Dissecting signaling and functions of adhesion G protein–coupled receptors
Gabriela Aust
Department of Surgery, Research Laboratories, University of Leipzig, Leipzig, Germany
Search for more papers by this authorDavide Calebiro
Institute of Pharmacology and Rudolf Virchow Center, DFG-Research Center for Experimental Biomedicine, University of Würzburg, Würzburg, Germany
Search for more papers by this authorFelix B. Engel
Department of Cardiac Development and Remodelling, Max-Planck-Institute for Heart and Lung Research, Bad Nauheim, Germany, and Laboratory of Experimental Renal and Cardiovascular Research, Department of Nephropathology, Institute of Pathology, University of Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorCaroline Formstone
MRC Centre for Developmental Neurobiology, King's College London, New Hunts House, London, United Kingdom
Search for more papers by this authorAndré Goffinet
Université Catholique de Louvain, Institute of Neuroscience, Developmental Neurobiology, Brussels, Belgium
Search for more papers by this authorJörg Hamann
Department of Experimental Immunology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Search for more papers by this authorRobert J. Kittel
Institute of Physiology, Department of Neurophysiology, University of Würzburg, Würzburg, Germany
Search for more papers by this authorInes Liebscher
Institute of Biochemistry, Molecular Biochemistry, Medical Faculty, University of Leipzig, Leipzig, Germany
Search for more papers by this authorHsi-Hsien Lin
Department of Microbiology and Immunology, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan
Search for more papers by this authorKelly R. Monk
Department of Developmental Biology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorAlexander Petrenko
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russia
Search for more papers by this authorXianhua Piao
Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital and Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorSimone Prömel
Institute of Biochemistry, Molecular Biochemistry, Medical Faculty, University of Leipzig, Leipzig, Germany
Search for more papers by this authorHelgi B. Schiöth
Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden
Search for more papers by this authorThue W. Schwartz
Laboratory for Molecular Pharmacology, Department of Neuroscience and Pharmacology, and the Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorMartin Stacey
Faculty of Biological Sciences, University of Leeds, Leeds, United Kingdom
Search for more papers by this authorYuri A. Ushkaryov
Division of Cell and Molecular Biology, Imperial College London, London, United Kingdom, and Medway School of Pharmacy, University of Kent, Chatham, United Kingdom
Search for more papers by this authorManja Wobus
Medical Clinic and Policlinic I, University Hospital Carl Gustav Carus, Dresden, Germany
Search for more papers by this authorUwe Wolfrum
Cell and Matrix Biology, Institute of Zoology, Johannes Gutenberg University of Mainz, Mainz, Germany
Search for more papers by this authorLei Xu
University of Rochester Medical Center, Rochester, New York
Search for more papers by this authorTobias Langenhan
Institute of Physiology, Department of Neurophysiology, University of Würzburg, Würzburg, Germany
Search for more papers by this authorGabriela Aust
Department of Surgery, Research Laboratories, University of Leipzig, Leipzig, Germany
Search for more papers by this authorDavide Calebiro
Institute of Pharmacology and Rudolf Virchow Center, DFG-Research Center for Experimental Biomedicine, University of Würzburg, Würzburg, Germany
Search for more papers by this authorFelix B. Engel
Department of Cardiac Development and Remodelling, Max-Planck-Institute for Heart and Lung Research, Bad Nauheim, Germany, and Laboratory of Experimental Renal and Cardiovascular Research, Department of Nephropathology, Institute of Pathology, University of Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorCaroline Formstone
MRC Centre for Developmental Neurobiology, King's College London, New Hunts House, London, United Kingdom
Search for more papers by this authorAndré Goffinet
Université Catholique de Louvain, Institute of Neuroscience, Developmental Neurobiology, Brussels, Belgium
Search for more papers by this authorJörg Hamann
Department of Experimental Immunology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Search for more papers by this authorRobert J. Kittel
Institute of Physiology, Department of Neurophysiology, University of Würzburg, Würzburg, Germany
