The orphan adhesion G protein-coupled receptor GPR97 regulates migration of lymphatic endothelial cells via the small GTPases RhoA and Cdc42

Journal of Biological Chemistry

Volumn 288, Issue 50, 2013, Pages 35736-37548

  Valtcheva, Nadejda ^a   Primorac, Adriana ^a   Jurisic, Giorgia ^a,b   Hollmén, Maija ^a   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; COLLECTIVE CELL MIGRATIONS; CYTOSKELETAL REARRANGEMENTS; G PROTEIN COUPLED RECEPTORS; MOLECULAR CHARACTERIZATION; PATHOLOGICAL CONDITIONS; PHARMACOLOGICAL MANIPULATION; VASCULAR ENDOTHELIAL CELLS;

ADHESION; ENDOTHELIAL CELLS; MAMMALS; PROTEINS;

ELECTROCHEMICAL CELLS;

BETA1 INTEGRIN; F ACTIN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 97; P21 ACTIVATED KINASE 4; PAXILLIN; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL ISOLATION; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTESTINE; LYMPH VESSEL ENDOTHELIUM; LYMPHATIC ENDOTHELIAL CELL; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION;

7-HELIX RECEPTOR; ADHESION; CYTOSKELETON; ENDOTHELIAL CELL; INTEGRIN; LYMPHANGIOGENESIS; PB99; WOUND HEALING ASSAY;

ANIMALS; ANTIGENS, CD29; CDC42 GTP-BINDING PROTEIN; CELL ADHESION; CELL MOVEMENT; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; INTESTINES; MICE; P21-ACTIVATED KINASES; PAXILLIN; PHOSPHORYLATION; RECEPTORS, G-PROTEIN-COUPLED; RHOA GTP-BINDING PROTEIN;

EID: 84890377135     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.512954     Document Type: Article

References (45)

