Loss of Lrp2 in zebrafish disrupts pronephric tubular clearance but not forebrain development

Developmental Dynamics

Volumn 240, Issue 6, 2011, Pages 1567-1577

  Kur, Esther ^a   Christa, Anna ^a   Veth, Kerry N ^b   Gajera, Chandresh R ^a   Andrade Navarro, Miguel A ^a   Zhang, Jingjing ^a   Willer, Jason R ^d   Gregg, Ronald G ^e   Abdelilah Seyfried, Salim ^a   Bachmann, Sebastian ^c   Link, Brian A ^b   Hammes, Annette ^a   Willnow, Thomas E ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Forebrain development; LDL receptor related proteins; Megalin; Pronephros

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 2B; MEGALIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; FOREBRAIN; GENE DISRUPTION; GENE SILENCING; GENETIC CONSERVATION; KIDNEY CLEARANCE; KIDNEY TUBULE; LARVAL STAGE; MAMMAL; MOUSE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TELEOST; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KIDNEY TUBULES; LDL-RECEPTOR RELATED PROTEIN 2; METABOLIC CLEARANCE RATE; MODELS, BIOLOGICAL; PHYLOGENY; PROSENCEPHALON; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; ZEBRAFISH;

DANIO RERIO; ERINACEIDAE; MAMMALIA; NEMATODA; TELEOSTEI;

EID: 79955720762     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22624     Document Type: Article

References (33)

