In Vitro Guidance of Retinal Axons by a Tectal Lamina-specific Glycoprotein Nel

Overview

Journal Mol Cell Neurosci

Specialties Cell Biology
Molecular Biology
Neurology

Date 2009 Mar 3

PMID 19249368

Citations 10

Authors

Yulan Jiang

Hiroya Obama

Soh Leh Kuan

Ritsuko Nakamura

Chizu Nakamoto

Zhufeng Ouyang

Masaru Nakamoto

Affiliations

Soon will be listed here.

Abstract

Nel is a glycoprotein containing five chordin-like and six epidermal growth factor-like domains and is strongly expressed in the nervous system. In this study, we have examined expression patterns and in vitro functions of Nel in the chicken retinotectal system. We have found that in the developing tectum, expression of Nel is localized in specific laminae that retinal axons normally do not enter, including the border between the retinorecipient and non-retinorecipient laminae. Nel-binding activity is detected on retinal axons both in vivo and in vitro, suggesting that retinal axons express a receptor for Nel. In vitro, Nel inhibits retinal axon outgrowth and induces growth cone collapse and axon retraction. These results indicate that Nel acts as an inhibitory guidance cue for retinal axons, and suggest its roles in the establishment of the lamina-specificity in the retinotectal projection.

Citing Articles

Trans-Seq maps a selective mammalian retinotectal synapse instructed by Nephronectin.

Tsai N, Wang F, Toma K, Yin C, Takatoh J, Pai E Nat Neurosci. 2022; 25(5):659-674.

PMID: 35524141 PMC: 9172271. DOI: 10.1038/s41593-022-01068-8.

NELL2-cdc42 signaling regulates BAF complexes and Ewing sarcoma cell growth.

Jayabal P, Zhou F, Lei X, Ma X, Blackman B, Weintraub S Cell Rep. 2021; 36(1):109254.

PMID: 34233189 PMC: 8312579. DOI: 10.1016/j.celrep.2021.109254.

NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance.

Pak J, DeLoughery Z, Wang J, Acharya N, Park Y, Jaworski A Nat Commun. 2020; 11(1):1489.

PMID: 32198364 PMC: 7083938. DOI: 10.1038/s41467-020-15211-1.

Macroglia-derived thrombospondin 2 regulates alterations of presynaptic proteins of retinal neurons following elevated hydrostatic pressure.

Wang S, Hu T, Wang Z, Li N, Zhou L, Liao L PLoS One. 2017; 12(9):e0185388.

PMID: 28953973 PMC: 5617560. DOI: 10.1371/journal.pone.0185388.

Expression and regulatory effects on cancer cell behavior of NELL1 and NELL2 in human renal cell carcinoma.

Nakamura R, Oyama T, Tajiri R, Mizokami A, Namiki M, Nakamoto M Cancer Sci. 2015; 106(5):656-64.

PMID: 25726761 PMC: 4452169. DOI: 10.1111/cas.12649.

References

Aihara K, Kuroda S, Kanayama N, Matsuyama S, Tanizawa K, Horie M . A neuron-specific EGF family protein, NELL2, promotes survival of neurons through mitogen-activated protein kinases. Brain Res Mol Brain Res. 2003; 116(1-2):86-93. DOI: 10.1016/s0169-328x(03)00256-0. View

Luo Y, Raible D, Raper J . Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell. 1993; 75(2):217-27. DOI: 10.1016/0092-8674(93)80064-l. View

Matsuyama S, Aihara K, Nishino N, Takeda S, Tanizawa K, Kuroda S . Enhanced long-term potentiation in vivo in dentate gyrus of NELL2-deficient mice. Neuroreport. 2004; 15(3):417-20. DOI: 10.1097/00001756-200403010-00007. View

Kim H, Ha C, Choi J, Choi E, Jeon J, Kim C . Ontogeny and the possible function of a novel epidermal growth factor-like repeat domain-containing protein, NELL2, in the rat brain. J Neurochem. 2002; 83(6):1389-400. DOI: 10.1046/j.1471-4159.2002.01245.x. View