Search for more papers by this authorInes Liebscher
Institute of Biochemistry, Molecular Biochemistry, Medical Faculty, University of Leipzig, Leipzig, Germany
Search for more papers by this authorHsi-Hsien Lin
Department of Microbiology and Immunology, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan
Search for more papers by this authorKelly R. Monk
Department of Developmental Biology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorAlexander Petrenko
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russia
Search for more papers by this authorXianhua Piao
Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital and Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorSimone Prömel
Institute of Biochemistry, Molecular Biochemistry, Medical Faculty, University of Leipzig, Leipzig, Germany
Search for more papers by this authorHelgi B. Schiöth
Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden
Search for more papers by this authorThue W. Schwartz
Laboratory for Molecular Pharmacology, Department of Neuroscience and Pharmacology, and the Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorMartin Stacey
Faculty of Biological Sciences, University of Leeds, Leeds, United Kingdom
Search for more papers by this authorYuri A. Ushkaryov
Division of Cell and Molecular Biology, Imperial College London, London, United Kingdom, and Medway School of Pharmacy, University of Kent, Chatham, United Kingdom
Search for more papers by this authorManja Wobus
Medical Clinic and Policlinic I, University Hospital Carl Gustav Carus, Dresden, Germany
Search for more papers by this authorUwe Wolfrum
Cell and Matrix Biology, Institute of Zoology, Johannes Gutenberg University of Mainz, Mainz, Germany
Search for more papers by this authorLei Xu
University of Rochester Medical Center, Rochester, New York
Search for more papers by this authorTobias Langenhan
Institute of Physiology, Department of Neurophysiology, University of Würzburg, Würzburg, Germany
Search for more papers by this authorAbstract
G protein–coupled receptors (GPCRs) comprise an expanded superfamily of receptors in the human genome. Adhesion class G protein–coupled receptors (adhesion-GPCRs) form the second largest class of GPCRs. Despite the abundance, size, molecular structure, and functions in facilitating cell and matrix contacts in a variety of organ systems, adhesion-GPCRs are by far the most poorly understood GPCR class. Adhesion-GPCRs possess a unique molecular structure, with extended N-termini containing various adhesion domains. In addition, many adhesion-GPCRs are autoproteolytically cleaved into an N-terminal fragment (NTF, NT, α-subunit) and C-terminal fragment (CTF, CT, β-subunit) at a conserved GPCR autoproteolysis–inducing (GAIN) domain that contains a GPCR proteolysis site (GPS). These two features distinguish adhesion-GPCRs from other GPCR classes. Though active research on adhesion-GPCRs in diverse areas, such as immunity, neuroscience, and development and tumor biology has been intensified in the recent years, the general biological and pharmacological properties of adhesion-GPCRs are not well known, and they have not yet been used for biomedical purposes. The “6th International Adhesion-GPCR Workshop,” held at the Institute of Physiology of the University of Würzburg on September 6–8, 2012, assembled a majority of the investigators currently actively pursuing research on adhesion-GPCRs, including scientists from laboratories in Europe, the United States, and Asia. The meeting featured the nascent mechanistic understanding of the molecular events driving the signal transduction of adhesion-GPCRs, novel models to evaluate their functions, and evidence for their involvement in human disease.
References
- 1
Yona, S.,
H.-H. Lin,
W.O. Siu,
et al
. 2008. Adhesion-GPCRs: emerging roles for novel receptors.
Trends Biochem. Sci.
33: 491–500.
- 2
Kwakkenbos, M.J.,
E.N. Kop,
M. Stacey,
et al
. 2004. The EGF-TM7 family: a postgenomic view.
Immunogenetics
55: 655–666.
- 3
Nordström, K.J.V.,
M. Sällman Almén,
M.M. Edstam,
et al
. 2011. Independent HHsearch, Needleman–Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families.
Mol. Biol. Evol.
28: 2471–2480.
- 4
Nordström, K.J.V.,
R. Fredriksson &
H.B. Schiöth. 2008. The amphioxus (Branchiostoma floridae) genome contains a highly diversified set of G protein-coupled receptors.
BMC Evol. Biol.
8: 9.
- 5
Kamesh, N.,
G.K. Aradhyam &
N. Manoj. 2008. The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis.
BMC Evol. Biol.
