The contribution of fucosyltransferases to cancer biology

Vasconcelos, A. O.; Vieira, L. M.; Rocha, C. R. C.; Beltrão, E. I. C.

doi:10.1590/1519-6984.278681

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Brazilian Journal of Biology

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Original Article • Braz. J. Biol. 84 • 2024 • https://doi.org/10.1590/1519-6984.278681 copy

The contribution of fucosyltransferases to cancer biology

A contribuição das fucosiltransferases para a biologia do câncer

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Fucosyltransferases are enzymes that transfer L-fucose residues from a donor substrate to target molecules. These enzymes are encoded by genes known as FUTs (FUT1 to FUT-11), along with POFUT1 and 2. Changes in FUT expression have a significant role in cancer development and malignancy. This review delves into the biochemistry and biological functions of FUTs and their contributions to cancer. Broadly, FUTs play roles in cancer tumorigenesis, survival, and metastasis. Interactions between fucosylated glycans and various molecules associated with cancer, such as E-selectins and the epidermal growth factor receptor (EGFR), offer alternative pathways for cancer development. The review also highlights FUTs as potential biomarkers for cancer prognosis and diagnosis, along with their application as targets for therapy.

Keywords:
fucosyltransferase; fucosylation; cancer; biomarkers

Gene	Chromosome Location	Exons	Recommended Protein Name	Alternative Protein Name	Short Name	Catalytic activity
POFUT1	20q11.21	9	GDP-fucose protein O-fucosyltransferase 1	Peptide-O- fucosyltransferase 1	O-FucT-1	O-fucosylation of serine/threonine hydroxyl
POFUT2	21q22.3	16	GDP-fucose protein O-fucosyltransferase 2	Peptide-O-fucosyltransferase 2	O-FucT-2	O-fucosylation of serine/threonine hydroxyl
FUT1	19q13.33	5	Galactoside alpha-(1,2)-fucosyltransferase 1	Fucosyltransferase 1	Alpha(1,2)FT 1	α-1,2 fucosylation
FUT2	19q13.33	2	Galactoside alpha-(1,2)-fucosyltransferase 2	Fucosyltransferase 2	Alpha(1,2)FT 2 or SE2	α-1,2 fucosylation
FUT3	19p13.3	5	3-galactosyl-N-acetylglucosaminide 4- alpha-L- fucosyltransferase FUT3	Fucosyltransferase 3	FucT-III	α-1,3/4 fucosylation
FUT4	11q21	1	Alpha-(1,3)-fucosyltransferase 4	Fucosyltransferase 4	Fuc-TIV or FucT-IV	α-1,3 fucosylation
FUT5	19p13.3	2	4-galactosyl-N-acetylglucosaminide 3-alpha-L-fucosyltransferase FUT5	Fucosyltransferase 5	Fuc-TV or FucT-V	α-1,3/4 fucosylation*
FUT6	19p13.3	2	4-galactosyl-N-acetylglucosaminide 3-alpha-L-fucosyltransferase FUT6	Fucosyltransferase 6	Fuc-TVI or FucT-VI	α-1,3 fucosylation
FUT7	9q34.3	2	Alpha-(1,3)-fucosyltransferase 7	Fucosyltransferase 7	Fuc-TVII or FucT-VII	α-1,3 fucosylation
FUT8	14q23.3	15	Alpha-(1,6)-fucosyltransferase	Fucosyltransferase 8	Alpha1-6FucT	α-1,6 fucosylation
FUT9	6q16.1	5	4-galactosyl-N-acetylglucosaminide 3-alpha-L-fucosyltransferase 9	Fucosyltransferase 9	Fuc-TIX or FucT-IX	α-1,3 fucosylation
FUT10	8p12	10	Alpha-(1,3)-fucosyltransferase 10	Fucosyltransferase 10	Fuc-TX or FucT-X	α-1,3 fucosylation
FUT11	10q22.2	3	Alpha-(1,3)-fucosyltransferase 11	Fucosyltransferase 11	Fuc-TXI or FucT-XI	α-1,3 fucosylation

