Skip to main content

GPR56 and the Developing Cerebral Cortex: Cells, Matrix, and Neuronal Migration

Molecular Neurobiology volume 47, pages 186–196 (2013)Cite this article

Abstract

GPR56, a member of the adhesion G protein-coupled receptor (GPCR) family, is integral to the development of the cortex, as mutations in GPR56 cause bilateral frontoparietal polymicrogyria (BFPP). BFPP is a cobblestone-like cortical malformation, characterized by overmigrating neurons and the formation of neuronal ectopias on the surface of the brain. Since its original cloning a decade ago, GPR56 has emerged from an orphaned and uncharacterized protein to an increasingly well-understood receptor, both in terms of its signaling and function. Collagen III is the ligand of GPR56 in the developing brain. Upon binding to collagen III, GPR56 activates RhoA via coupling to Gα12/13. This pathway appears to be particularly critical in the preplate neurons, which are the earliest born neurons in the cortex, as the expression pattern of GPR56 in these neurons mimics the anterior to posterior gradient of malformation associated with loss of GPR56 in both humans and mice. Further characterizing the role of GPR56 in the preplate will shed light on the mechanism of cortical development and patterning.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 63:1256–1272. doi:10.1124/mol.63.6.125663/6/1256

    PubMed  Article  CAS  Google Scholar 

  2. Lagerstrom MC, Schioth HB (2008) Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat Rev Drug Discov 7:339–357. doi:10.1038/nrd2518

    PubMed  Article  Google Scholar 

  3. Yona S, Lin HH, Siu WO, Gordon S, Stacey M (2008) Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem Sci 33:491–500. doi:10.1016/j.tibs.2008.07.005

    PubMed  Article  CAS  Google Scholar 

  4. Stacey M, Lin HH, Gordon S, McKnight AJ (2000) LNB-TM7, a group of seven-transmembrane proteins related to family-B G-protein-coupled receptors. Trends Biochem Sci 25:284–289

    PubMed  Article  CAS  Google Scholar 

  5. Strokes N, Piao X (2011) Adhesion-GPCRs in the CNS. Adv Exp Med Biol 706:87–97. doi:10.1007/978-1-4419-7913-1_7

    Article  Google Scholar 

  6. Piao X, Hill RS, Bodell A, Chang BS, Basel-Vanagaite L, Straussberg R et al (2004) G protein-coupled receptor-dependent development of human frontal cortex. Science 303:2033–2036

    PubMed  Article  CAS  Google Scholar 

  7. Piao X, Chang BS, Bodell A, Woods K, Benzeev B, Topcu M et al (2005) Genotype–phenotype analysis of human frontoparietal polymicrogyria syndromes. Ann Neurol 58:680–687

    PubMed  Article  CAS  Google Scholar 

  8. Harbord MG, Boyd S, Hall-Craggs MA, Kendall B, McShane MA, Baraitser M (1990) Ataxia, developmental delay and an extensive neuronal migration abnormality in 2 siblings. Neuropediatrics 21:218–221

    PubMed  Article  CAS  Google Scholar 

  9. Chang BS, Piao X, Bodell A, Basel-Vanagaite L, Straussberg R, Dobyns WB et al (2003) Bilateral frontoparietal polymicrogyria: clinical and radiological features in 10 families with linkage to chromosome 16. Ann Neurol 53:596–606

    PubMed  Article  CAS  Google Scholar 

  10. Piao X, Basel-Vanagaite L, Straussberg R, Grant PE, Pugh EW, Doheny K et al (2002) An autosomal recessive form of bilateral frontoparietal polymicrogyria maps to chromosome 16q12.2-21. Am J Hum Genet 70:1028–1033

    PubMed  Article  CAS  Google Scholar 

  11. Bahi-Buisson N, Poirier K, Boddaert N, Fallet-Bianco C, Specchio N, Bertini E et al (2010) GPR56-related bilateral frontoparietal polymicrogyria: further evidence for an overlap with the cobblestone complex. Brain 133:3194–3209. doi:10.1093/brain/awq259

