Neuronal leucine-rich repeat 6 (XlNLRR-6) is required for late lens and retina development in Xenopus laevis

Developmental Dynamics

Volumn 235, Issue 4, 2006, Pages 1027-1041

  Wolfe, Adam D ^a   Henry, Jonathan J ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b B107 Chem and Life Sci Laboratory   (United States)

Author keywords

Cornea; Lens; Morpholino; Neuronal leucine rich repeat protein; Retina; Xenopus laevis

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CELL PROTEIN; EYE PROTEIN; LEUCINE; MORPHOLINE DERIVATIVE; NEURONAL LEUCINE RICH REPEAT 6 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA; EMBRYO; EMBRYO DEVELOPMENT; EYE DEVELOPMENT; IN VIVO STUDY; LARVAL DEVELOPMENT; LENS; NEUROECTODERM; NEURULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; RETINA DEVELOPMENT; SEQUENCE ANALYSIS; TISSUE DIFFERENTIATION; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; ECTODERM; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; LENS, CRYSTALLINE; LEUCINE; MOLECULAR SEQUENCE DATA; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RETINA; SEQUENCE HOMOLOGY, AMINO ACID; XENOPUS LAEVIS; XENOPUS PROTEINS;

ANIMALIA; VERTEBRATA; XENOPUS LAEVIS;

EID: 33645472170     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20691     Document Type: Article

References (48)