Enzyme	Cancer	Expression Level and Biological and Clinical Impacts	References
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FUT2	Liver	High: increased Globo H antigen levels.	Wu et al. (2014)WU, C.S., YEN, C.J., CHOU, R.H., CHEN, J.N., HUANG, W.C., WU, C.Y. and YU, Y.L., 2014. Downregulation of microRNA-15b by hepatitis B virus X enhances hepatocellular carcinoma proliferation via fucosyltransferase 2-induced Globo H expression. International Journal of Cancer, vol. 134, no. 7, pp. 1638-1647. http://doi.org/10.1002/ijc.28501. PMid:24122375. http://doi.org/10.1002/ijc.28501...
FUT2	Lung	Low: decreased cell proliferation, migration and invasion; increased apoptosis.	Zhou et al. (2017)ZHOU, W., MA, H., DENG, G., TANG, L., LU, J. and CHEN, X., 2017. Clinical significance and biological function of fucosyltransferase 2 in lung adenocarcinoma. Oncotarget, vol. 8, no. 57, pp. 97246-97259. http://doi.org/10.18632/oncotarget.21896. PMid:29228607. http://doi.org/10.18632/oncotarget.21896...
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	Kidney	High: reduced OS and RFS.	Meng et al. (2017)MENG, L., XU, L., YANG, Y., ZHOU, L., CHANG, Y., SHI, T., TAN, S., AN, H., ZHU, Y. and XU, J., 2017. High expression of FUT3 is linked to poor prognosis in clear cell renal cell carcinoma. Oncotarget, vol. 8, no. 37, pp. 61036-61047. http://doi.org/10.18632/oncotarget.17717. PMid:28977844. http://doi.org/10.18632/oncotarget.17717...
	Colon/Recto	Low: reduced invasion and metastatic potential.	Hirakawa et al. (2014)HIRAKAWA, M., TAKIMOTO, R., TAMURA, F., YOSHIDA, M.M., ONO, M., MURASE, K., SATO, T., OSUGA, T., SATO, T., IYAMA, S., MIYANISHI, K., TAKADA, K., HAYASHI, T., KOBUNE, M. and KATO, J., 2014. Fucosylated TGF-β receptors transduces a signal for epithelial–mesenchymal transition in colorectal cancer cells. British Journal of Cancer, vol. 110, no. 1, pp. 156-163. http://doi.org/10.1038/bjc.2013.699. PMid:24253505. http://doi.org/10.1038/bjc.2013.699...
	Stomach	Low: reduced adhesion to endothelium via interactions with sLeX antigens and E-selectin.	Padró et al. (2011)PADRÓ, M., COBLER, L., GARRIDO, M. and DE BOLÓS, C., 2011. Down-regulation of FUT3 and FUT5 by shRNA alters Lewis antigens expression and reduces the adhesion capacities of gastric cancer cells. Biochimica et Biophysica Acta, vol. 1810, no. 12, pp. 1141-1149. http://doi.org/10.1016/j.bbagen.2011.09.011. PMid:21978830. http://doi.org/10.1016/j.bbagen.2011.09....
	Pancreas	Low: interrupted TGF-β-induced EMT.	Zhan et al. (2018)ZHAN, L., CHEN, L. and CHEN, Z., 2018. Knockdown of FUT3 disrupts the proliferation, migration, tumorigenesis and TGF-β induced EMT in pancreatic cancer cells. Oncology Letters, vol. 16, no. 1, pp. 924-930. http://doi.org/10.3892/ol.2018.8738. PMid:29963165. http://doi.org/10.3892/ol.2018.8738...
FUT4	Breast	High: increased LeY and cell proliferation and metastasis.	Zheng et al. (2017)ZHENG, Q., CUI, X., ZHANG, D., YANG, Y., YAN, X., LIU, M., NIANG, B., AZIZ, F., LIU, S., YAN, Q. and LIU, J., 2017. miR-200b inhibits proliferation and metastasis of breast cancer by targeting fucosyltransferase IV and α1,3-fucosylated glycans. Oncogenesis, vol. 6, no. 7, e358. http://doi.org/10.1038/oncsis.2017.58. PMid:28692034. http://doi.org/10.1038/oncsis.2017.58...