    PubMed  Article  Google Scholar 

  12. Luo R, Yang HM, Jin Z, Halley DJ, Chang BS, MacPherson L et al (2011) A novel GPR56 mutation causes bilateral frontoparietal polymicrogyria. Pediatr Neurol 45:49–53. doi:10.1016/j.pediatrneurol.2011.02.004

    PubMed  Article  Google Scholar 

  13. Parrini E, Ferrari AR, Dorn T, Walsh CA, Guerrini R (2009) Bilateral frontoparietal polymicrogyria, Lennox–Gastaut syndrome, and GPR56 gene mutations. Epilepsia 50(6):1344–1353

    PubMed  Article  CAS  Google Scholar 

  14. Zendman AJ, Cornelissen IM, Weidle UH, Ruiter DJ, van Muijen GN (1999) TM7XN1, a novel human EGF-TM7-like cDNA, detected with mRNA differential display using human melanoma cell lines with different metastatic potential. FEBS Lett 446:292–298

    PubMed  Article  CAS  Google Scholar 

  15. Liu M, Parker RM, Darby K, Eyre HJ, Copeland NG, Crawford J et al (1999) GPR56, a novel secretin-like human G-protein-coupled receptor gene. Genomics 55:296–305

    PubMed  Article  CAS  Google Scholar 

  16. Jeong SJ, Luo R, Li S, Strokes N, Piao X (2012) Characterization of G protein-coupled receptor 56 protein expression in the mouse developing neocortex. J Comp Neurol 520:2930–2940. doi:10.1002/cne.23076

    PubMed  Article  CAS  Google Scholar 

  17. Jansen A, Andermann E (2005) Genetics of the polymicrogyria syndromes. J Med Genet 42:369–378

    PubMed  Article  CAS  Google Scholar 

  18. Ferrer I, Catala I (1991) Unlayered polymicrogyria: structural and developmental aspects. Anat Embryol (Berl) 184:517–528

    Article  CAS  Google Scholar 

  19. Eriksson SH, Thom M, Heffernan J, Lin WR, Harding BN, Squier MV et al (2001) Persistent reelin-expressing Cajal–Retzius cells in polymicrogyria. Brain 124:1350–1361

    PubMed  Article  CAS  Google Scholar 

  20. Olson EC, Walsh CA (2002) Smooth, rough and upside-down neocortical development. Curr Opin Genet Dev 12:320–327

    PubMed  Article  CAS  Google Scholar 

  21. Dobyns WB, Patton MA, Stratton RF, Mastrobattista JM, Blanton SH, Northrup H (1996) Cobblestone lissencephaly with normal eyes and muscle. Neuropediatrics 27:70–75

    PubMed  Article  CAS  Google Scholar 

  22. Li S, Jin Z, Koirala S, Bu L, Xu L, Hynes RO et al (2008) GPR56 regulates pial basement membrane integrity and cortical lamination. J Neurosci 28:5817–5826

    PubMed  Article  CAS  Google Scholar 

  23. Koirala S, Jin Z, Piao X, Corfas G (2009) GPR56-regulated granule cell adhesion is essential for rostral cerebellar development. J Neurosci 29:7439–7449. doi:10.1523/JNEUROSCI.1182-09.2009

    PubMed  Article  CAS  Google Scholar 

  24. Kobayashi K, Nakahori Y, Miyake M, Matsumura K, Kondo-Iida E, Nomura Y et al (1998) An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 394:388–392

    PubMed  Article  CAS  Google Scholar 

  25. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M et al (2001) Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 1:717–724

    PubMed  Article  CAS  Google Scholar 

  26. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS et al (2002) Post-translational disruption of dystroglycan–ligand interactions in congenital muscular dystrophies. Nature 418:417–422

    PubMed  Article  CAS  Google Scholar 

  27. Yamamoto T, Kato Y, Kawaguchi M, Shibata N, Kobayashi M (2004) Expression and localization of fukutin, POMGnT1, and POMT1 in the central nervous system: consideration for functions of fukutin. Med Electron Microsc 37:200–207

