β-1,4-galactosyltransferase III suppresses extravillous trophoblast invasion through modifying β1-integrin glycosylation

Placenta

Volumn 36, Issue 4, 2015, Pages 357-364

  Liao, W C ^a,b   Liu, C H ^c   Chen, C H ^d   Hsu, W M ^e   Liao, Y Y ^e   Chang, H M ^f   Lan, C T ^a   Huang, M C ^g   Shyu, M K ^e  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^g NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

B4GALT3; Extraillous trophoblast; Glycosylation; Integrin; Invasion; Placenta

Indexed keywords

BETA 1,4 GALACTOSYLTRANSFERASE 3; BETA1 INTEGRIN; FOCAL ADHESION KINASE; GALACTOSYLTRANSFERASE; LAMININ; UNCLASSIFIED DRUG; ISOENZYME; N ACETYLLACTOSAMINE SYNTHASE; RECOMBINANT PROTEIN;

ARTICLE; BETA CHAIN; CATALYSIS; CELL ADHESION; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELLULAR DISTRIBUTION; CHORION VILLUS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTROPHOBLAST; DECIDUA; EXTRACELLULAR MATRIX; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; SECOND TRIMESTER PREGNANCY; SIGNAL TRANSDUCTION; SYNCYTIOTROPHOBLAST; THIRD TRIMESTER PREGNANCY; TROPHOBLAST; WESTERN BLOTTING; ADULT; CELL CULTURE; CELL LINE; CELL MOTION; CHEMISTRY; CYTOLOGY; DOWN REGULATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; METABOLISM; PREGNANCY; PROTEIN PROCESSING; REPRODUCTION;

ADULT; ANTIGENS, CD29; CELL ADHESION; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOSYLATION; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; N-ACETYLLACTOSAMINE SYNTHASE; PLACENTATION; PREGNANCY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; RECOMBINANT PROTEINS; TROPHOBLASTS;

EID: 84924540796     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2015.01.008     Document Type: Article

References (40)