8: 129.
- 6
Whittaker, C.A.,
K.-F. Bergeron,
J. Whittle,
et al
. 2006. The echinoderm adhesome.
Dev. Biol.
300: 252–266.
- 7
Nordström, K.J.V.,
M.C. Lagerström,
L.M.J. Wallér,
et al.
2009. The secretin GPCRs descended from the family of adhesion GPCRs.
Mol. Biol. Evol.
26: 71–84.
- 8
Krishnan, A.,
M.S. Almén,
R. Fredriksson &
H.B. Schiöth. 2012. The origin of GPCRs: identification of mammalian like rhodopsin, adhesion, glutamate and frizzled GPCRs in fungi.
PLoS ONE
7: e29817.
- 9
Krasnoperov, V.,
M.A. Bittner,
R.W. Holz,
et al
. 1999. Structural requirements for alpha-latrotoxin binding and alpha-latrotoxin-stimulated secretion. A study with calcium-independent receptor of alpha-latrotoxin (CIRL) deletion mutants.
J. Biol. Chem.
274: 3590–3596.
- 10
Lin, H.-H.,
G.-W. Chang,
J.Q. Davies,
et al
. 2004. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif.
J. Biol. Chem.
279: 31823–31832.
- 11
Volynski, K.E.,
J.-P. Silva,
V.G. Lelianova,
et al
. 2004. Latrophilin fragments behave as independent proteins that associate and signal on binding of LTX(N4C).
EMBO J.
23: 4423–4433.
- 12
Araç, D.,
A.A. Boucard,
M.F. Bolliger,
et al
. 2012. A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis.
EMBO J.
31: 1364–1378.
- 13
Paavola, K.J.,
J.R. Stephenson,
S.L. Ritter,
et al
. 2011. The N terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity.
J. Biol. Chem.
286: 28914–28921.
- 14
Krasnoperov, V.G.,
R. Beavis,
O.G. Chepurny,
et al
. 1996. The calcium-independent receptor of alpha-latrotoxin is not a neurexin.
Biochem. Biophys. Res. Commun.
227: 868–875.
- 15
Krasnoperov, V.G.,
M.A. Bittner,
R. Beavis,
et al
. 1997. alpha-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor.
Neuron
18: 925–937.
- 16
Langenhan, T.,
S. Prömel,
L. Mestek,
et al
. 2009. Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo.
Dev. Cell
17: 494–504.
- 17
Prömel, S.,
M. Frickenhaus,
S. Hughes,
et al
. 2012. The GPS motif is a molecular switch for bimodal activities of adhesion class G protein-coupled receptors.
Cell Reports
2: 321–331.
- 18
Okajima, D.,
G. Kudo &
H. Yokota. 2010. Brain-specific angiogenesis inhibitor 2 (BAI2) may be activated by proteolytic processing.
J. Recept. Signal Transduct. Res.
30: 143–153.
- 19
Silva, J.-P.,
V. Lelianova,
C. Hopkins,
et al
. 2009. Functional cross-interaction of the fragments produced by the cleavage of distinct adhesion G-protein-coupled receptors.
J. Biol. Chem.
284: 6495–6506.
- 20
Iguchi, T.,
K. Sakata,
K. Yoshizaki,
et al
. 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.
- 21
Park, D.,
A.-C. Tosello-Trampont,
M.R. Elliott,
et al
. 2007. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module.
Nature
450: 430–434.
- 22
Bohnekamp, J. &
T. Schöneberg. 2011. Cell adhesion receptor GPR133 couples to Gs protein.
J. Biol. Chem.
286: 41912–41916.
- 23
Gupte, J.,
G. Swaminath,
J. Danao,
et al
. 2012. Signaling property study of adhesion G-protein-coupled receptors.
FEBS Lett.
586: 1214–1219.
- 24
Engelstoft, M.S.,
K.L. Egerod,
B. Holst &
T.W. Schwartz. 2008. A gut feeling for obesity: 7TM sensors on enteroendocrine cells.
Cell Metab.
8: 447–449.
- 25
Hansen, H.S.,
M.M. Rosenkilde,
J.J. Holst &
T.W. Schwartz. 2012. GPR119 as a fat sensor.