    PubMed  Article  CAS  Google Scholar 

  28. Georges-Labouesse E, Mark M, Messaddeq N, Gansmuller A (1998) Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 8:983–986

    PubMed  Article  CAS  Google Scholar 

  29. De Arcangelis A, Mark M, Kreidberg J, Sorokin L, Georges-Labouesse E (1999) Synergistic activities of alpha3 and alpha6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 126:3957–3968

    PubMed  Google Scholar 

  30. Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z et al (2001) Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31:367–379

    PubMed  Article  CAS  Google Scholar 

  31. Beggs HE, Schahin-Reed D, Zang K, Goebbels S, Nave KA, Gorski J et al (2003) FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40:501–514

    PubMed  Article  CAS  Google Scholar 

  32. Niewmierzycka A, Mills J, St-Arnaud R, Dedhar S, Reichardt LF (2005) Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J Neurosci 25:7022–7031

    PubMed  Article  CAS  Google Scholar 

  33. Costell M, Gustafsson E, Aszodi A, Morgelin M, Bloch W, Hunziker E et al (1999) Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 147:1109–1122

    PubMed  Article  CAS  Google Scholar 

  34. Moers A, Nurnberg A, Goebbels S, Wettschureck N, Offermanns S (2008) Galpha12/Galpha13 deficiency causes localized overmigration of neurons in the developing cerebral and cerebellar cortices. Mol Cell Biol 28:1480–1488. doi:10.1128/MCB.00651-07

    PubMed  Article  CAS  Google Scholar 

  35. Kwiatkowski AV, Rubinson DA, Dent EW, Edward van Veen J, Leslie JD, Zhang J et al (2007) Ena/VASP is required for neuritogenesis in the developing cortex. Neuron 56:441–455. doi:10.1016/j.neuron.2007.09.008

    PubMed  Article  CAS  Google Scholar 

  36. Sarkisian MR, Bartley CM, Chi H, Nakamura F, Hashimoto-Torii K, Torii M et al (2006) MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 52:789–801. doi:10.1016/j.neuron.2006.10.024

    PubMed  Article  CAS  Google Scholar 

  37. Jaglin XH, Poirier K, Saillour Y, Buhler E, Tian G, Bahi-Buisson N et al (2009) Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat Genet 41:746–752. doi:10.1038/ng.380

    PubMed  Article  CAS  Google Scholar 

  38. Yang L, Chen G, Mohanty S, Scott G, Fazal F, Rahman A et al (2011) GPR56 regulates VEGF production and angiogenesis during melanoma progression. Cancer Res 71(16):5558–5568. doi:10.1158/0008-5472.CAN-10-4543

    PubMed  Article  CAS  Google Scholar 

  39. Luo R, Jin Z, Deng Y, Strokes N, Piao X (2012) Disease-associated mutations prevent GPR56–collagen III interaction. PLoS One 7:e29818. doi:10.1371/journal.pone.0029818

    PubMed  Article  CAS  Google Scholar 

  40. Shashidhar S, Lorente G, Nagavarapu U, Nelson A, Kuo J, Cummins J et al (2005) GPR56 is a GPCR that is overexpressed in gliomas and functions in tumor cell adhesion. Oncogene 24:1673–1682

    PubMed  Article  CAS  Google Scholar 

  41. Xu L, Begum S, Hearn JD, Hynes RO (2006) GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci U S A 103:9023–9028

    PubMed  Article  CAS  Google Scholar 

  42. Jin Z, Tietjen I, Bu L, Liu-Yesucevitz L, Gaur SK, Walsh CA et al (2007) Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum Mol Genet 16:1972–1985

    PubMed  Article  CAS  Google Scholar 

  43. Lin HH, Stacey M, Yona S, Chang GW (2010) GPS proteolytic cleavage of adhesion-GPCRs. Adv Exp Med Biol 706:49–58

    PubMed  Article  CAS  Google Scholar 

  44. Volynski KE, Silva JP, Lelianova VG, Atiqur Rahman M, Hopkins C, Ushkaryov YA (2004) Latrophilin fragments behave as independent proteins that associate and signal on binding of LTX(N4C). EMBO J 23:4423–4433. doi:10.1038/sj.emboj.7600443

