Receptor-like Protein-tyrosine Phosphatase α Enhances Cell Surface Expression of Neural Adhesion Molecule NB-3

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2011 May 31

PMID 21622556

Citations 8

Authors

Haihong Ye

Tian Zhao

Yen Ling Jessie Tan

Jianghong Liu

Catherine J Pallen

Zhi-Cheng Xiao

Affiliations

Soon will be listed here.

Abstract

Neural adhesion molecule NB-3 plays an important role in the apical dendrite development of layer V pyramidal neurons in the visual cortex, and receptor-like protein-tyrosine phosphatase α (PTPα) mediates NB-3 signaling in this process. Here we investigated the role of PTPα in regulating cell surface expression of NB-3. We found that cortical neurons from PTPα knock-out mice exhibited a lower level of NB-3 at the cell surface. When expressed in COS1 cells, NB-3 was enriched in the Golgi apparatus with a low level of cell surface expression. However, co-expression of PTPα increased the cell surface distribution of NB-3. Further analysis showed that PTPα facilitated Golgi exit of NB-3 and stabilized NB-3 protein at the cell surface by preventing its release from the plasma membrane. The extracellular region of PTPα but not its catalytic activity is necessary for its effect on NB-3 expression. Thus, the PTPα-mediated increase of NB-3 level at the cell surface represents a novel function of PTPα in NB-3 signaling in neural development.

Citing Articles

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References

Moller N, Moller K, Lammers R, Kharitonenkov A, Hoppe E, Wiberg F . Selective down-regulation of the insulin receptor signal by protein-tyrosine phosphatases alpha and epsilon. J Biol Chem. 1995; 270(39):23126-31. DOI: 10.1074/jbc.270.39.23126. View

Lei G, Xue S, Chery N, Liu Q, Xu J, Kwan C . Gain control of N-methyl-D-aspartate receptor activity by receptor-like protein tyrosine phosphatase alpha. EMBO J. 2002; 21(12):2977-89. PMC: 126051. DOI: 10.1093/emboj/cdf292. View

Sap J, DEustachio P, Givol D, Schlessinger J . Cloning and expression of a widely expressed receptor tyrosine phosphatase. Proc Natl Acad Sci U S A. 1990; 87(16):6112-6. PMC: 54482. DOI: 10.1073/pnas.87.16.6112. View

Ye H, Tan Y, Ponniah S, Takeda Y, Wang S, Schachner M . Neural recognition molecules CHL1 and NB-3 regulate apical dendrite orientation in the neocortex via PTP alpha. EMBO J. 2007; 27(1):188-200. PMC: 2206121. DOI: 10.1038/sj.emboj.7601939. View

von Wichert G, Jiang G, Kostic A, Vos K, Sap J, Sheetz M . RPTP-alpha acts as a transducer of mechanical force on alphav/beta3-integrin-cytoskeleton linkages. J Cell Biol. 2003; 161(1):143-53. PMC: 2172891. DOI: 10.1083/jcb.200211061. View

Cui X, Hu Q, Tekaya M, Shimoda Y, Ang B, Nie D . NB-3/Notch1 pathway via Deltex1 promotes neural progenitor cell differentiation into oligodendrocytes. J Biol Chem. 2004; 279(24):25858-65. DOI: 10.1074/jbc.M313505200. View

Hu Q, Ang B, Karsak M, Hu W, Cui X, Duka T . F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell. 2003; 115(2):163-75. DOI: 10.1016/s0092-8674(03)00810-9. View

Zheng X, Resnick R, Shalloway D . Mitotic activation of protein-tyrosine phosphatase alpha and regulation of its Src-mediated transforming activity by its sites of protein kinase C phosphorylation. J Biol Chem. 2002; 277(24):21922-9. PMC: 5641391. DOI: 10.1074/jbc.M201394200. View

Sakurai K, Toyoshima M, Ueda H, Matsubara K, Takeda Y, Karagogeos D . Contribution of the neural cell recognition molecule NB-3 to synapse formation between parallel fibers and Purkinje cells in mouse. Dev Neurobiol. 2009; 69(12):811-24. DOI: 10.1002/dneu.20742. View

10.

Wang P, Wang J, Xiao Z, Pallen C . Protein-tyrosine phosphatase alpha acts as an upstream regulator of Fyn signaling to promote oligodendrocyte differentiation and myelination. J Biol Chem. 2009; 284(48):33692-702. PMC: 2785211. DOI: 10.1074/jbc.M109.061770. View

11.

Demyanenko G, Schachner M, Anton E, Schmid R, Feng G, Sanes J . Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron. 2004; 44(3):423-37. DOI: 10.1016/j.neuron.2004.10.016. View

12.

Cuoco C, Ronchetto P, Gimelli S, Bena F, Divizia M, Lerone M . Microarray based analysis of an inherited terminal 3p26.3 deletion, containing only the CHL1 gene, from a normal father to his two affected children. Orphanet J Rare Dis. 2011; 6:12. PMC: 3090742. DOI: 10.1186/1750-1172-6-12. View

13.

Krndija D, Schmid H, Eismann J, Lother U, Adler G, Oswald F . Substrate stiffness and the receptor-type tyrosine-protein phosphatase alpha regulate spreading of colon cancer cells through cytoskeletal contractility. Oncogene. 2010; 29(18):2724-38. DOI: 10.1038/onc.2010.25. View

14.

Yang L, Alexandropoulos K, Sap J . c-SRC mediates neurite outgrowth through recruitment of Crk to the scaffolding protein Sin/Efs without altering the kinetics of ERK activation. J Biol Chem. 2002; 277(20):17406-14. DOI: 10.1074/jbc.M111902200. View

15.

den Hertog J, Pals C, Peppelenbosch M, Tertoolen L, de Laat S, Kruijer W . Receptor protein tyrosine phosphatase alpha activates pp60c-src and is involved in neuronal differentiation. EMBO J. 1993; 12(10):3789-98. PMC: 413662. DOI: 10.1002/j.1460-2075.1993.tb06057.x. View

16.

Verjaal M, De Nef M . A patient with a partial deletion of the short arm of chromosome 3. Am J Dis Child. 1978; 132(1):43-5. DOI: 10.1001/archpedi.1978.02120260045012. View

17.

Tsai W, Morielli A, Cachero T, Peralta E . Receptor protein tyrosine phosphatase alpha participates in the m1 muscarinic acetylcholine receptor-dependent regulation of Kv1.2 channel activity. EMBO J. 1999; 18(1):109-18. PMC: 1171107. DOI: 10.1093/emboj/18.1.109. View

18.

Pohjola P, de Leeuw N, Penttinen M, Kaariainen H . Terminal 3p deletions in two families--correlation between molecular karyotype and phenotype. Am J Med Genet A. 2010; 152A(2):441-6. DOI: 10.1002/ajmg.a.33215. View

19.

He D, Ron D . Autoregulation of glial cell line-derived neurotrophic factor expression: implications for the long-lasting actions of the anti-addiction drug, Ibogaine. FASEB J. 2006; 20(13):2420-2. DOI: 10.1096/fj.06-6394fje. View

20.

Takeda Y, Akasaka K, Lee S, Kobayashi S, Kawano H, Murayama S . Impaired motor coordination in mice lacking neural recognition molecule NB-3 of the contactin/F3 subgroup. J Neurobiol. 2003; 56(3):252-65. DOI: 10.1002/neu.10222. View