CD97 inhibits cell migration in human fibrosarcoma cells by modulating TIMP-2/MT1- MMP/MMP-2 activity - role of GPS autoproteolysis and functional cooperation between the N- and C-terminal fragments

FEBS Journal

Volumn 281, Issue 21, 2014, Pages 4878-4891

  Hsiao, Cheng Chih ^a,b   Wang, Wen Chih ^a   Kuo, Wan Lin ^a   Chen, Hsin Yi ^a   Chen, Tse Ching ^c   Hamann, Jörg ^b   Lin, Hsi Hsien ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Adhesion class G protein coupled receptors (adhesion GPCRs); CD97; Cell migration; Matrix metalloproteinases; Metastasis

Indexed keywords

CD97 ANTIGEN; G PROTEIN COUPLED RECEPTOR; GELATINASE A; INTEGRIN; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; TISSUE INHIBITOR OF METALLOPROTEINASE 2; CD97 PROTEIN, HUMAN; CULTURE MEDIUM; HYBRID PROTEIN; LEUKOCYTE ANTIGEN; MATRIX METALLOPROTEINASE 15; MMP14 PROTEIN, HUMAN; MMP15 PROTEIN, HUMAN; SMALL INTERFERING RNA; TIMP2 PROTEIN, HUMAN; TUMOR PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD97 GENE; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; FEMALE; FIBROSARCOMA CELL LINE; GENE EXPRESSION REGULATION; HT1080 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN SUBUNIT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL ADHESION; CELL MOTION; CHEMISTRY; CHEMOTAXIS; CULTURE MEDIUM; ENZYME ACTIVATION; ENZYMOLOGY; FIBROSARCOMA; GENETICS; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; SECONDARY; SECRETION (PROCESS); TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANTIGENS, CD; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; CULTURE MEDIA, CONDITIONED; ENZYME ACTIVATION; FEMALE; FIBROSARCOMA; HUMANS; INTEGRINS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 84915749120     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13027     Document Type: Article

References (44)

