Heart development, angiogenesis, and blood-brain barrier function is modulated by adhesion GPCRs

Handbook of Experimental Pharmacology

Volumn 234, Issue , 2016, Pages 351-368

  Musa, Gentian ^a   Engel, Felix B ^a   Niaudet, Colin ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Adhesion GPCRs; Angiogenesis; Blood brain barrier; Cardiovascular; Endothelium; Heart development; Trabeculation

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PROTEIN BINDING;

ANGIOGENESIS; BLOOD BRAIN BARRIER; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL MATURATION; ENDOTHELIUM; EXTRACELLULAR MATRIX; HEART DEVELOPMENT; HUMAN; LIGAND BINDING; MYELINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; VASCULARIZATION; ANIMAL; BINDING SITE; CELL ADHESION; CELL MEMBRANE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ANIMALS; BINDING SITES; BLOOD-BRAIN BARRIER; CELL ADHESION; CELL MEMBRANE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HUMANS; MODELS, MOLECULAR; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84995495611     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-319-41523-9_16     Document Type: Chapter

References (86)

1. High FA, Epstein JA (2008) The multifaceted role of Notch in cardiac development and disease. Nat Rev Genet 9:49-61
2. Pérez-Pomares JM, González-Rosa JM, Muñoz-Chápuli R (2009) Building the vertebrate heart-an evolutionary approach to cardiac development. Int J Dev Biol 53:1427-1443
3. von Gise A, Pu WT (2012) Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ Res 110:1628-1645
4. Samsa LA, Yang B, Liu J (2013) Embryonic cardiac chamber maturation: trabeculation, conduction, and cardiomyocyte proliferation. Am J Med Genet C Semin Med Genet 163C:157-168
5. Ferrand N, Pessah M, Frayon S, Marais J, Garel JM (1999) Olfactory receptors, Golf alpha and adenylyl cyclase mRNA expressions in the rat heart during ontogenic development. J Mol Cell Cardiol 31:1137-1142
6. Doyle SE, Scholz MJ, Greer KA, Hubbard AD, Darnell DK, Antin PB et al (2006) Latrophilin-2 is a novel component of the epithelial-mesenchymal transition within the atrioventricular canal of the embryonic chicken heart. Dev Dyn 235:3213-3221
7. Nechiporuk T, Urness LD, Keating MT (2001) ETL, a novel seven-transmembrane receptor that is developmentally regulated in the heart. ETL is a member of the secretin family and belongs to the epidermal growth factor-seven-transmembrane subfamily. J Biol Chem 276:4150-4157
8. Xiao J, Jiang H, Zhang R, Fan G, Zhang Y, Jiang D et al (2012) Augmented cardiac hypertrophy in response to pressure overload in mice lacking ELTD 1. PLoS One 7:e35779
9. Veninga H, Becker S, Hoek RM, Wobus M, Wandel E, van der Kaa J et al (2008) Analysis of CD97 expression and manipulation: antibody treatment but not gene targeting curtails granulocyte migration. J Immunol 181:6574-6583
10. Prömel S, Waller-Evans H, Dixon J, Zahn D, Colledge WH, Doran J et al (2012) Characterization and functional study of a cluster of four highly conserved orphan adhesion-GPCR in mouse. Dev Dyn 241:1591-1602
11. Waller-Evans H, Prömel S, Langenhan T, Dixon J, Zahn D, Colledge WH et al (2010) The orphan adhesion-GPCR GPR126 is required for embryonic development in the mouse. PLoS One 5:e14047
12. Patra C, van Amerongen MJ, Ghosh S, Ricciardi F, Sajjad A, Novoyatleva T et al (2013) Organ-specific function of adhesion G protein-coupled receptor GPR126 is domain-dependent. Proc Natl Acad Sci U S A 110:16898-16903
13. Patra C, Monk KR, Engel FB (2014) The multiple signaling modalities of adhesion G proteincoupled receptor GPR126 in development. Recept Clin Investig 1:79
14. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R et al (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378:390-394
15. Lee KF, Simon H, Chen H, Bates B, Hung MC, Hauser C (1995) Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378:394-398
16. Meyer D, Birchmeier C (1995) Multiple essential functions of neuregulin in development. Nature 378:386-390
17. Wang HU, Chen ZF, Anderson DJ (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B 4. Cell 93:741-753
18. Gerety SS, Wang HU, Chen ZF, Anderson DJ (1999) Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 4:403-414
19. Chen H, Shi S, Acosta L, Li W, Lu J, Bao S et al (2004) BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131:2219-2231