Trends Pharmacol. Sci.
33: 374–381.
- 26
Egerod, K.L.,
M.S. Engelstoft,
K.V. Grunddal,
et al
.
A major lineage of enteroendocrine cells co-express CCK, GLP-1, GIP, PYY, neurotensin, and secretin but not somatostatin.
Endocrinology
. In press.
- 27
Yang, L.,
G. Chen,
S. Mohanty,
et al
. 2011. GPR56 regulates VEGF production and angiogenesis during melanoma progression.
Cancer Res.
71: 5558–5568.
- 28
Hamann, J.,
B. Vogel,
G.M. van Schijndel &
R.A. van Lier. 1996. The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF).
J. Exp. Med.
184: 1185–1189.
- 29
Veninga, H.,
R.M. Hoek,
A.F. de Vos,
et al
. 2011. A novel role for CD55 in granulocyte homeostasis and anti-bacterial host defense.
PLoS ONE
6: e24431.
- 30
Hoek, R.M.,
D. de Launay,
E.N. Kop,
et al
. 2010. Deletion of either CD55 or CD97 ameliorates arthritis in mouse models.
Arthritis. Rheum.
62: 1036–1042.
- 31
Ward, Y.,
R. Lake,
J.J. Yin,
et al
. 2011. LPA receptor heterodimerizes with CD97 to amplify LPA-initiated RHO-dependent signaling and invasion in prostate cancer cells.
Cancer Res.
71: 7301–7311.
- 32
Chen, T.-Y.,
T.-L. Hwang,
C.-Y. Lin,
et al
. 2011. EMR2 receptor ligation modulates cytokine secretion profiles and cell survival of lipopolysaccharide-treated neutrophils.
Chang Gung Med. J.
34: 468–477.
- 33
Yona, S.,
H.-H. Lin,
P. Dri,
et al
. 2008. Ligation of the adhesion-GPCR EMR2 regulates human neutrophil function.
FASEB J.
22: 741–751.
- 34
Lin, H.-H.,
M. Stacey,
S. Yona &
G.-W. Chang. 2010. GPS proteolytic cleavage of adhesion-GPCRs.
Adv. Exp. Med. Biol.
706: 49–58.
- 35
Huang, Y.-S.,
N.-Y. Chiang,
C.-H. Hu,
et al
. Lin. 2012. Activation of myeloid cell-specific adhesion class G protein-coupled receptor EMR2 via ligation-induced translocation and interaction of receptor subunits in lipid raft microdomains.
Mol. Cell Biol.
32: 1408–1420.
- 36
Lohse, M.J.,
V.O. Nikolaev,
P. Hein,
et al
. 2008. Optical techniques to analyze real-time activation and signaling of G-protein-coupled receptors.
Trends Pharmacol. Sci.
29: 159–165.
- 37
Calebiro, D.,
V.O. Nikolaev,
M.C. Gagliani,
et al
. 2009. Persistent cAMP-signals triggered by internalized G-protein-coupled receptors.
PLoS Biol.
7: e1000172.
- 38
Nikolaev, V.O.,
M. Bünemann,
L. Hein,
et al
. 2004. Novel single chain cAMP sensors for receptor-induced signal propagation.
J. Biol. Chem.
279: 37215–37218.
- 39
Calebiro, D.,
V.O. Nikolaev,
L. Persani &
M.J. Lohse. 2010. Signaling by internalized G-protein-coupled receptors.
Trends Pharmacol. Sci.
31: 221–228.
- 40
Monk, K.R.,
S.G. Naylor,
T.D. Glenn,
et al
. 2009. A G protein-coupled receptor is essential for Schwann cells to initiate myelination.
Science
325: 1402–1405.
- 41
Monk, K.R.,
K. Oshima,
S. Jörs,
et al
. 2011. Gpr126 is essential for peripheral nerve development and myelination in mammals.
Development
138: 2673–2680.
- 42
Waller-Evans, H.,
S. Prömel,
T. Langenhan,
et al
. 2010. The orphan adhesion-GPCR GPR126 is required for embryonic development in the mouse.