1. Dorsam RT & Gutkind JS (2007) G-protein-coupled receptors and cancer. Nat Rev Cancer 7, 79-94.
2. Lappano R & Maggiolini M (2011) G protein-coupled receptors: novel targets for drug discovery in cancer. Nat Rev Drug Discov 10, 47-60.
3. Aust G (2010) Adhesion-GPCRS in tumorigenesis. Adv Exp Med Biol 706, 109-120.
4. Lin H-H (2012) Adhesion family of G protein-coupled receptors and cancer. Chang Gung Med J 35, 15-27.
5. Yona S, Lin H-H, Siu WO, Gordon S & Stacey M (2008) Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem Sci 33, 491-500.
6. Arac-D, Boucard AA, Bolliger MF, Nguyen J, Soltis SM, Südhof TC & Brunger A T (2012) A novel evolutionarily conserved domain of cell-Adhesion GPCRs mediates autoproteolysis. EMBO J 31, 1364-1378.
7. Lin H-H, Chang G-W, Davies JQ, Stacey M, Harris J & Gordon S (2004) Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G proteincoupled receptor proteolytic site motif. J Biol Chem 279, 31823-31832.
8. Hsiao C-C, Cheng K-F, Chen H-Y, Chou Y-H, Stacey M, Chang G-W & Lin H-H (2009) Site-specific N-glycosylation regulates the GPS auto-proteolysis of CD97. FEBS Lett 583, 3285-3290.
9. Langenhan T, Aust G & Hamann J (2013) Sticky signaling-Adhesion class G protein-coupled receptors take the stage. Sci Signal 6, re3.
10. Hamann J,Eichler W,Hamann D,Kerstens HM,Poddighe PJ,Hoovers JM,Hartmann E,Strauss M,van L ier RA 1995 Expression cloning and chromosomal mapping of the leukocyte activation antigen CD97, a new seven-span transmembrane molecule of the secretion receptor superfamily with an unusual extracellular domain. J Immunol 155, 1942-1950.
11. Gray JX, Haino M, Roth MJ, Maguire JE, Jensen PN, Yarme A, Stetler-Stevenson MA, Siebenlist U & Kelly K (1996) CD97 is a processed, seven-transmembrane, heterodimeric recepto r associated with inflammation. J Immunol 157, 5438-5447.
12. Veninga H, Becker S, Hoek RM, Wobus M, Wandel E, van der Kaa J, van der Valk M, de Vos AF, Haase H, Owens B et al. (2008) Analysis of CD97 expression and manipulation: antibody treatment but not gene targeting curtails granulocyte migration. J Immunol 181, 6574-6583.
13. Aust G, Eichler W, Laue S, Lehmann I, Heldin NE, Lotz O, Scherbaum WA, Dralle H & Hoang-Vu C (1997) CD97: a dedifferentiation marker in human thyroid carcinomas. Cancer Res 57, 1798-1806.
14. Steinert M, Wobus M, Boltze C, Schütz A, Wahlbuhl M, Hamann J & Aust G (2002) Expression and regulation of CD97 in colorectal carcinoma cell lines and tumor tissues. Am J Pathol 161, 1657-1667.
15. Aust G, Steinert M, Schütz A, Boltze C, Wahlbuhl M, Hamann J & Wobus M (2002) CD97, but not its closely related EGF-TM7 family member EMR2, is expressed on gastric, pancreatic, and esophageal carcinomas. Am J Clin Pathol 118, 699-707.
16. Wobus M, Huber O, Hamann J & Aust G (2006) CD97 overexpression in tumor cells at the invasion front in colorectal cancer (CC) is inde pendently regulated of the canonical Wnt pathway. Mol Carcinog 45, 881-886.
17. Galle J, Sittig D, Hanisch I, Wobus M, Wandel E, Loeffler M & Aust G (2006) Individual cell-based mo dels of tumor-environment interactions: multiple effects of CD97 on tumor invasion. Am J Pathol 169, 1802-1811.
18. Safaee M, Clark AJ, Oh MC, Ivan ME, Bloch O, Kaur G, Sun MZ, Kim JM, Oh T, Berger MS et al. (2013) Overexpression of CD97 confers an invasive phenotype in glioblastoma cells and is associated with decreased survival of glioblastoma patients. PLoS One 8, e62765.
19. Liu D, Trojanowicz B, Radestock Y, Fu T, Hammje K, Chen L & Hoang-Vu C (2010) Role of CD97 isoforms in gastric carcinoma. Int J Oncol 36, 1401-1408.
20. Visse R & Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92, 827-839.
21. Hsiao C-C, Cheng K-F, Chen H-Y, Chou Y-H, Stacey M, Chan g G-W & Lin H-H (2011) GPS autoproteolysis is required for CD97 to up-regulate the expression of N-cadherin that promotes homotypic cell-cell aggregation. FEBS Lett 585, 3285-3290.
22. Ward Y, Lake R, Yin JJ, Heger CD, Raffeld M, Goldsmith PK, Merino M & Kelly K (2011) LPA receptor heterodimerizes with CD97 to amplify LPAinitiated RHO-dependent signaling and invasion in prostate cancer cells. Cancer Res 71, 7301-7311.
23. Liu D, Trojanowicz B, Ye L, Li C, Zhang L, Li X, Li G, Zheng Y & Chen L (2012) The invasion and metastasis promotion role of CD97 small isoform in gastric carcinoma. PL oS One 7, e39989.
24. Chidambaram A, Fillmore HL, Van Meter TE, Dumur CI & Broaddus WC (2012) Novel report of expression and function of CD97 in malignant gliomas: correlation with Wilms tumor 1 ex pression and glioma cell invasiveness. J Neurosurg 116, 843-853.
