An in vivo functional screen identifies ST6GalNAc2 sialyltransferase as a breast cancer metastasis suppressor

Cancer Discovery

Volumn 4, Issue 3, 2014, Pages 304-317

  Murugaesu, Nirupa ^a,c   Iravani, Marjan ^a   Van Weverwijk, Antoinette ^a   Ivetic, Aleksandar ^b   Johnson, Damian A ^a   Antonopoulos, Aristotelis ^a   Fearns, Antony ^a   Jamal Hanjani, Mariam ^a,c   Sims, David ^a   Fenwick, Kerry ^a   Mitsopoulos, Costas ^a   Gao, Qiong ^a   Orr, Nick ^a   Zvelebil, Marketa ^a   Haslam, Stuart M ^a   Dell, Anne ^a   Yarwood, Helen ^a   Lord, Christopher J ^a   Ashworth, Alan ^a   Isacke, Clare M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GALECTIN 3; SIALYLTRANSFERASE;

ALPHA N ACETYLGALACTOSAMINIDE ALPHA 2,6 SIALYLTRANSFERASE 2 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST METASTASIS; CELL AGGREGATION; CELL FUNCTION; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA EXTRACTION; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; GENE SILENCING; HIGH THROUGHPUT SEQUENCING; HISTOLOGY; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; LUNG METASTASIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; TUMOR VOLUME;

ANIMALS; BREAST NEOPLASMS; CELL LINE; FEMALE; GALECTIN 3; GENE EXPRESSION REGULATION, NEOPLASTIC; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; RNA INTERFERENCE; SIALYLTRANSFERASES;

EID: 84895821357     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-13-0287     Document Type: Article

References (50)