1. Abe T, Muto Y, Hosoya N. 1975. Vitamin A transport in chicken plasma: isolation and characterization of retinol-binding protein (RBP), prealbumin (PA), and RBP-PA complex. J Lipid Res 16: 200-210.
2. Adolf B, Chapouton P, Lam CS, Topp S, Tannhauser B, Strahle U, Gotz M, Bally-Cuif L. 2006. Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295: 278-293.
3. Anzenberger U, Bit-Avragim N, Rohr S, Rudolph F, Dehmel B, Willnow TE, Abdelilah-Seyfried S. 2006. Elucidation of megalin/LRP2-dependent endocytic transport processes in the larval zebrafish pronephros. J Cell Sci 119: 2127-2137.
4. Byrd CA, Brunjes PC. 2001. Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105: 793-801.
5. Christensen EI, Birn H. 2001. Megalin and cubilin: synergistic endocytic receptors in renal proximal tubule. Am J Physiol Renal Physiol 280: F562-573.
6. Christensen EI, Birn H. 2002. Megalin and cubilin: multifunctional endocytic receptors. Nat Rev Mol Cell Biol 3: 256-266.
7. Christensen EI, Moskaug JO, Vorum H, Jacobsen C, Gundersen TE, Nykjaer A, Blomhoff R, Willnow TE, Moestrup SK. 1999. Evidence for an essential role of megalin in transepithelial transport of retinol. J Am Soc Nephrol 10: 685-695.
8. Drummond IA, Majumdar A, Hentschel H, Elger M, Solnica-Krezel L, Schier AF, Neuhauss SC, Stemple DL, Zwartkruis F, Rangini Z, Driever W, Fishman MC. 1998. Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125: 4655-4667.
9. Entchev EV, Kurzchalia TV. 2005. Requirement of sterols in the life cycle of the nematode Caenorhabditis elegans. Semin Cell Dev Biol 16: 175-182.
10. Gajera CR, Emich H, Lioubinski O, Christ A, Beckervordersandforth-Bonk R, Yoshikawa K, Bachmann S, Christensen EI, Gotz M, Kempermann G, Peterson AS, Willnow TE, Hammes A. 2010. LRP2 in ependymal cells regulates BMP signaling in the adult neurogenic niche. J Cell Sci 123: 1922-1930.
11. Gotthardt M, Trommsdorff M, Nevitt MF, Shelton J, Richardson JA, Stockinger W, Nimpf J, Herz J. 2000. Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J Biol Chem 275: 25616-25624.
12. Grigorenko AP, Moliaka YK, Soto MC, Mello CC, Rogaev EI. 2004. The Caenorhabditis elegans IMPAS gene, imp-2, is essential for development and is functionally distinct from related presenilins. Proc Natl Acad Sci USA 101: 14955-14960.
13. Hatta K, Kimmel CB, Ho RK, Walker C. 1991. The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system. Nature 350: 339-341.
14. Herz J, Gotthardt M, Willnow TE. 2000. Cellular signalling by lipoprotein receptors. Curr Opin Lipidol 11: 161-166.
15. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957.
16. Kantarci S, Al-Gazali L, Hill RS, Donnai D, Black GC, Bieth E, Chassaing N, Lacombe D, Devriendt K, Teebi A, Loscertales M, Robson C, Liu T, MacLaughlin DT, Noonan KM, Russell MK, Walsh CA, Donahoe PK, Pober BR. 2007. Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat Genet 39: 957-959.
17. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
18. Leheste JR, Rolinski B, Vorum H, Hilpert J, Nykjaer A, Jacobsen C, Aucouturier P, Moskaug JO, Otto A, Christensen EI, Willnow TE. 1999. Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 155: 1361-1370.
19. Matyash V, Entchev EV, Mende F, Wilsch-Brauninger M, Thiele C, Schmidt AW, Knolker HJ, Ward S, Kurzchalia TV. 2004. Sterol-derived hormone(s) controls entry into diapause in Caenorhabditis elegans by consecutive activation of DAF-12 and DAF-16. PLoS Biol 2: e280.
20. McCarthy RA, Barth JL, Chintalapudi MR, Knaak C, Argraves WS. 2002. Megalin functions as an endocytic sonic hedgehog receptor. J Biol Chem 277: 25660-25667.
21. Morris SM, Tallquist MD, Rock CO, Cooper JA. 2002. Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. Embo J 21: 1555-1564.
22. Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, Melsen F, Christensen EI, Willnow TE. 1999. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96: 507-515.
23. Schauerte HE, van Eeden FJ, Fricke C, Odenthal J, Strahle U, Haffter P. 1998. Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development 125: 2983-2993.
24. Schier AF, Neuhauss SC, Helde KA, Talbot WS, Driever W. 1997. The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail. Development 124: 327-342.
25. Serluca FC, Fishman MC. 2001. Pre-pattern in the pronephric kidney field of zebrafish. Development 128: 2233-2241.
26. Shanmugalingam S, Houart C, Picker A, Reifers F, Macdonald R, Barth A, Griffin K, Brand M, Wilson SW. 2000. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 127: 2549-2561.
27. Spoelgen R, Hammes A, Anzenberger U, Zechner D, Andersen OM, Jerchow B, Willnow TE. 2005. LRP2/megalin is required for patterning of the ventral telencephalon. Development 132: 405-414.
28. Tingaud-Sequeira A, Forgue J, Andre M, Babin PJ. 2006. Epidermal transient down-regulation of retinol-binding protein 4 and mirror expression of apolipoprotein Eb and estrogen receptor 2a during zebrafish fin and scale development. Dev Dyn 235: 3071-3079.
29. Veth KN, Willer JR, Collery RF, Gray MP, Willer GB, Wagner DS, Mullins MC, Udvadia AJ, Smith RS, John SWM, Gregg RG, Link BA. 2011. Mutations in zebrafish lrp2 result in adult-onset ocular pathogenesis that models myopia and other risk factors for glaucoma. PLoS Genetics 7: e1001310.
30. Willnow TE, Hilpert J, Armstrong SA, Rohlmann A, Hammer RE, Burns DK, Herz J. 1996. Defective forebrain development in mice lacking gp330/megalin. Proc Natl Acad Sci USA 93: 8460-8464.
31. Yochem J, Tuck S, Greenwald I, Han M. 1999. A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 126: 597-606.
32. Zheng G, Bachinsky DR, Stamenkovic I, Strickland DK, Brown D, Andres G, McCluskey RT. 1994. Organ distribution in rats of two members of the low-density lipoprotein receptor gene family, gp330 and LRP/alpa 2MR, and the receptor-associated protein (RAP). J Histochem Cytochem 42: 531-542.
33. Zupanc GK, Hinsch K, Gage FH. 2005. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488: 290-319.