1. Y. Zhou, C.H. Damsky, K. Chiu, J.M. Roberts, and S.J. Fisher Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts J Clin Invest 91 3 1993 950 960
2. G. Gerretsen, H.J. Huisjes, and J.D. Elema Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation Br J Obstet Gynaecol 88 9 1981 876 881
3. E. Ball, J.N. Bulmer, S. Ayis, F. Lyall, and S.C. Robson Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion J Pathol 208 4 2006 535 542
4. Y.M. Kim, E. Bujold, T. Chaiworapongsa, R. Gomez, B.H. Yoon, and H.T. Thaler Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes Am J Obstet Gynecol 189 4 2003 1063 1069
5. J.D. Aplin Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro J Cell Sci 99 Pt 4 1991 681 692
6. C. Chakraborty, L.M. Gleeson, T. McKinnon, and P.K. Lala Regulation of human trophoblast migration and invasiveness Can J Physiol Pharmacol 80 2 2002 116 124
7. M.M. Fuster, and J.D. Esko The sweet and sour of cancer: glycans as novel therapeutic targets Nat Rev Cancer 5 7 2005 526 542
8. G.W. Hart, and R.J. Copeland Glycomics hits the big time Cell 143 5 2010 672 676
9. D.J. Gill, K.M. Tham, J. Chia, S.C. Wang, C. Steentoft, and H. Clausen Initiation of GalNAc-type O-glycosylation in the endoplasmic reticulum promotes cancer cell invasiveness Proc Natl Acad Sci U S A 110 34 2013 E3152 E3161
10. Y.Y. Zhao, Y. Sato, T. Isaji, T. Fukuda, A. Matsumoto, and E. Miyoshi Branched N-glycans regulate the biological functions of integrins and cadherins FEBS J 275 9 2008 1939 1948
11. T.D. Burrows, A. King, and Y.W. Loke Trophoblast migration during human placental implantation Hum Reprod Update 2 4 1996 307 321
12. C.H. Damsky, C. Librach, K.H. Lim, M.L. Fitzgerald, M.T. McMaster, and M. Janatpour Integrin switching regulates normal trophoblast invasion Development 120 12 1994 3657 3666
13. L.K. Harris, C.J. Jones, and J.D. Aplin Adhesion molecules in human trophoblast - a review. II. extravillous trophoblast Placenta 30 4 2009 299 304
14. E. Yamamoto, K. Ino, E. Miyoshi, K. Inamori, A. Abe, and S. Sumigama N-acetylglucosaminyltransferase V regulates extravillous trophoblast invasion through glycosylation of alpha5beta1 integrin Endocrinology 150 2 2009 990 999
15. W.C. Liao, C.H. Chen, C.H. Liu, M.J. Huang, C.W. Chen, and J.S. Hung Expression of GALNT2 in human extravillous trophoblasts and its suppressive role in trophoblast invasion Placenta 33 12 2012 1005 1011
16. S. Guo, T. Sato, K. Shirane, and K. Furukawa Galactosylation of N-linked oligosaccharides by human beta-1,4-galactosyltransferases I, II, III, IV, V, and VI expressed in Sf-9 cells Glycobiology 11 10 2001 813 820
17. H.H. Chang, C.H. Chen, C.H. Chou, Y.F. Liao, M.J. Huang, and Y.H. Chen beta-1,4-galactosyltransferase III enhances invasive phenotypes via beta1-integrin and predicts poor prognosis in neuroblastoma Clin Cancer Res 19 7 2013 1705 1716
18. H.J. Kliman, J.E. Nestler, E. Sermasi, J.M. Sanger, and J.F. Strauss 3rd Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae Endocrinology 118 4 1986 1567 1582
19. J.D. Aplin, T. Haigh, C.J. Jones, H.J. Church, and L. Vicovac Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin alpha5beta1 Biol Reprod 60 4 1999 828 838
20. M. Ujita, A.K. Misra, J. McAuliffe, O. Hindsgaul, and M. Fukuda Poly-N-acetyllactosamine extension in N-glycans and core 2- and core 4-branched O-glycans is differentially controlled by i-extension enzyme and different members of the beta 1,4-galactosyltransferase gene family J Biol Chem 275 21 2000 15868 15875
21. T. Nishie, Y. Hikimochi, K. Zama, Y. Fukusumi, M. Ito, and H. Yokoyama beta 4-galactosyltransferase-5 is a lactosylceramide synthase essential for mouse extra-embryonic development Glycobiology 20 10 2010 1311 1322
22. N. Tokuda, S. Numata, X. Li, T. Nomura, M. Takizawa, and Y. Kondo beta4GalT6 is involved in the synthesis of lactosylceramide with less intensity than beta4GalT5 Glycobiology 23 10 2013 1175 1183
23. R. Almeida, M. Amado, L. David, S.B. Levery, E.H. Holmes, and G. Merkx A family of human beta4-galactosyltransferases. Cloning and expression of two novel UDP-galactose:beta-n-acetylglucosamine beta1, 4-galactosyltransferases, beta4Gal-T2 and beta4Gal-T3 J Biol Chem 272 51 1997 31979 31991
24. K.G. Kohlgraf, A.J. Gawron, M. Higashi, J.L. Meza, M.D. Burdick, and S. Kitajima Contribution of the MUC1 tandem repeat and cytoplasmic tail to invasive and metastatic properties of a pancreatic cancer cell line Cancer Res 63 16 2003 5011 5020
25. J.A. Schroeder, M.C. Adriance, M.C. Thompson, T.D. Camenisch, and S.J. Gendler MUC1 alters beta-catenin-dependent tumor formation and promotes cellular invasion Oncogene 22 9 2003 1324 1332
26. M.K. Shyu, M.C. Lin, C.H. Liu, Y.R. Fu, J.C. Shih, and C.N. Lee MUC1 expression is increased during human placental development and suppresses trophoblast-like cell invasion in vitro Biol Reprod 79 2 2008 233 239
27. H.B. Guo, Y. Zhang, and H.L. Chen Relationship between metastasis-associated phenotypes and N-glycan structure of surface glycoproteins in human hepatocarcinoma cells J Cancer Res Clin 127 4 2001 231 236
28. K. Murata, E. Miyoshi, S. Ihara, S. Noura, M. Kameyama, and O. Ishikawa Attachment of human colon cancer cells to vascular endothelium is enhanced by N-acetylglucosaminyltransferase V Oncol Basel 66 6 2004 492 501
29. R. Pijnenborg, G. Dixon, W.B. Robertson, and I. Brosens Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy Placenta 1 1 1980 3 19
30. G.E. Lash, H.A. Otun, B.A. Innes, J.N. Bulmer, R.F. Searle, and S.C. Robson Inhibition of trophoblast cell invasion by TGFB1, 2, and 3 is associated with a decrease in active proteases Biol Reprod 73 2 2005 374 381
31. O. Genbacev, R. Joslin, C.H. Damsky, B.M. Polliotti, and S.J. Fisher Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia J Clin Invest 97 2 1996 540 550
32. R.O. Hynes Integrins: bidirectional, allosteric signaling machines Cell 110 6 2002 673 687
33. T.D. Burrows, A. King, and Y.W. Loke Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin Hum Reprod 8 3 1993 475 484
34. M. Clement, J. Rocher, G. Loirand, and J. Le Pendu Expression of sialyl-Tn epitopes on beta1 integrin alters epithelial cell phenotype, proliferation and haptotaxis J Cell Sci 117 Pt 21 2004 5059 5069
35. T. Isaji, Y. Kariya, Q. Xu, T. Fukuda, N. Taniguchi, and J. Gu Functional roles of the bisecting GlcNAc in integrin-mediated cell adhesion Meth Enzymol 480 2010 445 459
36. S.H. Lee, S. Hatakeyama, S.Y. Yu, X.F. Bao, C. Ohyama, and K.H. Khoo Core3 O-glycan synthase suppresses tumor formation and metastasis of prostate carcinoma PC3 and LNCaP cells through down-regulation of alpha 2 beta 1 integrin complex J Biol Chem 284 25 2009 17157 17169
37. H.B. Guo, I. Lee, M. Kamar, S.K. Akiyama, and M. Pierce Aberrant N-glycosylation of beta1 integrin causes reduced alpha5beta1 integrin clustering and stimulates cell migration Cancer Res 62 23 2002 6837 6845
38. M.E. Janik, A. Litynska, and P. Vereecken Cell migration-the role of integrin glycosylation Biochim Biophys Acta 1800 6 2010 545 555
39. A. Arjonen, J. Alanko, S. Veltel, and J. Ivaska Distinct recycling of active and inactive beta1 integrins Traffic 13 4 2012 610 625
40. V.H. Lobert, A. Brech, N.M. Pedersen, J. Wesche, A. Oppelt, and L. Malerod Ubiquitination of alpha 5 beta 1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes Dev Cell 19 1 2010 148 159