PLoS ONE
5: e14047.
- 43
Stehlik, C.,
R. Kroismayr,
A. Dorfleutner,
et al
. 2004. VIGR—a novel inducible adhesion family G-protein coupled receptor in endothelial cells.
FEBS Lett.
569: 149–155.
- 44
Moriguchi, T.,
K. Haraguchi,
N. Ueda,
et al
. 2004. DREG, a developmentally regulated G protein-coupled receptor containing two conserved proteolytic cleavage sites.
Genes Cells
9: 549–560.
- 45
Tissir, F.,
I. Bar,
Y. Jossin,
et al
. 2005. Protocadherin Celsr3 is crucial in axonal tract development.
Nat. Neurosci.
8: 451–457.
- 46
Tissir, F.,
Y. Qu,
M. Montcouquiol,
et al
. 2010. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus.
Nat. Neurosci.
13: 700–707.
- 47
Qu, Y.,
D.M. Glasco,
L. Zhou,
et al
. 2010. Atypical cadherins Celsr1–3 differentially regulate migration of facial branchiomotor neurons in mice.
J. Neurosci.
30: 9392–9401.
- 48
Song, H.,
J. Hu,
W. Chen,
et al
. 2010. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning.
Nature
466: 378–382
- 49
Curtin, J.A.,
E. Quint,
V. Tsipouri,
et al
. 2003. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse.
Curr. Biol.
13: 1129–1133.
- 50
Yates, L.L.,
C. Schnatwinkel,
J.N. Murdoch,
et al
. 2010. The PCP genes Celsr1 and Vangl2 are required for normal lung branching morphogenesis.
Hum Mol Genet
19: 2251–2267.
- 51
Devenport, D.,
D. Oristian,
E. Heller &
E. Fuchs. 2011. Mitotic internalization of planar cell polarity proteins preserves tissue polarity.
Nat. Cell Biol.
13: 893–902.
- 52
Formstone, C.J.,
C. Moxon,
J. Murdoch,
et al
. 2010. Basal enrichment within neuroepithelia suggests novel function(s) for Celsr1 protein.
Mol. Cell. Neurosci.
44: 210–222.
- 53
Yates, L.L.,
C. Schnatwinkel,
L. Hazelwood,
et al
.
Scribble is required for normal epithelial cell-cell contacts and lumen morphogenesis in the mammalian lung.
Dev Biol
. In press.
- 54
Becker, S.,
E. Wandel,
M. Wobus,
et al
. 2010. Overexpression of CD97 in intestinal epithelial cells of transgenic mice attenuates colitis by strengthening adherens junctions.
PLoS ONE
5: e8507.
- 55
Cummins, A.G. &
F.M. Thompson. 2002. Effect of breast milk and weaning on epithelial growth of the small intestine in humans.
Gut
51: 748–754.
- 56
Tobaben, S.,
T.C. Südhof &
B. Stahl. 2002. Genetic analysis of alpha-latrotoxin receptors reveals functional interdependence of CIRL/latrophilin 1 and neurexin 1 alpha.
J. Biol. Chem.
277: 6359–6365.
- 57
Davletov, B.A.,
O.G. Shamotienko,
V.G. Lelianova,
et al
. 1996. Isolation and biochemical characterization of a Ca2+-independent alpha-latrotoxin-binding protein.
J. Biol. Chem.
271: 23239–23245.
- 58
Davletov, B.A.,
F.A. Meunier,
A.C. Ashton,
et al
. 1998. Vesicle exocytosis stimulated by alpha-latrotoxin is mediated by latrophilin and requires both external and stored Ca2.
EMBO J.
17: 3909–3920.
- 59
Silva, J.-P. &
Y.A. Ushkaryov. 2010. The latrophilins, “split-personality” receptors.
Adv. Exp. Med. Biol.
706: 59–75.
- 60
Silva, J.-P.,
V.G. Lelianova,
Y.S. Ermolyuk,
et al
. 2011. Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities.
Proc. Natl. Acad. Sci. USA
108: 12113–12118.
- 61
Silva, J.P.,
N. Vysokov,
G.V. Lelianova,
et al
.