1. Steeg PS, Theodorescu D. Metastasis: a therapeutic target for cancer. Nat Clin Pract Oncol 2008;5:206-19.
2. Smith SC, Theodorescu D. Learning therapeutic lessons from metastasis suppressor proteins. Nat Rev Cancer 2009;9:253-64.
3. Bric A, Miething C, Bialucha CU, Scuoppo C, Zender L, Krasnitz A, et al. Functional identifi cation of tumor-suppressor genes through an in vivo RNA interference screen in a mouse lymphoma model. Cancer Cell 2009;16:324-35.
4. Gobeil S, Zhu X, Doillon CJ, Green MR. A genome-wide shRNA screen identifi es GAS1 as a novel melanoma metastasis suppressor gene. Genes Dev 2008;22:2932-40.
5. Gumireddy K, Li A, Gimotty PA, Klein-Szanto AJ, Showe LC, Katsaros D, et al. KLF17 is a negative regulator of epithelial-mesenchymal transition and metastasis in breast cancer. Nat Cell Biol 2009; 11: 1297-1304.
6. Meacham CE, Ho EE, Dubrovsky E, Gertler FB, Hemann MT. In vivo RNAi screening identifi es regulators of actin dynamics as key determinants of lymphoma progression. Nat Genet 2009;41:1133-7.
7. Berns K, Hijmans EM, Mullenders J, Brummelkamp TR, Velds A, Heimerikx M, et al. A large-scale RNAi screen in human cells identifi es new components of the p53 pathway. Nature 2004;428:431-7.
8. Simpson KJ, Selfors LM, Bui J, Reynolds A, Leake D, Khvorova A, et al. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 2008;10:1027-38.
9. Westbrook TF, Martin ES, Schlabach MR, Leng Y, Liang AC, Feng B, et al. A genetic screen for candidate tumor suppressors identifi es REST. Cell 2005;121:837-48.
10. Dickins RA, Hemann MT, Zilfou JT, Simpson DR, Ibarra I, Hannon GJ, et al. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat Genet 2005;37:1289-95.
11. Zender L, Xue W, Zuber J, Semighini CP, Krasnitz A, Ma B, et al. An oncogenomics-based in vivo RNAi screen identifi es tumor suppressors in liver cancer. Cell 2008;135:852-64.
12. Marcos NT, Pinho S, Grandela C, Cruz A, Samyn-Petit B, Harduin-Lepers A, et al. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res 2004;64:7050-7.
13. Brockhausen I. Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep 2006;7: 599-604.
14. Cazet A, Julien S, Bobowski M, Burchell J, Delannoy P. Tumour-associated carbohydrate antigens in breast cancer. Breast Cancer Res 2010;12:204.
15. Sims D, Bursteinas B, Gao Q, Jain E, MacKay A, Mitsopoulos C, et al. ROCK: a breast cancer functional genomics resource. Breast Cancer Res Treat 2010;124:567-72.
16. Karn T, Pusztai L, Holtrich U, Iwamoto T, Shiang CY, Schmidt M, et al. Homogeneous datasets of triple negative breast cancers enable the identifi cation of novel prognostic and predictive signatures. PLoS ONE 2011;6:e28403.
17. Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer 2005;5:29-41.
18. Yu LG, Andrews N, Zhao Q, McKean D, Williams JF, Connor LJ, et al. Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem 2007;282:773-81.
19. Glinsky VV, Glinsky GV, Rittenhouse-Olson K, Huflejt ME, Glinskii OV, Deutscher SL, et al. The role of Thomsen-Friedenreich antigen in adhesion of human breast and prostate cancer cells to the endothe-lium. Cancer Res 2001;61:4851-7.
20. Khaldoyanidi SK, Glinsky VV, Sikora L, Glinskii AB, Mossine VV, Quinn TP, et al. MDA-MB-435 human breast carcinoma cell homo-and heterotypic adhesion under fl ow conditions is mediated in part by Thomsen-Friedenreich antigen-galectin-3 interactions. J Biol Chem 2003;278:4127-34.
21. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, Rhodes JM, et al. Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 2009;69:6799-806.
22. Zou J, Glinsky VV, Landon LA, Matthews L, Deutscher SL. Pep-tides specifi c to the galectin-3 carbohydrate recognition domain inhibit metastasis-associated cancer cell adhesion. Carcinogenesis 2005;26:309-18.
23. Chauhan D, Li G, Podar K, Hideshima T, Neri P, He D, et al. A novel carbohydrate-based therapeutic GCS-100 overcomes bortezomib resistance and enhances dexamethasone-induced apoptosis in multiple myeloma cells. Cancer Res 2005;65:8350-8.
24. Streetly MJ, Maharaj L, Joel S, Schey SA, Gribben JG, Cotter FE. GCS-100, a novel galectin-3 antagonist, modulates MCL-1, NOXA, and cell cycle to induce myeloma cell death. Blood 2010;115:3939-48.
25. Bockhorn M, Jain RK, Munn LL. Active versus passive mechanisms in metastasis: do cancer cells crawl into vessels, or are they pushed? Lancet Oncol 2007;8:444-8.