	Lung	High: promoted EMT	Wang et al. (2017)WANG, A., LU, C., NING, Z., GAO, W., XIE, Y., ZHANG, N., LIANG, J., ABBASI, F.S., YAN, Q. and LIU, J., 2017. Tumor-associated macrophages promote Ezrin phosphorylation-mediated epithelial-mesenchymal transition in lung adenocarcinoma through FUT4/LeY up-regulation. Oncotarget, vol. 8, no. 17, pp. 28247-28259. http://doi.org/10.18632/oncotarget.16001. PMid:28423676. http://doi.org/10.18632/oncotarget.16001...
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FUT5	Stomach	Low: reduced adhesion to endothelium via interactions with sLe antigens and E-selectin.	Padró et al. (2011)PADRÓ, M., COBLER, L., GARRIDO, M. and DE BOLÓS, C., 2011. Down-regulation of FUT3 and FUT5 by shRNA alters Lewis antigens expression and reduces the adhesion capacities of gastric cancer cells. Biochimica et Biophysica Acta, vol. 1810, no. 12, pp. 1141-1149. http://doi.org/10.1016/j.bbagen.2011.09.011. PMid:21978830. http://doi.org/10.1016/j.bbagen.2011.09....
FUT6	Colon/Recto	High: induced cellular adhesion. Low: reduced invasion and metastatic potential.	Hirakawa et al. (2014)HIRAKAWA, M., TAKIMOTO, R., TAMURA, F., YOSHIDA, M.M., ONO, M., MURASE, K., SATO, T., OSUGA, T., SATO, T., IYAMA, S., MIYANISHI, K., TAKADA, K., HAYASHI, T., KOBUNE, M. and KATO, J., 2014. Fucosylated TGF-β receptors transduces a signal for epithelial–mesenchymal transition in colorectal cancer cells. British Journal of Cancer, vol. 110, no. 1, pp. 156-163. http://doi.org/10.1038/bjc.2013.699. PMid:24253505. http://doi.org/10.1038/bjc.2013.699... ; Kanoh et al. (2003)KANOH, A., OTA, M., NARIMATSU, H. and IRIMURA, T., 2003. Expression levels of FUT6 gene transfected into human colon carcinoma cells switch two sialyl-Lewis X-related carbohydrate antigens with distinct properties in cell adhesion. Biochemical and Biophysical Research Communications, vol. 303, no. 3, pp. 896-901. http://doi.org/10.1016/S0006-291X(03)00420-0. PMid:12670495. http://doi.org/10.1016/S0006-291X(03)004...
	Liver	High: promoted cell growth, colony formation, Akt phosphorylation; suppresses p21 expression.	Guo et al. (2012)GUO, Q., GUO, B., WANG, Y., WU, J., JIANG, W., ZHAO, S., QIAO, S. and WU, Y., 2012. Functional analysis of α1,3/4-fucosyltransferase VI in human hepatocellular carcinoma cells. Biochemical and Biophysical Research Communications, vol. 417, no. 1, pp. 311-317. http://doi.org/10.1016/j.bbrc.2011.11.106. PMid:22155250. http://doi.org/10.1016/j.bbrc.2011.11.10...
	Breast	High: reduced cell migration, invasion, and proliferation. Low: increased cell migration, invasion, and proliferation.	Li et al. (2016)LI, N., LIU, Y., MIAO, Y., ZHAO, L., ZHOU, H. and JIA, L., 2016. MicroRNA-106b targets FUT6 to promote cell migration, invasion, and proliferation in human breast cancer. IUBMB Life, vol. 68, no. 9, pp. 764-775. http://doi.org/10.1002/iub.1541. PMid:27519168. http://doi.org/10.1002/iub.1541...
FUT7	Lung	High: regulated sLeX expression; promoted cell proliferation, migration, invasion and monocyte-endothelial adhesion.	Zhang et al. (2018)ZHANG, J., JU, N., YANG, X., CHEN, L. and YU, C., 2018. The α1,3-fucosyltransferase FUT7 regulates IL-1β-induced monocyte-endothelial adhesion via fucosylation of endomucin. Life Sciences, vol. 192, pp. 231-237. http://doi.org/10.1016/j.lfs.2017.11.017. PMid:29138114. http://doi.org/10.1016/j.lfs.2017.11.017... ; Liu et al. (2008)LIU, S., ZHANG, Y., LIU, Y., QIN, H., WANG, X. and YAN, Q., 2008. FUT7 antisense sequence inhibits the expression of FUT7/sLeX and adhesion between embryonic and uterine cells. IUBMB Life, vol. 60, no. 7, pp. 461-466. http://doi.org/10.1002/iub.62. PMid:18553500. http://doi.org/10.1002/iub.62...
