GPR56 inhibits melanoma growth by internalizing and degrading its ligand TG2

Cancer Research

Volumn 74, Issue 4, 2014, Pages 1022-1031

  Yang, Liquan ^a,b   Friedland, Scott ^a   Corson, Nancy ^a   Xu, Lei ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; GENES, TUMOR SUPPRESSOR; GTP-BINDING PROTEINS; LIGANDS; MELANOMA; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTORS, G-PROTEIN-COUPLED; TRANSGLUTAMINASES; TUMOR MICROENVIRONMENT;

EID: 84894273369     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1268     Document Type: Article

References (49)

1. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009;9:239-52.
2. Naba A, Clauser KR, Hoersch S, Liu H, Carr SA, Hynes RO. The matrisome: in silico definition and in vivo characterization by proteo-mics of normal and tumor extracellular matrices. Mol Cell Proteomics 2012;11:M111.014647.
3. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012;196:395-406.
4. Hynes RO. The extracellular matrix: not just pretty fibrils. Science 2009;326:1216-9.
5. Yamada KM. Integrin signaling. Matrix Biol 1997;16:137-41.
6. Berrier AL, Yamada KM. Cell-matrix adhesion. J Cell Physiol 2007;213: 565-73.
7. Streuli C. Extracellular matrix remodelling and cellular differentiation. Curr Opin Cell Biol 1999;11:634-40.
8. McKeown-Longo PJ, Hanning R, Mosher DF. Binding and degradation of platelet thrombospondin by cultured fibroblasts. J Cell Biol 1984;98:22-8.
9. Murphy-Ullrich JE, Mosher DF. Interactions of thrombospondin with endothelial cells: receptor-mediated binding and degradation. J Cell Biol 1987;105:1603-11.
10. Shi F, Sottile J. Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J Cell Sci 2008;121: 2360-71.
11. Colpaert C, Vermeulen P, Van Marck E, Dirix L. The presence of a fibrotic focus is an independent predictor of early metastasis in lymph node-negative breast cancer patients. Am J Surg Pathol 2001;25: 1557-8.
12. Reticker-Flynn NE, Malta DF, Winslow MM, Lamar JM, Xu MJ, Under-hill GH, et al. A combinatorial extracellular matrix platform identifies cell-extracellular matrix interactions that correlate with metastasis. Nat Commun 2012;3:1122.
13. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005;8:241-54.
14. Xiao Q, Ge G. Lysyl oxidase, extracellular matrix remodeling and cancer metastasis. Cancer Microenviron 2012;5:261-73.
15. Schafer M, Werner S. Cancer as an overhealing wound: an old hypothesis revisited. Nat Rev Mol Cell Biol 2008;9:628-38.
16. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009;139:891-906.
17. Kotsakis P, Griffin M. Tissue transglutaminase in tumour progression: friend or foe? Amino Acids 2007;33:373-84.
18. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 2003;4:140-56.
19. Kumar A, Xu J, Brady S, Gao H, Yu D, Reuben J, et al. Tissue transglutaminase promotes drug resistance and invasion by inducing mesenchymal transition in mammary epithelial cells. PloS ONE 2010;5: e13390.
20. Yakubov B, Chelladurai B, Schmitt J, Emerson R, Turchi JJ, Matei D. Extracellular tissue transglutaminase activates noncanonical NF-kap-paB signaling and promotes metastasis in ovarian cancer. Neoplasia 2013;15:609-19.
21. Yang L, Xu L. GPR56 in cancer progression: current status and future perspective. Future Oncol 2012;8:431-40.
22. Jones RA, Kotsakis P, Johnson TS, Chau DY, Ali S, Melino G, et al. Matrix changes induced by transglutaminase 2 lead to inhibition of angiogenesis and tumor growth. Cell Death Differ 2006;13: 1442-53.
23. Di Giacomo G, Lentini A, Beninati S, Piacentini M, Rodolfo C. In vivo evaluation of type 2 transglutaminase contribution to the metastasis formation in melanoma. Amino Acids 2009;36:717-24.
24. Arac D, Aust G, Calebiro D, Engel FB, Formstone C, Goffinet A, et al. Dissecting signaling and functions of adhesion G protein-coupled receptors. Ann N Y Acad Sci 2012;1276:1-25.
