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Adhesion-GPCRs in the CNS

  • Natalie Strokes
  • Xianhua Piao
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 706)

Abstract

There are a total of 33 members of adhesion G protein-coupled receptors (GPCRs) in humans and 30 members in mice and rats. More than half of these receptors are expressed in the central nervous system (CNS), indicating their possible roles in the development and function of the CNS. Indeed, it has been shown that adhesion-GPCRs are involved in the regulation of neurulation, cortical development and neurite growth. Among the few adhesion-GPCRs being studied, GPR56 is so far the only member associated with a human brain malformation called bilateral frontoparietal polymicrogyria (BFPP). The histopathology of BFPP is a cobblestone-like brain malformation characterized by neuronal overmigration through a breached pial basement membrane (BM). Further studies in the Gpr56 knockout mouse model revealed that GPR56 is expressed in radial glial cells and regulates the integrity of the pial BM by binding a putative ligand in the extracellular matrix of the developing brain.

Keywords

Neurite Growth Ventricular Zone Audiogenic Seizure Radial Glial Cell Congenital Muscular Dystrophy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Piao X, Hill RS, Bodell A et al. G protein-coupled receptor-dependent development of human frontal cortex. Science 2004; 303(5666):2033–2036.PubMedCrossRefGoogle Scholar
  2. 2.
    Piao X, Chang BS, Bodell A et al. Genotype-phenotype analysis of human frontoparietal polymicrogyria syndromes. Ann Neurol 2005; 58(5):680–687.PubMedCrossRefGoogle Scholar
  3. 3.
    Li S, Jin Z, Koirala S et al. GPR56 regulates pial basement membrane integrity and cortical lamination. J Neurosci 2008; 28(22):5817–5826.PubMedCrossRefGoogle Scholar
  4. 4.
    Mori K, Kanemura Y, Fujikawa H et al. Brain-specific angiogenesis inhibitor 1 (BAI 1) is expressed in human cerebral neuronal cells. Neurosci Res 2002; 43(1):69–74.PubMedCrossRefGoogle Scholar
  5. 5.
    Kee HJ, Koh JT, Kim MY et al. Expression of brain-specific angiogenesis inhibitor 2 (BAI2) in normal and ischemic brain: involvement of BAI2 in the ischemia-induced brain angiogenesis. J Cereb Blood Flow Metab 2002; 22(9):1054–1067.PubMedCrossRefGoogle Scholar
  6. 6.
    Koh JT, Lee ZH, Ahn KY et al. Characterization of mouse brain-specific angiogenesis inhibitor 1 (BAI1) and phytanoyl-CoA alpha-hydroxylase-associated protein 1, a novel BAI1-binding protein. Brain Res Mol Brain Res 2001; 87(2):223–237.PubMedCrossRefGoogle Scholar
  7. 7.
    Kee HJ, Ahn KY, Choi KC et al. Expression of brain-specific angiogenesis inhibitor 3 (BAI3) in normal brain and implications for BAI3 in ischemia-induced brain angiogenesis and malignant glioma. FEBS Lett 2004; 569(1-3):307–316.PubMedCrossRefGoogle Scholar
  8. 8.
    Ichtchenko K, Bittner MA, Krasnoperov V et al. A novel ubiquitously expressed alpha-latrotoxin receptor is a member of the CIRL family of G-protein-coupled receptors. J Biol Chem 1999; 274(9):5491–5498.PubMedCrossRefGoogle Scholar
  9. 9.
    Matsushita H, Lelianova VG, Ushkaryov YA. The latrophilin family: multiply spliced G protein-coupled receptors with differential tissue distribution. FEBS Lett. 1999; 443(3):348–352.PubMedCrossRefGoogle Scholar
  10. 10.
    Shima Y, Copeland NG, Gilbert DJ et al. Differential expression of the seven-pass transmembrane cadherin genes Celsrl-3 and distribution of the Celsr2 protein during mouse development. Dev Dyn 2002;223(3):321–332.PubMedCrossRefGoogle Scholar
  11. 11.