Interaction between latrophilin-1 and Lasso is required for functional maturation of synapses. Manuscript in preparation.
- 62
McMillan, D.R. &
P.C. White. 2010. Studies on the very large G protein-coupled receptor: from initial discovery to determining its role in sensorineural deafness in higher animals.
Adv. Exp. Med. Biol.
706: 76–86.
- 63
McGee, J.,
R.J. Goodyear,
D.R. McMillan,
et al
. 2006. 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.
26: 6543–6553.
- 64
Maerker, T.,
E. van Wijk,
N. Overlack,
et al
. 2008. A novel Usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells.
Hum. Mol. Genet.
17: 71–86.
- 65
Wolfrum, U.
2011. Protein networks related to the Usher syndrome gain insights in the molecular basis of the disease. In
Usher Syndrome: Pathogenesis, Diagnosis and Therapy . S.A.
Ed.: 51–73. Nova Science Publishers, Inc.
Hauppauge
,
NY
.
- 66
Reiners, J.,
E. van Wijk,
T. Märker,
et al
. 2005. Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and type 2.
Hum. Mol. Genet.
14: 3933–3943.
- 67
Piao, X.,
B.S. Chang,
A. Bodell,
et al
. 2005. Genotype-phenotype analysis of human frontoparietal polymicrogyria syndromes.
Ann. Neurol.
58: 680–687.
- 68
Piao, X.,
R.S. Hill,
A. Bodell,
et al
. 2004. G protein-coupled receptor-dependent development of human frontal cortex.
Science
303: 2033–2036.
- 69
Luo, R.,
S.-J. Jeong,
Z. Jin,
et al
. 2011. G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination.
Proc. Natl. Acad. Sci. USA
108: 12925–12930.
- 70
Li, S.,
Z. Jin,
S. Koirala,
et al
. 2008. GPR56 regulates pial basement membrane integrity and cortical lamination.
J. Neurosci.
28: 5817–5826.
- 71
Jeong, S.-J.,
S. Li,
R. Luo,
et al
. 2012. Loss of Col3a1, the gene for Ehlers-Danlos syndrome type IV, results in neocortical dyslamination.
PLoS ONE
7: e29767.
- 72
Jeong, S.-J.,
R. Luo,
S. Li,
et al
. 2012. Characterization of G protein-coupled receptor 56 protein expression in the mouse developing neocortex.
J. Comp. Neurol.
520: 2930–2940.
- 73
Xu, L.,
S. Begum,
J.D. Hearn &
R.O. Hynes. 2006. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis.
Proc. Natl. Acad. Sci. USA
103: 9023–9028.
- 74
Lorand, L. &
R.M. Graham. 2003. Transglutaminases: crosslinking enzymes with pleiotropic functions.
Nat. Rev. Mol. Cell Biol.
4: 140–156.
- 75
Belkin, A.M.
2011. Extracellular TG2: emerging functions and regulation.
FEBS J.
278: 4704–4716.
- 76
Davies, J.Q.,
H.-H. Lin,
M. Stacey,
et al
. 2011. Leukocyte adhesion-GPCR EMR2 is aberrantly expressed in human breast carcinomas and is associated with patient survival.
Oncol. Rep.
25: 619–627.
- 77
Becker, P.S.
2012. Dependence of acute myeloid leukemia on adhesion within the bone marrow microenvironment.
The Scientific World Journal
2012: 856467.
- 78
van Pel, M.,
H. Hagoort,
J. Hamann &
W.E. Fibbe. 2008. CD97 is differentially expressed on murine hematopoietic stem-and progenitor-cells.
Haematologica
93: 1137–1144.
- 79
Wandel, E.,
A. Saalbach,
D. Sittig,
et al
. 2012. Thy-1 (CD90) is an interacting partner for CD97 on activated endothelial cells.
J. Immunol.
188: 1442–1450.
- 80
Kiyoi, H. &
T. Naoe. 2006. Biology, clinical relevance, and molecularly targeted therapy in acute leukemia with FLT3 mutation.
Int. J. Hematol.
83: 301–308.