20. Grego-Bessa J, Luna-Zurita L, del Monte G, Bolós V, Melgar P, Arandilla A et al (2007) Notch signaling is essential for ventricular chamber development. Dev Cell 12:415-429
21. D’Amato G, Luxán G, Del Monte-Nieto G, Martínez-Poveda B, Torroja C, Walter W et al (2016) Sequential Notch activation regulates ventricular chamber development. Nat Cell Biol 18:7-20
22. Newbern J, Birchmeier C (2010) Nrg1/ErbB signaling networks in Schwann cell development and myelination. Semin Cell Dev Biol 21:922-928
23. Woodhoo A, Alonso MBD, Droggiti A, Turmaine M, D’Antonio M, Parkinson DB et al (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 12:839-847. doi:10.1038/nn.2323
24. Monk KR, Oshima K, Jörs S, Heller S, Talbot WS (2011) Gpr126 is essential for peripheral nerve development and myelination in mammals. Development 138:2673-2680
25. Sigoillot SM, Monk KR, Piao X, Selimi F, Harty BL (2016) Adhesion G protein-coupled receptors in the nervous system: from synapse and dendrite morphogenesis to myelination. In: Langenhan T, Schöneberg T (eds) Adhesion G protein-coupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
26. Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, Calabro A et al (2000) Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 106:349-360
27. Stankunas K, Hang CT, Tsun Z-Y, Chen H, Lee NV, Wu JI et al (2008) Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev Cell 14:298-311
28. Patra C, Diehl F, Ferrazzi F, van Amerongen MJ, Novoyatleva T, Schaefer L et al (2011) Nephronectin regulates atrioventricular canal differentiation via Bmp4-Has2 signaling in zebrafish. Development 138:4499-4509
29. Chernousov MA, Yu W-M, Chen Z-L, Carey DJ, Strickland S (2008) Regulation of Schwann cell function by the extracellular matrix. Glia 56:1498-1507
30. Paavola KJ, Sidik H, Zuchero JB, Eckart M, Talbot WS (2014) Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR 126. Sci Signal 7:ra76
31. Petersen SC, Luo R, Liebscher I, Giera S, Jeong S-J, Mogha A et al (2015) The adhesion GPCR GPR126 has distinct, domain-dependent functions in Schwann cell development mediated by interaction with laminin-211. Neuron 85:755-769
32. Aird WC (2007) Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 100:158-173. doi:10.1161/01.RES.0000255691.76142.4a
33. Aird WC (2012) Endothelial cell heterogeneity. Cold Spring Harb Perspect Med 2:a006429
34. Wallgard E, Larsson E, He L, Hellström M, Armulik A, Nisancioglu MH et al (2008) Identification of a core set of 58 gene transcripts with broad and specific expression in the microvasculature. Arterioscler Thromb Vasc Biol 28:1469-1476
35. Nolan DJ, Ginsberg M, Israely E, Palikuqi B, Poulos MG, James D et al (2013) Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell 26:204-219
36. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O’Keeffe S et al (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34:11929-11947
37. Zeisel A, Muñoz-Manchado AB, Codeluppi S, Lönnerberg P, La Manno G, Juréus A et al (2015) Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347:1138-1142
38. Fukushima Y, Okada M, Kataoka H, Hirashima M, Yoshida Y, Mann F et al (2011) Sema3EPlexinD1 signaling selectively suppresses disoriented angiogenesis in ischemic retinopathy in mice. J Clin Invest 121:1974-1985
39. Durr E, Yu J, Krasinska KM, Carver LA, Yates JR, Testa JE et al (2004) Direct proteomic mapping of the lung microvascular endothelial cell surface in vivo and in cell culture. Nat Biotechnol 22:985-992
40. Valtcheva N, Primorac A, Jurisic G, Hollmén M, Detmar M (2013) The orphan adhesion G protein-coupled receptor GPR97 regulates migration of lymphatic endothelial cells via the small GTPases RhoA and Cdc 42. J Biol Chem 288:35736-35748
41. Liu NM, Yokota T, Maekawa S, Lü P, Zheng Y-W, Tei I et al (2013) Transcription profiles of endothelial cells in the rat ductus arteriosus during a perinatal period. PLoS One 8:e73685
42. Aranguren XL, Agirre X, Beerens M, Coppiello G, Uriz M, Vandersmissen I et al (2013) Unraveling a novel transcription factor code determining the human arterial-specific endothelial cell signature. Blood 122:3982-3992
43. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML et al (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66