Nelson B, Matsuhashi S, Lefcort F . Restricted neural epidermal growth factor-like like 2 (NELL2) expression during muscle and neuronal differentiation. Mech Dev. 2003; 119 Suppl 1:S11-9. DOI: 10.1016/s0925-4773(03)00084-4. View

Takagi S, Kasuya Y, Shimizu M, Matsuura T, Tsuboi M, Kawakami A . Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system. Dev Biol. 1995; 170(1):207-22. DOI: 10.1006/dbio.1995.1208. View

Kuroda S, Oyasu M, Kawakami M, Kanayama N, Tanizawa K, Saito N . Biochemical characterization and expression analysis of neural thrombospondin-1-like proteins NELL1 and NELL2. Biochem Biophys Res Commun. 1999; 265(1):79-86. DOI: 10.1006/bbrc.1999.1638. View

Nelson B, Claes K, Todd V, Chaverra M, Lefcort F . NELL2 promotes motor and sensory neuron differentiation and stimulates mitogenesis in DRG in vivo. Dev Biol. 2004; 270(2):322-35. DOI: 10.1016/j.ydbio.2004.03.004. View

Monnier P, Sierra A, Macchi P, Deitinghoff L, Andersen J, Mann M . RGM is a repulsive guidance molecule for retinal axons. Nature. 2002; 419(6905):392-5. DOI: 10.1038/nature01041. View

10.

Ting K, Vastardis H, Mulliken J, Soo C, Tieu A, Do H . Human NELL-1 expressed in unilateral coronal synostosis. J Bone Miner Res. 1999; 14(1):80-9. DOI: 10.1359/jbmr.1999.14.1.80. View

11.

Flanagan J, Cheng H, Feldheim D, Hattori M, Lu Q, Vanderhaeghen P . Alkaline phosphatase fusions of ligands or receptors as in situ probes for staining of cells, tissues, and embryos. Methods Enzymol. 2000; 327:19-35. DOI: 10.1016/s0076-6879(00)27264-9. View

12.

Sugiyama S, Nakamura H . The role of Grg4 in tectal laminar formation. Development. 2002; 130(3):451-62. DOI: 10.1242/dev.00232. View

13.

Matsuyama S, Doe N, Kurihara N, Tanizawa K, Kuroda S, Iso H . Spatial learning of mice lacking a neuron-specific epidermal growth factor family protein, NELL2. J Pharmacol Sci. 2005; 98(3):239-43. DOI: 10.1254/jphs.fp0050211. View

14.

Goshima Y, Nakamura F, STRITTMATTER P, Strittmatter S . Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature. 1995; 376(6540):509-14. DOI: 10.1038/376509a0. View

15.

Miskevich F, Zhu Y, Ranscht B, Sanes J . Expression of multiple cadherins and catenins in the chick optic tectum. Mol Cell Neurosci. 1998; 12(4-5):240-55. DOI: 10.1006/mcne.1998.0718. View

16.

Nishida K, Flanagan J, Nakamoto M . Domain-specific olivocerebellar projection regulated by the EphA-ephrin-A interaction. Development. 2002; 129(24):5647-58. DOI: 10.1242/dev.00162. View

17.

Luce M, Burrows P . The neuronal EGF-related genes NELL1 and NELL2 are expressed in hemopoietic cells and developmentally regulated in the B lineage. Gene. 1999; 231(1-2):121-6. DOI: 10.1016/s0378-1119(99)00093-1. View

18.

Hansen M, Dallal G, Flanagan J . Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron. 2004; 42(5):717-30. DOI: 10.1016/j.neuron.2004.05.009. View

19.

FEINER L, Koppel A, Kobayashi H, Raper J . Secreted chick semaphorins bind recombinant neuropilin with similar affinities but bind different subsets of neurons in situ. Neuron. 1997; 19(3):539-45. DOI: 10.1016/s0896-6273(00)80370-0. View

20.

Beckmann G, Hanke J, Bork P, Reich J . Merging extracellular domains: fold prediction for laminin G-like and amino-terminal thrombospondin-like modules based on homology to pentraxins. J Mol Biol. 1998; 275(5):725-30. DOI: 10.1006/jmbi.1997.1510. View