusitis Nachrichten

Persistieren Sinusitisbeschwerden bei Kindern länger als zehn Tage, ist eine Antibiotikatherapie häufig gut wirksam: Ein Therapieversagen ist damit zu über 40% seltener zu beobachten als unter Placebo.

Neuer Typ-1-Diabetes bei Kindern am Wochenende eher übersehen

23.04.2024 Typ-1-Diabetes Nachrichten

Wenn Kinder an Werktagen zum Arzt gehen, werden neu auftretender Typ-1-Diabetes und diabetische Ketoazidosen häufiger erkannt als bei Arztbesuchen an Wochenenden oder Feiertagen.

Neue Studienergebnisse zur Myopiekontrolle mit Atropin

22.04.2024 Fehlsichtigkeit Nachrichten

Augentropfen mit niedrig dosiertem Atropin können helfen, das Fortschreiten einer Kurzsichtigkeit bei Kindern zumindest zu verlangsamen, wie die Ergebnisse einer aktuellen Studie mit verschiedenen Dosierungen zeigen.

Spinale Muskelatrophie: Neugeborenen-Screening lohnt sich

18.04.2024 Spinale Muskelatrophien Nachrichten

Seit 2021 ist die Untersuchung auf spinale Muskelatrophie Teil des Neugeborenen-Screenings in Deutschland. Eine Studie liefert weitere Evidenz für den Nutzen der Maßnahme.

Update Pädiatrie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.