Endothelial LGALS9 splice variant expression in endothelial cell biology and angiogenesis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 2, 2014, Pages 284-292

  Heusschen, Roy ^a   Schulkens, Iris A ^a   van Beijnum, Judy ^a   Griffioen, Arjan W ^a   Thijssen, Victor L ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Blood vessel; Cancer; Galectin; Vasculature

Indexed keywords

ECALECTIN; GALECTIN 1; GALECTIN 3; GALECTIN 8;

ANGIOGENESIS; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CARCINOMA CELL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXON; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG CARCINOMA; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; UMBILICAL VEIN ENDOTHELIAL CELL;

BLOOD VESSEL; CANCER; GALECTIN; VASCULATURE;

ALTERNATIVE SPLICING; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; GALECTINS; GENE EXPRESSION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR CELLS, CULTURED;

EID: 84890820771     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.12.003     Document Type: Article

References (52)

1. Barondes S.H., Castronovo V., Cooper D.N., Cummings R.D., Drickamer K., Feizi T., Gitt M.A., Hirabayashi J., Hughes C., Kasai K., et al. Galectins: a family of animal beta-galactoside-binding lectins. Cell 1994, 76:597-598.
2. Leffler H., Carlsson S., Hedlund M., Qian Y., Poirier F. Introduction to galectins. Glycoconj. J. 2004, 19:433-440.
3. Heusschen R., Griffioen A.W., Thijssen V.L. Galectin-9 in tumor biology: a jack of multiple trades. Biochim. Biophys. Acta 2013, 1836:177-185.
4. Bi S., Earl L.A., Jacobs L., Baum L.G. Structural features of galectin-9 and galectin-1 that determine distinct T cell death pathways. J. Biol. Chem. 2008, 283:12248-12258.
5. Earl L.A., Bi S., Baum L.G. Galectin multimerization and lattice formation are regulated by linker region structure. Glycobiology 2011, 21:6-12.
6. Liu F.T., Rabinovich G.A. Galectins as modulators of tumour progression. Nat. Rev. Cancer 2005, 5:29-41.
7. Irie A., Yamauchi A., Kontani K., Kihara M., Liu D., Shirato Y., Seki M., Nishi N., Nakamura T., Yokomise H., Hirashima M. Galectin-9 as a prognostic factor with antimetastatic potential in breast cancer. Clin. Cancer Res. 2005, 11:2962-2968.
8. Zhang Z.Y., Dong J.H., Chen Y.W., Wang X.Q., Li C.H., Wang J., Wang G.Q., Li H.L., Wang X.D. Galectin-9 acts as a prognostic factor with antimetastatic potential in hepatocellular carcinoma. Asian Pac. J. Cancer Prev. 2012, 13:2503-2509.
9. Kageshita T., Kashio Y., Yamauchi A., Seki M., Abedin M.J., Nishi N., Shoji H., Nakamura T., Ono T., Hirashima M. Possible role of galectin-9 in cell aggregation and apoptosis of human melanoma cell lines and its clinical significance. Int. J. Cancer 2002, 99:809-816.
10. Liang M., Ueno M., Oomizu S., Arikawa T., Shinonaga R., Zhang S., Yamauchi A., Hirashima M. Galectin-9 expression links to malignant potential of cervical squamous cell carcinoma. J. Cancer Res. Clin. Oncol. 2008, 134:899-907.
11. Wiersma V.R., de Bruyn M., Helfrich W., Bremer E. Therapeutic potential of galectin-9 in human disease. Med. Res. Rev. 2013, 33(Suppl 1):E102-E126.
12. Kobayashi T., Kuroda J., Ashihara E., Oomizu S., Terui Y., Taniyama A., Adachi S., Takagi T., Yamamoto M., Sasaki N., Horiike S., Hatake K., Yamauchi A., Hirashima M., Taniwaki M. Galectin-9 exhibits anti-myeloma activity through JNK and p38 MAP kinase pathways. Leukemia 2010, 24:843-850.
13. Kuroda J., Yamamoto M., Nagoshi H., Kobayashi T., Sasaki N., Shimura Y., Horiike S., Kimura S., Yamauchi A., Hirashima M., Taniwaki M. Targeting activating transcription factor 3 by galectin-9 induces apoptosis and overcomes various types of treatment resistance in chronic myelogenous leukemia. Mol. Cancer Res. 2010, 8:994-1001.
14. Nobumoto A., Nagahara K., Oomizu S., Katoh S., Nishi N., Takeshita K., Niki T., Tominaga A., Yamauchi A., Hirashima M. Galectin-9 suppresses tumor metastasis by blocking adhesion to endothelium and extracellular matrices. Glycobiology 2008, 18:735-744.