1. Almeida A, Zhu XX, Vogt N, Tyagi R, Muleris M, Dutrillaux A-M, Dutrillaux B, Ross D, Malfoy B, Hanash S. 1998. GAC1, a new member of the leucine-rich repeat superfamily on chromosome band 1q32.1, is amplified and overexpressed in malignant gliomas. Oncogene 16:2997-3002.
2. Ando H, Kobayashi M, Tsubokawa T, Uyemura K, Furuta T, Okamoto H. 2005. Lhx2 mediates the activity of Six3 in zebrafish forebrain growth. Dev Biol 287:456-468.
3. Audic Y, Boyle B, Slevin M, Hartley RS. 2001. Cyclin E morpholino delays embryogenesis in Xenopus. Genesis 30:107-109.
4. Bando T, Sekine K, Kobayashi S, Watabe AM, Rump A, Tanaka M, Suda Y, Kato S, Morikawa Y, Manabe T, Miyajima A. 2005. Neuronal leucine-rich repeat protein 4 functions in hippocampus-dependent long-lasting memory. Mol Cell Biol 25:4166-4175.
5. Belo JA, Bouwmeester T, Leyns L, Kertesz N, Gallo M, Follettie M, De Robertis EM. 1997. Cerberus-like is a secreted factor with neuralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech Dev 68:45-57.
6. Bormann P, Roth LWA, Andel D, Ackermann M, Reinhard E. 1999. zfNLRR, a novel leucine-rich repeat protein is preferentially expressed during regeneration in zebrafish. Mol Cell Neurosci 13:167-179.
7. Carim-Todd L, Escarceller M, Estivill X, Sumoy L. 2003. LRRN6A/LERN1 (leucine-rich repeat neuronal protein 1), a novel gene with enriched expression in limbic system and neocortex. Eur J Neurosci 18: 3167-3182.
8. Chow RL, Lang RA. 2001. Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255-296.
9. Chung HA, Hyodo-Miura J, Nagamune T, Ueno N. 2005. FGF signal regulates gastrulation cell movements and morphology through its target NRH. Dev Biol 282:95-110.
10. Fukamachi K, Matsuoka Y, Kitanaka C, Kuchino Y, Tsuda H. 2001. Rat neuronal leucine-rich repeat protein-3: cloning and regulation of the gene expression. Biochem Biophys Res Commun 287:257-263.
11. Fukamachi K, Matsuoka Y, Ohno H, Hamaguchi T, Tsuda H. 2002. Neuronal leucine-rich repeat protein-3 amplifies MAPK activation by epidermal growth factor through a carboxyl-terminal region containing endocytosis motifs. J Biol Chem 277:43549-43552.
12. Grainger RM. 1996. New perspectives on embryonic lens induction. Semin Cell Dev Biol 7:149-155.
13. Hamano S, Ohira M, Isogai E, Nakada K, Nakagawara A. 2004. Identification of novel human neuronal leucine-rich repeat (hNLRR) family genes and inverse association of expression of Nbla10449/hNLRRO1 and Nbla10677/hNLRR-3 with the prognosis of primary neuroblastomas. Int J Oncol 24:1457-1466.
14. Harland RM. 1991. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36: 685-695.
15. Hashiguchi A, Okabayashi K, Asashima M. 2004. Role of TSC-22 during early embryogenesis in Xenopus laevis. Dev Growth Differ 46:535-544.
16. Hashimoto C, Hudson KL, Anderson KV. 1988. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52:269-279.
17. Hay ED. 1977. Interaction between the cell surface and extracellular matrix in corneal development. Soc Gen Physiol Ser 32:115-137.
18. Hayata T, Uochi T, Asashima M. 1998. Molecular cloning of XNLRR-1, a Xenopus homolog of mouse neuronal leucine-rich repeat protein expressed in the developing Xenopus nervous system. Gene 221: 159-166.
19. Heasman J. 2002. Morpholino oligos: making sense of antisense? Dev Biol 243:209-214.
20. Henry JJ, Grainger RM. 1987. Inductive interactions in the spatial and temporal restriction of lens-forming potential in embryonic ectoderm of Xenopus laevis. Dev Biol 124:200-214.
21. Henry JJ, Grainger RM. 1990. Early tissue interactions leading to embryonic lens formation in Xenopus laevis. Dev Biol 141:149-163.
22. Henry JJ, Mittleman JM. 1995. The matured eye of Xenopus laevis tadpoles produces factors that elicit a lens-forming response in embryonic ectoderm. Dev Biol 171:39-50.
23. Henry JJ, Carinato ME, Schaefer JJ, Wolfe AD, Walter BE, Perry KJ, Elbl TE. 2002. Characterizing gene expression during lens formation in Xenopus laevis: evaluating the model for embryonic lens induction. Dev Dyn 224:168-185.
24. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310-2314.
25. Humason GL. 1972. Animal tissue techniques. 3rd ed. San Francisco, CA: W.H. Freeman and Company.
26. Hyer J, Mima T, Mikawa T. 1998. FGF1 patterns the optic vesicle by directing the placement of the neural retina domain. Development 125:869-877.
27. Hyer J, Kuhlman J, Afif E, Mikawa T. 2003. Optic cup morphogenesis requires pre-lens ectoderm but not lens differentiation. Dev Biol 259:351-363.
28. Ishii N, Wanaka A, Tohyama M. 1996. Increased expression of NLRR-3 mRNA after cortical brain injury in mouse. Mol Brain Res 40:148-152.
29. Khokha MK, Yeh J, Grammer TC, Harland RM. 2005. Depletion of three BMP antagonists from Spemann's Organizer leads to a catastrophic loss of dorsal structures. Dev Cell 8:401-411.
30. Kobe B, Deisenhofer J. 1994. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415-421.
31. Kobe B, Deisenhofer J. 1995. Proteins with leucine-rich repeats. Curr Biol 5:409-416.
32. Lauren J, Airaksinen MS, Saarma M, Timmusk TT. 2003. A novel gene family encoding leucine-rich repeat transmembrane proteins differentially expressed in the nervous system. Genomics 81:411-421.
33. Lillien L. 1995. Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 377:158-162.
34. Maidment JM, Duncan G, Tamiya S, Collison DJ, Wang L, Wormstone IM. 2004. Regional differences in tyrosine kinase receptor signaling components determine differential growth patterns in the human lens. Invest Ophthalmol Vis Sci 45:1427-1435.
35. Mayor R, Morgan R, Sargent MG. 1995. Induction of the prospective neural crest of Xenopus. Development 121:767-777.
36. McDevitt DS, Brahma SK. 1973. Ontogeny and localization of crystalline during embryonic lens development in Xenopus laevis. J Exp Zool 186:127-140.
37. Nakamura Y, Gojobori T, Ikemura T. 2000. Codon usage tabulated from the international DNA sequence databases: status for the year 2000. Nucleic Acids Res 28: 292.
38. Nieuwkoop PD, Faber J. 1956. Normal table of Xenopus laevis (Daudin): a systematical & chronological survey of the development from the fertilized egg till the end of metamorphosis. Amsterdam: North-Holland Publishing Company.
39. Nose A, Mahajan VB, Goodman CS. 1992. Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70:553-567.
40. Rhee KD, Goureau O, Chen S, Yang X-J. 2004. Cytokine-induced activation of signal transducer and activator of transcription in photoreceptor precursors regulates rod differentiation in the developing mouse retina. J Neurosci 24: 9779-9788.
41. Rothberg JM, Hartley DA, Walther Z, Artavanis-Tsakonas S. 1988. slit: an EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system. Cell 55:1047-1059.
42. Sambrook J, Russell DW. 2001. molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
43. Schaefer JJ, Oliver G, Henry JJ. 1999. Conservation of gene expression during embryonic lens formation and cornealens transdifferentiation in Xenopus laevis. Dev Dyn 215:308-318.
44. Taguchi A, Wanaka A, Mori T, Matsumoto K, Imai Y, Tagaki T, Tohyama M. 1996. Molecular cloning of novel leucine-rich repeat proteins and their expression in the developing mouse nervous system. Mol Brain Res 35:31-40.
45. Taniguchi H, Tohyama M, Takagi T. 1996. Cloning and expression of a novel gene for a protein with leucine-rich repeats in the developing mouse nervous system. Mol Brain Res 36:45-52.
46. Taniguchi H, Shishido E, Takeichi M, Nose A. 2000. Functional dissection of Drosophila capricious: its novel roles in neuronal pathfinding and selective synapse formation. J Neurobiol 42:104-116.
47. Walter BE, Tian Y, Garlisch AK, Carinato ME, Elkins MB, Wolfe AD, Schaefer JJ, Perry KJ, Henry JJ. 2004. Molecular profiling: gene expression reveals discrete phases of lens induction and development in Xenopus laevis. Mol Vis 10: 186-198.
48. Wolfe AD, Crimmins G, Cameron JA, Henry JJ. 2004. Early regeneration genes: building a molecular profile for shared expression in cornea-lens trans-differentiation and hind limb regeneration in Xenopus laevis. Dev Dyn 230:615-629.