26. Geng Y, Marshall JR, King MR. Glycomechanics of the metastatic cascade: tumor cell-endothelial cell interactions in the circulation. Ann Biomed Eng 2012;40:790-805.
27. Glinsky VV. Intravascular cell-to-cell adhesive interactions and bone metastasis. Cancer Metastasis Rev 2006;25:531-40.
28. Ahmad N, Gabius HJ, Andre S, Kaltner H, Sabesan S, Roy R, et al. Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J Biol Chem 2004;279:10841-7.
29. Glinsky VV, Glinsky GV, Glinskii OV, Huxley VH, Turk JR, Mossine VV, et al. Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Cancer Res 2003;63:3805-11.
30. Dumic J, Dabelic S, Flogel M. Galectin-3: an open-ended story. Bio-chim Biophys Acta 2006;1760:616-35.
31. Takenaka Y, Fukumori T, Raz A. Galectin-3 and metastasis. Glyco-conj J 2004;19:543-9.
32. Chiu CG, Strugnell SS, Griffith OL, Jones SJ, Gown AM, Walker B, et al. Diagnostic utility of galectin-3 in thyroid cancer. Am J Pathol 2010;176:2067-81.
33. Matsuda Y, Yamagiwa Y, Fukushima K, Ueno Y, Shimosegawa T. Expression of galectin-3 involved in prognosis of patients with hepa-tocellular carcinoma. Hepatol Res 2008;38:1098-111.
34. O'Driscoll L, Linehan R, Kennedy SM, Cronin D, Purcell R, Glynn S, et al. Lack of prognostic significance of survivin, survivin-deltaEx3, survivin-2B, galectin-3, bag-1, bax-alpha and MRP-1 mRNAs in breast cancer. Cancer Lett 2003;201:225-36.
35. Vereecken P, Awada A, Suciu S, Castro G, Morandini R, Litynska A, et al. Evaluation of the prognostic significance of serum galectin-3 in American Joint Committee on Cancer stage III and stage IV melanoma patients. Melanoma Res 2009;19:316-20.
36. Burchell JM, Mungul A, Taylor-Papadimitriou J. O-linked glycosyla-tion in the mammary gland: changes that occur during malignancy. J Mammary Gland Biol Neoplasia 2001;6:355-64.
37. Dall'Olio F, Chiricolo M. Sialyltransferases in cancer. Glycoconj J 2001;18:841-50.
38. Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P. The human sialyltransferase family. Biochimie 2001;83:727-37.
39. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, et al. Genes that mediate breast cancer metastasis to the brain. Nature 2009;459:1005-9.
40. Burchell J, Poulsom R, Hanby A, Whitehouse C, Cooper L, Clausen H, et al. An alpha2,3 sialyltransferase (ST3Gal I) is elevated in primary breast carcinomas. Glycobiology 1999;9:1307-11.
41. Julien S, Adriaenssens E, Ottenberg K, Furlan A, Courtand G, Vercoutter-Edouart AS, et al. ST6GalNAc I expression in MDA-MB-231 breast cancer cells greatly modifi es their O-glycosylation pattern and enhances their tumourigenicity. Glycobiology 2006; 16: 54-64.
42. Julien S, Lagadec C, Krzewinski-Recchi MA, Courtand G, Le Bourhis X, Delannoy P. Stable expression of sialyl-Tn antigen in T47-D cells induces a decrease of cell adhesion and an increase of cell migration. Breast Cancer Res Treat 2005;90:77-84.
43. Pinho S, Marcos NT, Ferreira B, Carvalho AS, Oliveira MJ, Santos-Silva F, et al. Biological significance of cancer-associated sialyl-Tn antigen: modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett 2007;249:157-70.
44. Sewell R, Backstrom M, Dalziel M, Gschmeissner S, Karlsson H, Noll T, et al. The ST6GalNAc-I sialyl transferase localizes throughout the Golgi and is responsible for the synthesis of the tumor-associated sialyl-Tn O-glycan in human breast cancer. J Biol Chem 2006; 281: 3586-94.
45. Glinsky VV, Raz A. Modified citrus pectin anti-metastatic properties: one bullet, multiple targets. Carbohydr Res 2009;344:1788-91.
46. Schlabach MR, Luo J, Solimini NL, Hu G, Xu Q, Li MZ, et al. Cancer proliferation gene discovery through functional genomics. Science 2008;319:620-4.
47. Silva JM, Li MZ, Chang K, Ge W, Golding MC, Rickles RJ, et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat Genet 2005;37:1281-8.
48. Sims D, Mendes-Pereira AM, Frankum J, Burgess D, Cerone MA, Lombardelli C, et al. High-throughput RNA interference screening using pooled shRNA libraries and next generation sequencing. Genome Biol 2011;12:R104.
49. Jang-Lee J, North SJ, Sutton-Smith M, Goldberg D, Panico M, Morris H, et al. Glycomic profi ling of cells and tissues by mass spectrometry: f ngerprinting and sequencing methodologies. Methods Enzymol 2006;415:59-86.
50. Sutton-Smith M, Dell A. Analysis of carbohydrates/glycoproteins by mass spectrometry. In: Celis JE, editor. Cell biology: a laboratory handbook. Amsterdam, the Netherlands: Elsevier Academic; 2006. p. 415-25.