15. Thijssen V.L., Hulsmans S., Griffioen A.W. The galectin profile of the endothelium; altered expression and localization in activated and tumor endothelial cells. Am. J. Pathol. 2008, 172:545-553.
16. D'Haene N., Catteau X., Maris C., Martin B., Salmon I., Decaestecker C. Endothelial hyperplasia and endothelial galectin-3 expression are prognostic factors in primary central nervous system lymphomas. Br. J. Haematol. 2008, 140:402-410.
17. Cardenas Delgado V.M., Nugnes L.G., Colombo L.L., Troncoso M.F., Fernandez M.M., Malchiodi E.L., Frahm I., Croci D.O., Compagno D., Rabinovich G.A., Wolfenstein-Todel C., Elola M.T. Modulation of endothelial cell migration and angiogenesis: a novel function for the "tandem-repeat" lectin galectin-8. FASEB J. 2011, 25:242-254.
18. Thijssen V.L., Poirier F., Baum L.G., Griffioen A.W. Galectins in the tumor endothelium; opportunities for combined cancer therapy. Blood 2007, 110:2819-2827.
19. Nangia-Makker P., Honjo Y., Sarvis R., Akahani S., Hogan V., Pienta K.J., Raz A. Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am. J. Pathol. 2000, 156:899-909.
20. Croci D.O., Salatino M., Rubinstein N., Cerliani J.P., Cavallin L.E., Leung H.J., Ouyang J., Ilarregui J.M., Toscano M.A., Domaica C.I., Croci M.C., Shipp M.A., Mesri E.A., Albini A., Rabinovich G.A. Disrupting galectin-1 interactions with N-glycans suppresses hypoxia-driven angiogenesis and tumorigenesis in Kaposi's sarcoma. J. Exp. Med. 2012, 209:1985-2000.
21. Hsieh S.H., Ying N.W., Wu M.H., Chiang W.F., Hsu C.L., Wong T.Y., Jin Y.T., Hong T.M., Chen Y.L. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 2008, 27:3746-3753.
22. Thijssen V.L., Postel R., Brandwijk R.J., Dings R.P., Nesmelova I., Satijn S., Verhofstad N., Nakabeppu Y., Baum L.G., Bakkers J., Mayo K.H., Poirier F., Griffioen A.W. Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15975-15980.
23. Thijssen V.L., Barkan B., Shoji H., Aries I.M., Mathieu V., Deltour L., Hackeng T.M., Kiss R., Kloog Y., Poirier F., Griffioen A.W. Tumor cells secrete galectin-1 to enhance endothelial cell activity. Cancer Res. 2010, 70:6216-6224.
24. Laderach D.J., Gentilini L.D., Giribaldi L., Delgado V.C., Nugnes L., Croci D.O., Al Nakouzi N., Sacca P., Casas G., Mazza O., Shipp M.A., Vazquez E., Chauchereau A., Kutok J.L., Rodig S.J., Elola M.T., Compagno D., Rabinovich G.A. A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease. Cancer Res. 2013, 73:86-96.
25. Markowska A.I., Liu F.T., Panjwani N. Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response. J. Exp. Med. 2010, 207:1981-1993.
26. van Beijnum J.R., Dings R.P., van der Linden E., Zwaans B.M., Ramaekers F.C., Mayo K.H., Griffioen A.W. Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood 2006, 108:2339-2348.
27. van Beijnum J.R., Rousch M., Castermans K., van der Linden E., Griffioen A.W. Isolation of endothelial cells from fresh tissues. Nat. Protoc. 2008, 3:1085-1091.
28. Martelli P.L., D'Antonio M., Bonizzoni P., Castrignanò T., D'Erchia A.M., D'Onorio De Meo P., Fariselli P., Finelli M., Licciulli F., Mangiulli M., Mignone F., Pavesi G., Picardi E., Rizzi R., Rossi I., Valletti A., Zauli A., Zambelli F., Casadio R., Pesole G. ASPicDB: a database of annotated transcript and protein variants generated by alternative splicing. Nucleic Acids Res. 2011, 39:D80-D85.
29. Krause A., Haas S.A., Coward E., Vingron M. SYSTERS, GeneNest, SpliceNest: exploring sequence space from genome to protein. Nucleic Acids Res. 2002, 30:299-300.
30. Nangia-Makker P., Wang Y., Raz T., Tait L., Balan V., Hogan V., Raz A. Cleavage of galectin-3 by matrix metalloproteases induces angiogenesis in breast cancer. Int. J. Cancer 2010, 127:2530-2541.
31. Hirashima M., Kashio Y., Nishi N., Yamauchi A., Imaizumi T.A., Kageshita T., Saita N., Nakamura T. Galectin-9 in physiological and pathological conditions. Glycoconj. J. 2004, 19:593-600.
32. Spitzenberger F., Graessler J., Schroeder H.E. Molecular and functional characterization of galectin 9 mRNA isoforms in porcine and human cells and tissues. Biochimie 2001, 83:851-862.