    PubMed  Article  CAS  Google Scholar 

  45. Fredriksson R, Lagerstrom MC, Hoglund PJ, Schioth HB (2002) Novel human G protein-coupled receptors with long N-terminals containing GPS domains and Ser/Thr-rich regions. FEBS Lett 531:407–414

    PubMed  Article  CAS  Google Scholar 

  46. Bjarnadottir TK, Fredriksson R, Hoglund PJ, Gloriam DE, Lagerstrom MC, Schioth HB (2004) The human and mouse repertoire of the adhesion family of G-protein-coupled receptors. Genomics 84:23–33

    PubMed  Article  CAS  Google Scholar 

  47. Qian F, Boletta A, Bhunia AK, Xu H, Liu L, Ahrabi AK et al (2002) Cleavage of polycystin-1 requires the receptor for egg jelly domain and is disrupted by human autosomal-dominant polycystic kidney disease 1-associated mutations. Proc Natl Acad Sci U S A 99:16981–16986

    PubMed  Article  CAS  Google Scholar 

  48. Mengerink KJ, Moy GW, Vacquier VD (2002) suREJ3, a polycystin-1 protein, is cleaved at the GPS domain and localizes to the acrosomal region of sea urchin sperm. J Biol Chem 277:943–948. doi:10.1074/jbc.M109673200M109673200

    PubMed  Article  CAS  Google Scholar 

  49. Arac D, Boucard AA, Bolliger MF, Nguyen J, Soltis SM, Sudhof TC et al (2012) A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. EMBO J 31:1364–1378. doi:10.1038/emboj.2012.26emboj201226

    PubMed  Article  CAS  Google Scholar 

  50. Chiang NY, Hsiao CC, Huang YS, Chen HY, Hsieh IJ, Chang GW et al (2011) Disease-associated GPR56 mutations cause bilateral frontoparietal polymicrogyria via multiple mechanisms. J Biol Chem 286:14215–14225. doi:10.1074/jbc.M110.183830

    PubMed  Article  CAS  Google Scholar 

  51. Boscher C, Dennis JW, Nabi IR (2011) Glycosylation, galectins and cellular signaling. Curr Opin Cell Biol 23:383–392. doi:10.1016/j.ceb.2011.05.001

    PubMed  Article  CAS  Google Scholar 

  52. Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27:534–539

    PubMed  Article  CAS  Google Scholar 

  53. Gaudry CA, Verderio E, Aeschlimann D, Cox A, Smith C, Griffin M (1999) Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal beta-sandwich domain. J Biol Chem 274:30707–30714

    PubMed  Article  CAS  Google Scholar 

  54. Telci D, Wang Z, Li X, Verderio EA, Humphries MJ, Baccarini M et al (2008) Fibronectin-tissue transglutaminase matrix rescues RGD-impaired cell adhesion through syndecan-4 and beta1 integrin co-signaling. J Biol Chem 283:20937–20947. doi:10.1074/jbc.M801763200

    PubMed  Article  CAS  Google Scholar 

  55. De Laurenzi V, Melino G (2001) Gene disruption of tissue transglutaminase. Mol Cell Biol 21:148–155. doi:10.1128/MCB.21.1.148-155.2001

    PubMed  Article  Google Scholar 

  56. Maggio N, Sellitti S, Capano CP, Papa M (2001) Tissue-transglutaminase in rat and human brain: light and electron immunocytochemical analysis and in situ hybridization study. Brain Res Bull 56:173–182

    PubMed  Article  CAS  Google Scholar 

  57. Bailey CD, Johnson GV (2004) Developmental regulation of tissue transglutaminase in the mouse forebrain. J Neurochem 91:1369–1379. doi:10.1111/j.1471-4159.2004.02825.x