1. Cueni, L. N., and Detmar, M. (2008) The lymphatic system in health and disease. Lymphat. Res. Biol. 6, 109-122
2. Tammela, T., and Alitalo, K. (2010) Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140, 460-476
3. Alitalo, K. (2011) The lymphatic vasculature in disease. Nat. Med. 17, 1371-1380
4. Christiansen, A., and Detmar, M. (2011) Lymphangiogenesis and cancer. Genes Cancer 2, 1146-1158
5. Huggenberger, R., Siddiqui, S. S., Brander, D., Ullmann, S., Zimmermann, K., Antsiferova, M., Werner, S., Alitalo, K., and Detmar, M. (2011) An important role of lymphatic vessel activation in limiting acute inflammation. Blood 117, 4667-4678
6. Huggenberger, R., Ullmann, S., Proulx, S. T., Pytowski, B., Alitalo, K., and Detmar, M. (2010) Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J. Exp. Med. 207, 2255-2269
7. Alitalo, A., and Detmar, M. (2012) Interaction of tumor cells and lymphatic vessels in cancer progression. Oncogene 31, 4499-4508
8. Jacoby, E., Bouhelal, R., Gerspacher, M., and Seuwen, K. (2006) The 7 TM G-protein-coupled receptor target family. Chem. Med. Chem. 1, 761-782
9. Dunworth, W. P., and Caron, K. M. (2009)Gprotein-coupled receptors as potential drug targets for lymphangiogenesis and lymphatic vascular diseases. Arterioscler. Thromb. Vasc. Biol. 29, 650-656
10. Kriehuber, E., Breiteneder-Geleff, S., Groeger, M., Soleiman, A., Schoppmann, S. F., Stingl, G., Kerjaschki, D., and Maurer, D. (2001) Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med. 194, 797-808
11. Hirakawa, S., Hong, Y. K., Harvey, N., Schacht, V., Matsuda, K., Libermann, T., and Detmar, M. (2003) Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 162, 575-586
12. Petrova, T. V., Mäkinen, T., Mäkelä, T. P., Saarela, J., Virtanen, I., Ferrell, R. E., Finegold, D. N., Kerjaschki, D., Ylä-Herttuala, S., and Alitalo, K. (2002) Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 21, 4593-4599
13. Jurisic, G., Maby-El Hajjami, H., Karaman, S., Ochsenbein, A. M., Alitalo, A., Siddiqui, S. S., Ochoa Pereira, C., Petrova, T. V., and Detmar, M. (2012) An unexpected role of semaphorin3a-neuropilin-1 signaling in lymphatic vessel maturation and valve formation. Circ. Res. 111, 426-436
14. Jurisic, G., Iolyeva, M., Proulx, S. T., Halin, C., and Detmar, M. (2010) Thymus cell antigen 1 (Thy1, CD90) is expressed by lymphatic vessels and mediates cell adhesion to lymphatic endothelium. Exp. Cell Res. 316, 2982-2992
15. Fredriksson, R., Lagerström, M. C., Höglund, P. J., and Schiöth, H. B. (2002) Novel human G protein-coupled receptors with long N-terminals containing GPS domains and Ser/Thr-rich regions. FEBS Lett. 531, 407-414
16. Yona, S., Lin, H.-H., Siu, W. O., Gordon, S., and Stacey, M. (2008) Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem. Sci. 33, 491-500
17. Bjarnadóttir, T. K., Fredriksson, R., and Schiöth, H. B. (2007) The adhesion GPCRs: a unique family of G protein-coupled receptors with important roles in both central and peripheral tissues. Cell. Mol. Life Sci. 64, 2104-2119
18. Gupte, J., Swaminath, G., Danao, J., Tian, H., Li, Y., and Wu, X. (2012) Signaling property study of adhesion G-protein-coupled receptors. FEBS Lett. 586, 1214-1219
19. Mizuno, N., and Itoh, H. (2010) Signal transduction mediated through adhesion-GPCRs. Adv. Exp. Med. Biol. 706, 157-166
20. Yona, S., Lin, H. H., and Stacey, M. (2010) Immunity and adhesion-GPCRs. Adv. Exp. Med. Biol. 706, 121-127
21. Cotton, M., and Claing, A. (2009) G protein-coupled receptors stimulation and the control of cell migration. Cell Signal 21, 1045-1053
22. Adams, R. H., and Alitalo, K. (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478
23. -ΔΔCT method. Methods 25, 402-408
24. Gebäck, T., Schulz, M. M., Koumoutsakos, P., and Detmar, M. (2009) TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. BioTechniques 46, 265-274
25. Xu, L., Begum, S., Hearn, J. D., and Hynes, R. O. (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
26. Luo, R., Jeong, S. J., Jin, Z., Strokes, N., Li, S., and Piao, X. (2011)Gprotein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc. Natl. Acad. Sci. U.S.A. 108, 12925-12930
27. 1. Proc. Natl. Acad. Sci. U.S.A. 90, 9051-9055
28. Jurisic, G., and Detmar, M. (2009) Lymphatic endothelium in health and disease. Cell Tissue Res. 335, 97-108
29. Fritz-Six, K. L., Dunworth, W. P., Li, M., and Caron, K. M. (2008) Adrenomedullin signaling is necessary for murine lymphatic vascular development. J. Clin. Invest. 118, 40-50
30. Sleckman, B. P., Khan, W. N., Xu, W., Bassing, C. H., Malynn, B. A., Copeland, N. G., Bardon, C. G., Breit, T. M., Davidson, L., Oltz, E. M., Jenkins, N. A., Berman, J. E., and Alt, F. W. (2000) Cloning and functional characterization of the early-lymphocyte-specific Pb99 gene. Mol. Cell. Biol. 20, 4405-4410
31. Gratzinger, D., Canosa, S., Engelhardt, B., and Madri, J. A. (2003) Platelet endothelial cell adhesion molecule-1 modulates endothelial cell motility through the small G-protein Rho. FASEB J. 17, 1458-1469
32. Scholten, D. J., Canals, M., Maussang, D., Roumen, L., Smit, M. J., Wijtmans, M., de Graaf, C., Vischer, H. F., and Leurs, R. (2012) Pharmacological modulation of chemokine receptor function. Br. J. Pharmacol. 165, 1617-1643
33. 12/13 and Rho pathway. J. Biol. Chem. 283, 14469-14478
34. Yang, L., Chen, G., Mohanty, S., Scott, G., Fazal, F., Rahman, A., Begum, S., Hynes, R. O., and Xu, L. (2011) GPR56 Regulates VEGF production and angiogenesis during melanoma progression. Cancer Res. 71, 5558-5568
35. Nobes, C. D., and Hall, A. (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244
36. Ispanovic, E., Serio, D., and Haas, T. L. (2008) Cdc42 and RhoA have opposing roles in regulating membrane type 1-matrix metalloproteinase localization and matrix metalloproteinase-2 activation. Am. J. Physiol. Cell Physiol. 295, C600-C610
37. Shum, M. S., Pasquier, E., Po'uha, S. T., O'Neill, G. M., Chaponnier, C., Gunning, P. W., and Kavallaris, M. (2011) γ-Actin regulates cell migration and modulates the ROCK signaling pathway. FASEB J. 25, 4423-4433
38. 12 inhibits α2β1 integrin-mediated Madin-Darby canine kidney cell attachment and migration on collagen-I and blocks tubulogenesis. Mol. Biol. Cell 20, 4596-4610
39. Koh, W., Sachidanandam, K., Stratman, A. N., Sacharidou, A., Mayo, A. M., Murphy, E. A., Cheresh, D. A., and Davis, G. E. (2009) Formation of endothelial lumens requires a coordinated PKCε-, Src-, Pak- and Rafkinase-dependent signaling cascade downstream of Cdc42 activation. J. Cell Sci. 122, 1812-1822
40. Paavola, K. J., and Hall, R. A. (2012) Adhesion G protein-coupled receptors: signaling, pharmacology, and mechanisms of activation. Mol. Pharmacol. 82, 777-783
41. 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631-24634
42. 2-induced inhibition of Rac and migration in vascular smooth muscle in a manner dependent on Rho but not Rho kinase. Cardiovasc. Res. 79, 689-697
43. q/11 association. Mol. Biol. Cell 15, 2375-2387
44. King, S. J., Worth, D. C., Scales, T. M., Monypenny, J., Jones, G. E., and Parsons, M. (2011) β1 integrins regulate fibroblast chemotaxis through control of N-WASP stability. EMBO J. 30, 1705-1718
45. Araç, D., Boucard, A. A., Bolliger, M. F., Nguyen, J., Soltis, S. M., Südhof, T. C., and Brunger, A. T. (2012) A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. EMBO J. 31, 1364-1378