25. Deryugina EI & Quigley JP (2006) Matrix metalloproteinases and tumor metastasis. Cancer Metast Rev 25, 9-34.
26. Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA & Goldberg GI (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270, 5331-5338.
27. Butler GS, Butler MJ, Atkinson SJ, Will H, Tamura T, Schade van Westrum S, Crabbe T, Clements J, d'Ortho MP & Murphy G (1998) The TIMP2 membrane type 1 metalloproteinase 'receptor' regulates the concentration and efficient activation of progelatinase A. A kinetic study. J Biol Chem 273, 871-880.
28. Stanton H, Gavrilovic J, Atkinson SJ, d'Ortho MP, Yamada KM, Zardi L & Murphy G (1998) The activation of ProMMP-2 (gelatinase A) by HT1080 fibrosarcoma cells is promoted by culture on a fibronectin substrate and is concom itant with an increase in processing of MT1-MMP (MMP-14) to a kDa form. J Cell Sci 111 (Pt 18), 2789-2798.
29. Cho J-A, Osenkowski P, Zhao H, Kim S, Toth M, Cole K, Abouka meel A, Saliganan A, Schuger L, Bonfil RD et al. (2008) The inactive 44-kDa processed form of membrane type 1 matrix metalloproteinase (MT1-MMP) enhances proteolytic activity via regulation of endocytosis of active MT1-MMP. J Biol Chem 283, 17391-17405.
30. Wang T, Ward Y, Tian L, Lake R, Guedez L, Stetler-Stevenson WG & Kelly K (2005) CD97, an adhesion receptor on inflammatory cells, stimulates angiogenesis through binding integrin counterreceptors on endothelial cells. Blood 105, 2836-2844.
31. Lin HH, Stacey M, Hamann J, Gordon S & McKnight AJ (2000) Human EMR2, a novel EGF-TM7 molecule on chromosome 19p13.1, is closely related to CD97. Genomics 67, 188-200.
32. Kwakkenbos MJ,Matmati M,Madsen O, PouwelsW, Wang Y, Bontrop RE, Heidt PJ, HoekRM & Hamann J (2006) An unusual mod e of concerted evolution of the EGFTM7 receptor chimera EMR2. FASEB J 20, 2582-2584.
33. Huang Y-S, Chiang N-Y, Hu C-H, Hsiao C-C, Cheng K-F, Tsai W-P, Yona S, Stacey M, Gordon S, C hang G-W et al. (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.
34. Langenhan T, Prömel S, Mestek L, Esmaeili B, Waller-Evans H, Hennig C, Kohara Y, Avery L, Vakonakis I, Schnabel R et al. (2009) Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo. Dev Cell 17, 494-504.
35. Paavola KJ, Stephenson JR, Ritter SL, Alter SP & Hall RA (2011) The N terminus of the adhesion G proteincoupled receptor GPR56 controls receptor signaling activity. J Biol Chem 286, 28914-28921.
36. Stephenson JR, Paavola KJ, Schaefer SA, Kaur B, Van Meir EG & Hall RA (2013) Brain-sp ecific angiogenesis inhibitor-1 signaling, regulation, and enrichment in the postsynaptic density. J Biol Chem 288, 22248-22256.
37. Hamann J, Vogel B, van SchijndelGM&van LierRA(1996) The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF).JExpMed 184, 1185-1189.
38. Stacey M, Chang G-W, Davies JQ, Kwakkenbos MJ, Sanderson RD, Hamann J, Gordon S & Lin H-H ( 2003) The epidermal growth factor-like domains of the human EMR2 receptor mediate cell attachment through chondroitin sulfate glycosaminoglycans. Blood 102, 2916-2924.
39. Wandel E, Saalbach A, Sittig D, Gebhardt C & Aust G (2012) Thy-1 (CD90) is an interacting partner for CD97 on activated endothelial cells. J Immunol 188, 1442-1450.
40. Aust G, Kerner C, Gonsior S, Sittig D, Schneide r H, Buske P, Scholz M, Dietrich N, Oldenburg S, Karpus ON et al. (2013) Mice overexpressing CD97 in intestinal epithelial cells provide a unique model for mammalian postnatal intestinal cylindrical growth. Mol Biol Cell 24, 2256-2268.
41. Ward Y, Lake R, Martin PL, Killian K, Salerno P, Wang T, Meltzer P, Merino M, Cheng S-Y, Santoro M et al. (2013) CD97 amplifies LPA receptor signaling and promotes thyroid cancer progression in a mouse model. Oncogene 22, 2726-2738.
42. Park S-J, Lee K-P, Kang S, Chung H-Y, Bae Y-S, Okajima F & Im D-S (2013) Lysophosphatidylethanolamine utilizes LPA1 and CD97 in MDA-MB-231 breast cancer cells. Cell Signal 25, 2147-2154.
43. Oliver GW, Le ferson JD, Stetler-Stevenson WG & Kleiner DE (1997) Quantitative reverse zymography: analysis of picogram amounts of metalloproteinase inhibitors using gelatinase A and B reverse zymograms. Anal Biochem 244, 161-166.
44. Hattori S, Fujisaki H, Kiriyama T, Yokoyama T & Irie S (2002) Real-time zymography and reverse zymography: a method for detecting activities of matrix metalloproteinases and their inhibitors using FITCl abeled collagen and casein as substrates. Anal Biochem 301, 27-34.