    PubMed  Article  CAS  Google Scholar 

  58. Luo R, Jeong SJ, Jin Z, Strokes N, Li S, Piao X (2011) G protein-coupled receptor 56 and collagen III, a receptor–ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci U S A 108(31):12925–12930. doi:10.1073/pnas.1104821108

    PubMed  Article  CAS  Google Scholar 

  59. Jeong SJ, Li S, Luo R, Strokes N, Piao X (2012) Loss of Col3a1, the gene for Ehlers–Danlos syndrome type IV, results in neocortical dyslamination. PLoS One 7:e29767. doi:10.1371/journal.pone.0029767

    PubMed  Article  CAS  Google Scholar 

  60. Kim JK, Xu Y, Xu X, Keene DR, Gurusiddappa S, Liang X et al (2005) A novel binding site in collagen type III for integrins alpha1beta1 and alpha2beta1. J Biol Chem 280:32512–32520. doi:10.1074/jbc.M502431200

    PubMed  Article  CAS  Google Scholar 

  61. Nykvist P, Tu H, Ivaska J, Kapyla J, Pihlajaniemi T, Heino J (2000) Distinct recognition of collagen subtypes by alpha(1)beta(1) and alpha(2)beta(1) integrins. Alpha(1)beta(1) mediates cell adhesion to type XIII collagen. J Biol Chem 275:8255–8261

    PubMed  Article  CAS  Google Scholar 

  62. Germain DP (2007) Ehlers–Danlos syndrome type IV. Orphanet J Rare Dis 2:32. doi:10.1186/1750-1172-2-32

    PubMed  Article  Google Scholar 

  63. Kontusaari S, Tromp G, Kuivaniemi H, Romanic AM, Prockop DJ (1990) A mutation in the gene for type III procollagen (COL3A1) in a family with aortic aneurysms. J Clin Invest 86:1465–1473. doi:10.1172/JCI114863

    PubMed  Article  CAS  Google Scholar 

  64. Kuivaniemi H, Tromp G, Bergfeld WF, Kay M, Helm TN (1995) Ehlers–Danlos syndrome type IV: a single base substitution of the last nucleotide of exon 34 in COL3A1 leads to exon skipping. J Invest Dermatol 105:352–356

    PubMed  Article  CAS  Google Scholar 

  65. Pope FM, Martin GR, Lichtenstein JR, Penttinen R, Gerson B, Rowe DW et al (1975) Patients with Ehlers–Danlos syndrome type IV lack type III collagen. Proc Natl Acad Sci U S A 72:1314–1316

    PubMed  Article  CAS  Google Scholar 

  66. Prockop DJ, Kivirikko KI (1984) Heritable diseases of collagen. N Engl J Med 311:376–386. doi:10.1056/NEJM198408093110606

    PubMed  Article  CAS  Google Scholar 

  67. Schwarze U, Schievink WI, Petty E, Jaff MR, Babovic-Vuksanovic D, Cherry KJ et al (2001) Haploinsufficiency for one COL3A1 allele of type III procollagen results in a phenotype similar to the vascular form of Ehlers–Danlos syndrome, Ehlers–Danlos syndrome type IV. Am J Hum Genet 69:989–1001. doi:10.1086/324123

    PubMed  Article  CAS  Google Scholar 

  68. Plancke A, Holder-Espinasse M, Rigau V, Manouvrier S, Claustres M, Khau Van Kien P (2009) Homozygosity for a null allele of COL3A1 results in recessive Ehlers–Danlos syndrome. Eur J Hum Genet 17:1411–1416. doi:10.1038/ejhg.2009.76

    PubMed  Article  Google Scholar 

  69. Semeralul MO, Boutros PC, Likhodi O, Okey AB, Van Tol HH, Wong AH (2006) Microarray analysis of the developing cortex. J Neurobiol 66:1646–1658. doi:10.1002/neu.20302

    PubMed  Article  CAS  Google Scholar 

  70. Narumiya S, Tanji M, Ishizaki T (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 28:65–76. doi:10.1007/s10555-008-9170-7