33. Zhang F., Zheng M., Qu Y., Li J., Ji J., Feng B., Lu A., Li J., Wang M., Liu B. Different roles of galectin-9 isoforms in modulating E-selectin expression and adhesion function in LoVo colon carcinoma cells. Mol. Biol. Rep. 2009, 36:823-830.
34. Imaizumi T., Kumagai M., Sasaki N., Kurotaki H., Mori F., Seki M., Nishi N., Fujimoto K., Tanji K., Shibata T., Tamo W., Matsumiya T., Yoshida H., Cui X.-F., Takanashi S., Hanada K., Okumura K., Yagihashi S., Wakabayashi K., Nakamura T., Hirashima M., Satoh K. Interferon-{gamma} stimulates the expression of galectin-9 in cultured human endothelial cells. J. Leukoc. Biol. 2002, 72:486-491.
35. Lipkowitz M.S., Leal-Pinto E., Rappoport J.Z., Najfeld V., Abramson R.G. Functional reconstitution, membrane targeting, genomic structure, and chromosomal localization of a human urate transporter. J. Clin. Invest. 2001, 107:1103-1115.
36. Lahm H., Andre S., Hoeflich A., Fischer J.R., Sordat B., Kaltner H., Wolf E., Gabius H.J. Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures. J. Cancer Res. Clin. Oncol. 2001, 127:375-386.
37. Yoshida H., Teraoka M., Nishi N., Nakakita S., Nakamura T., Hirashima M., Kamitori S. X-ray structures of human galectin-9C-terminal domain in complexes with a biantennary oligosaccharide and sialyllactose. J. Biol. Chem. 2010, 285:36969-36976.
38. Nagae M., Nishi N., Murata T., Usui T., Nakamura T., Wakatsuki S., Kato R. Structural analysis of the recognition mechanism of poly-N-acetyllactosamine by the human galectin-9N-terminal carbohydrate recognition domain. Glycobiology 2009, 19:112-117.
39. Resh M.D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1999, 1451:1-16.
40. Nishi N., Itoh A., Fujiyama A., Yoshida N., Araya S., Hirashima M., Shoji H., Nakamura T. Development of highly stable galectins: truncation of the linker peptide confers protease-resistance on tandem-repeat type galectins. FEBS Lett. 2005, 579:2058-2064.
41. Nishi N., Itoh A., Shoji H., Miyanaka H., Nakamura T. Galectin-8 and galectin-9 are novel substrates for thrombin. Glycobiology 2006, 16:15C-20C.
42. Bidon-Wagner N., Le Pennec J.P. Human galectin-8 isoforms and cancer. Glycoconj. J. 2004, 19:557-563.
43. Chabot S., Kashio Y., Seki M., Shirato Y., Nakamura K., Nishi N., Nakamura T., Matsumoto R., Hirashima M. Regulation of galectin-9 expression and release in Jurkat T cell line cells. Glycobiology 2002, 12:111-118.
44. Matsushita N., Nishi N., Seki M., Matsumoto R., Kuwabara I., Liu F.T., Hata Y., Nakamura T., Hirashima M. Requirement of divalent galactoside-binding activity of ecalectin/galectin-9 for eosinophil chemoattraction. J. Biol. Chem. 2000, 275:8355-8360.
45. Alam S., Li H., Margariti A., Martin D., Zampetaki A., Habi O., Cockerill G., Hu Y., Xu Q., Zeng L. Galectin-9 protein expression in endothelial cells is positively regulated by histone deacetylase 3. J. Biol. Chem. 2011, 286:44211-44217.
46. Zaidi M.R., Merlino G. The two faces of interferon-γ in cancer. Clin. Cancer Res. 2011, 17:6118-6124.
47. Rabinovich G.A., Toscano M.A. Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 2009, 9:338-352.
48. Matsumoto R., Matsumoto H., Seki M., Hata M., Asano Y., Kanegasaki S., Stevens R.L., Hirashima M. Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T lymphocytes. J. Biol. Chem. 1998, 273:16976-16984.
49. Zhu C., Anderson A.C., Schubart A., Xiong H., Imitola J., Khoury S.J., Zheng X.X., Strom T.B., Kuchroo V.K. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 2005, 6:1245-1252.
50. Wang F., He W., Zhou H., Yuan J., Wu K., Xu L., Chen Z.K. The Tim-3 ligand galectin-9 negatively regulates CD8+ alloreactive T cell and prolongs survival of skin graft. Cell. Immunol. 2007, 250:68-74.
51. Su E.W., Bi S., Kane L.P. Galectin-9 regulates T helper cell function independently of Tim-3. Glycobiology 2011, 21:1258-1265.
52. He J., Baum L.G. Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration. Lab. Invest. 2006, 86:578-590.