44. Wittko-Schneider IM, Schneider FT, Plate KH (2014) Cerebral angiogenesis during development: who is conducting the orchestra? Methods Mol Biol 1135:3-20
45. Raab S, Beck H, Gaumann A, Yüce A, Gerber H-P, Plate K et al (2004) Impaired brain angiogenesis and neuronal apoptosis induced by conditional homozygous inactivation of vascular endothelial growth factor. Thromb Haemost 91:595-605
46. Ben-Zvi A, Lacoste B, Kur E, Andreone BJ, Mayshar Y, Yan H et al (2014) Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature 509:507-511
47. Wälchli T, Mateos JM, Weinman O, Babic D, Regli L, Hoerstrup SP et al (2015) Quantitative assessment of angiogenesis, perfused blood vessels and endothelial tip cells in the postnatal mouse brain. Nat Protoc 10:53-74
48. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N et al (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161:653-660
49. Gaengel K, Niaudet C, Hagikura K, Laviña B, Siemsen BL, Muhl L et al (2012) The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR 2. Dev Cell 23:587-599
50. Kuhnert F, Mancuso MR, Shamloo A, Wang H-T, Choksi V, Florek M et al (2010) Essential regulation of CNS angiogenesis by the orphan G protein-coupled receptor GPR 124. Science 330:985-989
51. Niaudet C, Hofmann JJ, Mäe MA, Jung B, Gaengel K, Vanlandewijck M et al (2015) Gpr116 receptor regulates distinctive functions in pneumocytes and vascular endothelium. PLoS One 10:e0137949
52. Tobaben S, Südhof TC, Stahl B (2002) Genetic analysis of alpha-latrotoxin receptors reveals functional interdependence of CIRL/latrophilin 1 and neurexin 1 alpha. J Biol Chem 277:6359-6365
53. Wallis D, Hill DS, Mendez IA, Abbott LC, Finnell RH, Wellman PJ et al (2012) Initial characterization of mice null for Lphn3, a gene implicated in ADHD and addiction. Brain Res 1463:85-92
54. Wang J-J, Zhang L-L, Zhang H, Shen C-L, Lu SY, Kuang Y et al (2013) Gpr97 is essential for the follicular versus marginal zone B-lymphocyte fate decision. Cell Death Dis 4, e853
55. 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
56. Lin H-H, Faunce DE, Stacey M, Terajewicz A, Nakamura T, Zhang-Hoover J et al (2005) The macrophage F4/80 receptor is required for the induction of antigen-specific efferent regulatory T cells in peripheral tolerance. J Exp Med 201:1615-1625
57. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, Chavala S et al (2007) Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449:346-350
58. Anderson KD, Pan L, Yang X, Hughes VC, Walls JR, Dominguez MG et al (2011) Angiogenic sprouting into neural tissue requires Gpr124, an orphan G protein-coupled receptor. Proc Natl Acad Sci U S A 108:2807-2812
59. Cullen M, Elzarrad MK, Seaman S, Zudaire E, Stevens J, Yang MY et al (2011) GPR124, an orphan G protein-coupled receptor, is required for CNS-specific vascularization and establishment of the blood-brain barrier. Proc Natl Acad Sci U S A 108:5759-5764
60. Zhou Y, Nathans J (2014) Gpr124 controls CNS angiogenesis and blood-brain barrier integrity by promoting ligand-specific canonical wnt signaling. Dev Cell 31:248-256
61. Vanhollebeke B, Stone OA, Bostaille N, Cho C, Zhou Y, Maquet E, et al (2015) Tip cellspecific requirement for an atypical Gpr124-and Reck-dependent Wnt/β-catenin pathway during brain angiogenesis. eLife 4
62. Posokhova E, Shukla A, Seaman S, Volate S, Hilton MB, Wu B et al (2015) GPR124 functions as a WNT7-specific coactivator of canonical β-catenin signaling. Cell Rep 10:123-130
63. Tatin F, Taddei A, Weston A, Fuchs E, Devenport D, Tissir F et al (2013) Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev Cell 26:31-44
64. Vallon M, Essler M (2006) Proteolytically processed soluble tumor endothelial marker (TEM) 5 mediates endothelial cell survival during angiogenesis by linking integrin alpha(v)beta3 to glycosaminoglycans. J Biol Chem 281:34179-34188
65. Vallon M, Rohde F, Janssen K-P, Essler M (2010) Tumor endothelial marker 5 expression in endothelial cells during capillary morphogenesis is induced by the small GTPase Rac and mediates contact inhibition of cell proliferation. Exp Cell Res 316:412-421
66. Vallon M, Aubele P, Janssen K-P, Essler M (2012) Thrombin-induced shedding of tumour endothelial marker 5 and exposure of its RGD motif are regulated by cell-surface protein disulfide-isomerase. Biochem J 441:937-944