    PubMed  Article  CAS  Google Scholar 

  71. Iguchi T, Sakata K, Yoshizaki K, Tago K, Mizuno N, Itoh H (2008) Orphan G protein-coupled receptor GPR56 regulates neural progenitor cell migration via a G alpha 12/13 and Rho pathway. J Biol Chem 283:14469–14478

    PubMed  Article  CAS  Google Scholar 

  72. Worzfeld T, Wettschureck N, Offermanns S (2008) G(12)/G(13)-mediated signalling in mammalian physiology and disease. Trends Pharmacol Sci 29:582–589. doi:10.1016/j.tips.2008.08.002

    PubMed  Article  CAS  Google Scholar 

  73. Paavola KJ, Stephenson JR, Ritter SL, Alter SP, Hall RA (2011) The N terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity. J Biol Chem 286:28914–28921. doi:10.1074/jbc.M111.247973

    PubMed  Article  CAS  Google Scholar 

  74. Caviness VS Jr (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res 256:293–302

    PubMed  Google Scholar 

  75. Del Rio JA, Martinez A, Auladell C, Soriano E (2000) Developmental history of the subplate and developing white matter in the murine neocortex. Neuronal organization and relationship with the main afferent systems at embryonic and perinatal stages. Cereb Cortex 10:784–801

    PubMed  Article  Google Scholar 

  76. Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C (2003) Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25:139–151. doi:10.1159/00007226372263

    PubMed  Article  CAS  Google Scholar 

  77. Wood JG, Martin S, Price DJ (1992) Evidence that the earliest generated cells of the murine cerebral cortex form a transient population in the subplate and marginal zone. Brain Res Dev Brain Res 66:137–140

    PubMed  Article  CAS  Google Scholar 

  78. Sheppard AM, Pearlman AL (1997) Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J Comp Neurol 378:173–179. doi:10.1002/(SICI)1096-9861(19970210)378:2<173::AID-CNE2>3.0.CO;2-0

    PubMed  Article  CAS  Google Scholar 

  79. Nichols AJ, Olson EC (2010) Reelin promotes neuronal orientation and dendritogenesis during preplate splitting. Cereb Cortex 20:2213–2223. doi:10.1093/cercor/bhp303

    PubMed  Article  Google Scholar 

  80. Schneider S, Gulacsi A, Hatten ME (2011) Lrp12/Mig13a reveals changing patterns of preplate neuronal polarity during corticogenesis that are absent in reeler mutant mice. Cereb Cortex 21:134–144. doi:10.1093/cercor/bhq070

    PubMed  Article  Google Scholar 

  81. Little KD, Hemler ME, Stipp CS (2004) Dynamic regulation of a GPCR–tetraspanin–G protein complex on intact cells: central role of CD81 in facilitating GPR56-Galpha q/11 association. Mol Biol Cell 15:2375–2387

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported in part by NINDS grant RO1 NS057536 (X.P.), the William Randolph Hearst Fund Award (S.J. and R.L.), the Leonard and Isabelle Goldenson Research Fellowship (R.L.), and the NIH Training Grant 5T32HD7466-15 (S.J.).

Author information

Affiliations

  1. Division of Newborn Medicine, Department of Medicine, Boston Children’s Hospital and Harvard Medical School, 300 Longwood Avenue, Boston, MA, 02115, USA

    Kathleen Singer, Rong Luo, Sung-Jin Jeong & Xianhua Piao

Authors
  1. Kathleen Singer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sung-Jin Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianhua Piao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xianhua Piao.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Singer, K., Luo, R., Jeong, SJ. et al. GPR56 and the Developing Cerebral Cortex: Cells, Matrix, and Neuronal Migration. Mol Neurobiol 47, 186–196 (2013). https://doi.org/10.1007/s12035-012-8343-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-012-8343-0

Keywords

  • Adhesion G protein-coupled receptor
  • GPR56
  • Bilateral frontoparietal polymicrogyria
  • Extracellular matrix
  • Neuronal migration