25. Yona S, Lin HH, Siu WO, Gordon S, Stacey M. Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem Sci 2008;33: 491-500.
26. Lin HH, Chang GW, Davies JQ, Stacey M, Harris J, Gordon S. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J Biol Chem 2004;279:31823-32.
27. Krasnoperov VG, Bittner MA, Beavis R, Kuang Y, Salnikow KV, Che-purny OG, et al. alpha-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 1997;18: 925-37.
28. Xu L, Begum S, Hearn JD, Hynes RO. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci USA 2006;103:9023-8.
29. De Laurenzi V, Melino G. Gene disruption of tissue transglutaminase. Mol Cell Biol 2001;21:148-55.
30. Zhang J, Lesort M, Guttmann RP, Johnson GV. Modulation of the in situ activity of tissue transglutaminase by calcium and GTP. J Biol Chem 1998;273:2288-95.
31. Chiang NY, Hsiao CC, Huang YS, Chen HY, Hsieh IJ, Chang GW, et al. Disease-associated GPR56 mutations cause bilateral frontoparietal polymicrogyria via multiple mechanisms. J Biol Chem 2011;286: 14215-25.
32. Yang L, Chen G, Mohanty S, Scott G, Fazal F, Rahman A, et al. GPR56 Regulates VEGF production and angiogenesis during melanoma progression. Cancer Res 2011;71:5558-68.
33. Zemskov EA, Janiak A, Hang J, Waghray A, Belkin AM. The role of tissue transglutaminase in cell-matrix interactions. Front Biosci 2006;11:1057-76.
34. Filiano AJ, Bailey CD, Tucholski J, Gundemir S, Johnson GV. Trans-glutaminase 2 protects against ischemic insult, interacts with HIF1-beta, and attenuates HIF1 signaling. FASEB J 2008;22:2662-75.
35. Magalhaes AC, Dunn H, Ferguson SS. Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins. Br J Pharmacol 2012;165:1717-36.
36. LeMosy EK, Erickson HP, Beyer WF Jr., Radek JT, Jeong JM, Murthy SN, et al. Visualization of purified fibronectin-transglutaminase complexes. J Biol Chem 1992;267:7880-5.
37. Miyamoto S, Katz BZ, Lafrenie RM, Yamada KM. Fibronectin and integrins in cell adhesion, signaling, and morphogenesis. Ann N Y Acad Sci 1998;857:119-29.
38. Akimov SS, Krylov D, Fleischman LF, Belkin AM. Tissue transgluta-minase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 2000;148:825-38.
39. Zemskov EA, Mikhailenko I, Strickland DK, Belkin AM. Cell-surface transglutaminase undergoes internalization and lysosomal degradation: an essential role for LRP1. J Cell Sci 2007;120:3188-99.
40. Kaariainen E, Nummela P, Soikkeli J, Yin M, Lukk M, Jahkola T, et al. Switch to an invasive growth phase in melanoma is associated with tenascin-C, fibronectin, and procollagen-I forming specific channel structures for invasion. J Pathol 2006;210:181-91.
41. Danen EH, Yamada KM. Fibronectin, integrins, and growth control. J Cell Physiol 2001;189:1-13.
42. Barkan D, Green JE, Chambers AF. Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur J Cancer 2010;46:1181-8.
43. Dallas SL, Chen Q, Sivakumar P. Dynamics of assembly and reorganization of extracellular matrix proteins. Curr Topi Dev Biol 2006;75: 1-24.
44. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol 2002;3:207-14.
45. Bergers G, Coussens LM. Extrinsic regulators of epithelial tumor progression: metalloproteinases. Curr Opin Genet Dev 2000;10:120-7.
46. Sottile J, Chandler J. Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol Biol Cell 2005;16:757-68.
47. Piao X, Hill RS, Bodell A, Chang BS, Basel-Vanagaite L, Straussberg R, et al. G protein-coupled receptor-dependent development of human frontal cortex. Science 2004;303:2033-6.
48. Maerker T, van Wijk E, Overlack N, Kersten FF, McGee J, Goldmann T, et al. A novel usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells. Hum Mol Genet 2008;17:71-86.
49. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, et al. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 2010;466:869-73.