67. Wang T, Ward Y, Tian L, Lake R, Guedez L, Stetler-Stevenson WG et al (2005) CD97, an adhesion receptor on inflammatory cells, stimulates angiogenesis through binding integrin counterreceptors on endothelial cells. Blood 105:2836-2844
68. Kaur B, Brat DJ, Devi NS, Van Meir EG (2005) Vasculostatin, a proteolytic fragment of brain angiogenesis inhibitor 1, is an antiangiogenic and antitumorigenic factor. Oncogene 24:3632-3642
69. Masiero M, Simões FC, Han HD, Snell C, Peterkin T, Bridges E et al (2013) A core human primary tumor angiogenesis signature identifies the endothelial orphan receptor ELTD1 as a key regulator of angiogenesis. Cancer Cell 24:229-241
70. Aust G, Zhu D, Van Meir EG, Xu L (2016) Adhesion GPCRs in tumorigenesis. In: Langenhan T, Schöneberg T (eds) Adhesion G protein-coupled receptors: molecular, physiological and pharmacological principles in health and disease. Springer, Heidelberg
71. Lu YY, Sweredoski MJ, Huss D, Lansford R, Hess S, Tirrell DA (2014) Prometastatic GPCR CD97 is a direct target of tumor suppressor microRNA-126. ACS Chem Biol 9:334-338
72. Wang Y, Cho S-G, Wu X, Siwko S, Liu M (2014) G-protein coupled receptor 124 (GPR124) in endothelial cells regulates vascular endothelial growth factor (VEGF)-induced tumor angiogenesis. Curr Mol Med 14:543-554
73. Fukushima Y, Oshika Y, Tsuchida T, Tokunaga T, Hatanaka H, Kijima H et al (1998) Brainspecific angiogenesis inhibitor 1 expression is inversely correlated with vascularity and distant metastasis of colorectal cancer. Int J Oncol 13:967-970
74. Nam D-H, Park K, Suh YL, Kim J-H (2004) Expression of VEGF and brain specific angiogenesis inhibitor-1 in glioblastoma: prognostic significance. Oncol Rep 11:863-869
75. Cork SM, Kaur B, Devi NS, Cooper L, Saltz JH, Sandberg EM et al (2012) A proprotein convertase/MMP-14 proteolytic cascade releases a novel 40 kDa vasculostatin from tumor suppressor BAI 1. Oncogene 31:5144-5152
76. Duda DG, Sunamura M, Lozonschi L, Yokoyama T, Yatsuoka T, Motoi F et al (2002) Overexpression of the p53-inducible brain-specific angiogenesis inhibitor 1 suppresses efficiently tumour angiogenesis. Br J Cancer 86:490-496
77. Kudo S, Konda R, Obara W, Kudo D, Tani K, Nakamura Y et al (2007) Inhibition of tumor growth through suppression of angiogenesis by brain-specific angiogenesis inhibitor 1 gene transfer in murine renal cell carcinoma. Oncol Rep 18:785-791
78. Kaur B, Cork SM, Sandberg EM, Devi NS, Zhang Z, Klenotic PA et al (2009) Vasculostatin inhibits intracranial glioma growth and negatively regulates in vivo angiogenesis through a CD36-dependent mechanism. Cancer Res 69:1212-1220
79. Andersson M, Karlsson L, Svensson P-A, Ulfhammer E, Ekman M, Jerna°s M et al (2005) Differential global gene expression response patterns of human endothelium exposed to shear stress and intraluminal pressure. J Vasc Res 42:441-452
80. White SJ, Hayes EM, Lehoux S, Jeremy JY, Horrevoets AJG, Newby AC (2011) Characterization of the differential response of endothelial cells exposed to normal and elevated laminar shear stress. J Cell Physiol 226:2841-2848
81. Kee HJ, Koh JT, Kim M-Y, Ahn KY, Kim JK, Bae CS et al (2002) 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 22:1054-1067
82. Costello CM, Howell K, Cahill E, McBryan J, Konigshoff M, Eickelberg O et al (2008) Lungselective gene responses to alveolar hypoxia: potential role for the bone morphogenetic antagonist gremlin in pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 295: L272-L284
83. Mayer H, Bilban M, Kurtev V, Gruber F, Wagner O, Binder BR et al (2004) Deciphering regulatory patterns of inflammatory gene expression from interleukin-1-stimulated human endothelial cells. Arterioscler Thromb Vasc Biol 24:1192-1198
84. Viemann D, Goebeler M, Schmid S, Nordhues U, Klimmek K, Sorg C et al (2006) TNF induces distinct gene expression programs in microvascular and macrovascular human endothelial cells. J Leukoc Biol 80:174-185
85. Rajashekhar G, Grow M, Willuweit A, Patterson CE, Clauss M (2007) Divergent and convergent effects on gene expression and function in acute versus chronic endothelial activation. Physiol Genomics 31:104-113
86. Tugues S, Morales-Ruiz M, Fernandez-Varo G, Ros J, Arteta D, Muñoz-Luque J et al (2005) Microarray analysis of endothelial differentially expressed genes in liver of cirrhotic rats. Gastroenterology 129:1686-1695