    Shima Y, Kengaku M, Hirano T et al. Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev Cell 2004; 7(2):205–216.PubMedCrossRefGoogle Scholar
  12. 12.
    Shima Y, Kawaguchi SY, Kosaka K et al. Opposing roles in neurite growth control by two seven-pass transmembrane cadherins. Nat Neurosci 2007; 10(8):963–969.PubMedCrossRefGoogle Scholar
  13. 13.
    Tissir F, Bar I, Jossin Y et al. Protocadherin Celsr3 is crucial in axonal tract development. Nat Neurosci 2005; 8(4):451–457.PubMedGoogle Scholar
  14. 14.
    Curtin JA, Quint E, Tsipouri V et al. Mutation of Celsrl disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Current Biology 2003; 13(13):1129–1133.PubMedCrossRefGoogle Scholar
  15. 15.
    McMillan DR, Kayes-Wandover KM, Richardson JA et al. Very large G protein-coupled receptor-1, the largest known cell surface protein, is highly expressed in the developing central nervous system. J Biol Chem 2002; 277(1):785–792.PubMedCrossRefGoogle Scholar
  16. 16.
    McMillan DR, White PC. Loss of the transmembrane and cytoplasmic domains of the very large G protein-coupled receptor-1 (VLGR1 or Mass1) causes audiogenic seizures in mice. Mol Cell Neurosci 2004; 26(2):322–329.PubMedCrossRefGoogle Scholar
  17. 17.
    Skradski SL, White HS, Ptacek LJ. Genetic mapping of a locus (mass1) causing audiogenic seizures in mice. Genomics 1998; 49(2): 188–192.PubMedCrossRefGoogle Scholar
  18. 18.
    Weston MD, Luijendijk MW, Humphrey KD et al. Mutations in the VLGR1 gene implicate G-protein signaling in the pathogenesis of Usher syndrome type II. Am J Hum Genet 2004; 74(2):357–366.PubMedCrossRefGoogle Scholar
  19. 19.
    van Wijk E, van der Zwaag B, Peters T et al. The DFNB31 gene product whirlin connects to the Usher protein network in the cochlea and retina by direct association with USH2A and VLGR1. Hum Mol Genet 2006; 15(5):751–765.PubMedCrossRefGoogle Scholar
  20. 20.
    McGee J, Goodyear RJ, McMillan DR et al. The very large G-protein-coupled receptor VLGR1: a component of the ankle link complex required for the normal development of auditory hair bundles. J Neurosci 2006; 26(24):6543–6553.PubMedCrossRefGoogle Scholar
  21. 21.
    Piao X, Basel-Vanagaite L, Straussberg R et al. An autosomal recessive form of bilateral frontoparietal polymicrogyria maps to chromosome 16q12.2-21. Am J Hum Genet 2002; 70(4): 1028–1033.PubMedCrossRefGoogle Scholar
  22. 22.
    Chang BS, Piao X, Bodell A et al. Bilateral frontoparietal polymicrogyria: clinical and radiological features in 10 families with linkage to chromosome 16. Ann Neurol 2003; 53(5):596–606.PubMedCrossRefGoogle Scholar
  23. 23.
    Parrini E, Ferrari AR, Dorn T et al. Bilateral frontoparietal polymicrogyria, Lennox-Gastaut syndrome and GPR56 gene mutations. Epilepsia 2008; 50(6):1344–1353.PubMedCrossRefGoogle Scholar
  24. 24.
    Jin Z, Tietjen I, Bu L et al. Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum Mol Genet 2007; 16(16):1972–1985.PubMedCrossRefGoogle Scholar
  25. 25.
    Olson EC, Walsh CA. Smooth, rough and upside-down neocortical development. Curr Opin Genet Dev 2002; 12(3):320–327.PubMedCrossRefGoogle Scholar
  26. 26.
    Kobayashi K, Nakahori Y, Miyake M et al. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 1998; 394(6691):388–392.PubMedCrossRefGoogle Scholar
  27. 27.
    Yoshida A, Kobayashi K, Manya H et al. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 2001; 1(5):717–724.PubMedCrossRefGoogle Scholar
  28. 28.
    Michele DE, Barresi R, Kanagawa M et al. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 2002; 418(6896):417–422.PubMedCrossRefGoogle Scholar
  29. 29.
    Georges-Labouesse E, Mark M, Messaddeq N et al. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 1998; 8(17):983–986.PubMedCrossRefGoogle Scholar
  30. 30.
    De Arcangelis A, Mark M, Kreidberg J et al. Synergistic activities of alpha3 and alpha6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 1999; 126(17):3957–3968.PubMedGoogle Scholar
  31. 31.
    Graus-Porta D, Blaess S, Senften M et al. Betal-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 2001; 31(3):367–379.PubMedCrossRefGoogle Scholar
  32. 32.
    Beggs HE, Schahin-Reed D, Zang K et al. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 2003; 40(3):501–514.PubMedCrossRefGoogle Scholar
  33. 33.
    Niewmierzycka A, Mills J, St-Arnaud R et al. Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J Neurosci 2005; 25(30):7022–7031.PubMedCrossRefGoogle Scholar
  34. 34.
    Costell M, Gustafsson E, Aszodi A et al. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 1999; 147(5): 1109–1122.PubMedCrossRefGoogle Scholar
  35. 35.
    Sarkisian MR, Bartley CM, Chi H et al. MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 2006; 52(5):789–801.PubMedCrossRefGoogle Scholar
  36. 36.
    Voss AK, Britto JM, Dixon MP et al. C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 2008; 135(12):2139–2149.PubMedCrossRefGoogle Scholar
  37. 37.
    Kwiatkowski AV, Rubinson DA, Dent EW et al. Ena/VASP is required for neuritogenesis in the developing cortex. Neuron 2007; 56(3):441–455.PubMedCrossRefGoogle Scholar
  38. 38.
    Halfter W, Dong S, Yip YP et al. A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 2002; 22(14):6029–6040.PubMedGoogle Scholar
  39. 39.
    Haubst N, Georges-Labouesse E, De Arcangelis A et al. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 2006; 133(16):3245–3254.PubMedCrossRefGoogle Scholar
  40. 40.
    Hu H, Yang Y, Eade A et al. Breaches of the pial basement membrane and disappearance of the glia limitans during development underlie the cortical lamination defect in the mouse model of muscle-eye-brain disease. J Comp Neurol 2007; 501(1):168–183.PubMedCrossRefGoogle Scholar
  41. 41.
    Koirala S, Jin Z, Piao X et al. GPR56-regulated granule cell adhesion is essential for rostral cerebellar development. J Neurosci 2009; 29(23):7439–7449.PubMedCrossRefGoogle Scholar
  42. 42.
    Little KD, Hemler ME, Stipp CS. Dynamic regulation of a GPCR-tetraspanin-G protein complex on intact cells: central role of CD81 infacilitatingGPR56-Gαq/11 association. Mol Biol Cell 2004; 15(5):2375–2387.PubMedCrossRefGoogle Scholar
  43. 43.
    Levy S, Shoham T. The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol 2005;5(2):136–148.PubMedCrossRefGoogle Scholar
  44. 44.
    Xu L, Begum S, Hearn JD et al. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2 and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci USA 13 2006; 103(24):9023–9028.CrossRefGoogle Scholar
  45. 45.
    Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 2003; 4(2): 140–156.PubMedCrossRefGoogle Scholar
  46. 46.
    Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 2002; 27(10):534–539.PubMedCrossRefGoogle Scholar
  47. 47.
    Gaudry CA, Verderio E, Aeschlimann D et al. Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal beta-sandwich domain. J Biol Chem 1999; 274(43):30707–30714.PubMedCrossRefGoogle Scholar
  48. 48.
    Telci D, Wang Z, Li X et al. Fibronectin-tissue transglutaminase matrix rescues RGD-impaired cell adhesion through syndecan-4 and betal integrin cosignaling. J Biol Chem 2008; 283(30):20937–20947.PubMedCrossRefGoogle Scholar
  49. 49.
    Mhaouty-Kodja S. Ghalpha/tissue transglutaminase 2: an emerging G protein in signal transduction. Biol Cell 2004; 96(5):363–367.PubMedCrossRefGoogle Scholar
  50. 50.
    Nakaoka H, Perez DM, Baek KJ et al. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 1994; 264(5165):1593–1596.PubMedCrossRefGoogle Scholar
  51. 51.
    Kang SK, Yi KS, Kwon NS et al. Alpha1B-adrenoceptor signaling and cell motility: GTPase function of Gh/transglutaminase 2 inhibits cell migration through interaction with cytoplasmic tail of integrin alpha subunits. J Biol Chem 2004; 279(35):36593–36600.PubMedCrossRefGoogle Scholar
  52. 52.
    Bailey CD, Johnson GV. Developmental regulation of tissue transglutaminase in the mouse forebrain. J Neurochem 2004; 91(6):1369–1379.PubMedCrossRefGoogle Scholar
  53. 53.
    Sievers J, Pehlemann FW, Gude S et al. Meningeal cells organize the superficial glialimitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 1994; 23(2):135–149.PubMedCrossRefGoogle Scholar
  54. 54.
    Super H, Martinez A, Soriano E. Degeneration of Cajal-Retzius cells in the developing cerebral cortex of the mouse after ablation of meningeal cells by 6-hydroxy dopamine. Brain Res Dev Brain Res 1997; 98(1):15–20.PubMedCrossRefGoogle Scholar
  55. 55.
    Zarbalis K, Siegenthaler JA, Choe Y et al. Cortical dysplasia and skull defects in mice with a Foxc1 allele reveal the role of meningeal differentiation in regulating cortical development. Proc Natl Acad Sci USA 2007; 104(35):14002–14007.PubMedCrossRefGoogle Scholar
  56. 56.
    Paredes MF, Li G, Berger O et al. Stromal-derived factor-1 (CXCL12) regulates laminar position of Cajal-Retzius cells in normal and dysplastic brains. J Neurosci 2006; 26(37):9404–9412.PubMedCrossRefGoogle Scholar
  57. 57.
    Inoue T, Ogawa M, Mikoshiba K et al. Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type II lissencephaly. J Neurosci 2008; 28(18):4712–4725.PubMedCrossRefGoogle Scholar
  58. 58.
    Iguchi T, Sakata K, Yoshizaki K et al. Orphan G protein-coupled receptor GPR56 regulates neural progenitor cell migration via a Gα12/13 and Rho pathway. J Biol Chem 2008; 283(21):14469–14478.PubMedCrossRefGoogle Scholar
  59. 59.
    Shashidhar S, Lorente G, Nagavarapu U et al. GPR56 is a GPCR that is overexpressed in gliomas and functions in tumor cell adhesion. Oncogene 2005; 24(10):1673–1682.PubMedCrossRefGoogle Scholar
  60. 60.
    Haitina T, Olsson F, Stephansson O et al. Expression profile of the entire family of Adhesion Gprotein-coupled receptors in mouse and rat. BMC Neurosci 2008;9:43.PubMedCrossRefGoogle Scholar
  61. 61.
    Lein ES, Hawrylycz MJ, Ao N et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007; 445(7124):168–176.PubMedCrossRefGoogle Scholar
  62. 62.
    Pickering C, Hagglund M, Szmydynger-Chodobska J et al. The Adhesion-GPCR GPR125 is specifically expressed in the choroid plexus and is upregulated following brain injury. BMC Neurosci 2008; 9:97.PubMedCrossRefGoogle Scholar
  63. 63.
    Lagerström MC, Rabe N, Haitina T et al. The evolutionary history and tissue mapping of GPR123: specific CNS expression pattern predominantly in thalamic nuclei and regions contraining large pyramidal cells. J Neurochem 2007; 100:1129–1142.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Natalie Strokes
  • Xianhua Piao
    • 1
  1. 1.Division of Newborn Medicine, Children’s Hospital BostonHarvard Medical SchoolBostonUSA

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