FUT7	Bladder	High: reduced OS and RFS; stimulates proliferation, migration, invasion and EMT; increased immune cells infiltration Low: inhibited the proliferation, migration, invasion and EMT.	Liu et al. (2021)LIU, M., ZHENG, Q., CHEN, S., LIU, J. and LI, S., 2021. FUT7 Promotes the epithelial-mesenchymal transition and immune infiltration in bladder urothelial carcinoma. Journal of Inflammation Research, vol. 14, pp. 1069-1084. http://doi.org/10.2147/JIR.S296597. PMid:33790621. http://doi.org/10.2147/JIR.S296597...
FUT8	Prostate	High: influenced invasion and metastasis, tumor growth and indicated poor prognosis.	Wang et al. (2014b) WANG, X., CHEN, J., LI, Q.K., PESKOE, S.B., ZHANG, B., CHOI, C., PLATZ, E.A. and ZHANG, H., 2014b. Overexpression of α (1,6) fucosyltransferase associated with aggressive prostate cancer. Glycobiology, vol. 24, no. 10, pp. 935-944. http://doi.org/10.1093/glycob/cwu051. PMid:24906821. http://doi.org/10.1093/glycob/cwu051...
	Skin	High: influenced invasion and metastasis.	Agrawal et al. (2017)AGRAWAL, P., FONTANALS-CIRERA, B., SOKOLOVA, E., JACOB, S., VAIANA, C.A., ARGIBAY, D., DAVALOS, V., MCDERMOTT, M., NAYAK, S., DARVISHIAN, F., CASTILLO, M., UEBERHEIDE, B., OSMAN, I., FENYÖ, D., MAHAL, L.K. and HERNANDO, E., 2017. A systems biology approach identifies FUT8 as a driver of melanoma metastasis. Cancer Cell, vol. 31, no. 6, pp. 804-819.e7. http://doi.org/10.1016/j.ccell.2017.05.007. PMid:28609658. http://doi.org/10.1016/j.ccell.2017.05.0...
	Breast	High: promoted stemness and EMT.	Yang et al. (2017)YANG, H.F., YU, M., JIN, H.D., YAO, J.Q., LU, Z.L., YABASIN, I.B., YAN, Q. and WEN, Q.P., 2017. Fentanyl promotes breast cancer cell stemness and epithelial-mesenchymal transition by upregulating α1, 6-fucosylation via Wnt/β-catenin signaling pathway. Frontiers in Physiology, vol. 8, pp. 510. http://doi.org/10.3389/fphys.2017.00510. PMid:28798691. http://doi.org/10.3389/fphys.2017.00510...
	Liver	High: promoted tumorigenesis.	Wang et al. (2015)WANG, Y., FUKUDA, T., ISAJI, T., LU, J., IM, S., HANG, Q., GU, W., HOU, S., OHTSUBO, K. and GU, J., 2015. Loss of α1,6-fucosyltransferase inhibits chemical-induced hepatocellular carcinoma and tumorigenesis by down-regulating several cell signaling pathways. The FASEB Journal, vol. 29, no. 8, pp. 3217-3227. http://doi.org/10.1096/fj.15-270710. PMid:25873065. http://doi.org/10.1096/fj.15-270710...
	Lung	High: associated to poor survival and prognosis.	Honma et al. (2015)HONMA, R., KINOSHITA, I., MIYOSHI, E., TOMARU, U., MATSUNO, Y., SHIMIZU, Y., TAKEUCHI, S., KOBAYASHI, Y., KAGA, K., TANIGUCHI, N. and DOSAKA-AKITA, H., 2015. Expression of fucosyltransferase 8 is associated with an unfavorable clinical outcome in non-small cell lung cancers. Oncology, vol. 88, no. 5, pp. 298-308. http://doi.org/10.1159/000369495. PMid:25572677. http://doi.org/10.1159/000369495...
FUT9	Colon/Recto	High: increased proliferation and migration; suppresses expansion of cells and inhibits tumor development (colon cancer). Low: associated to poor survival and tumor suppression.	Auslander et al. (2017)AUSLANDER, N., CUNNINGHAM, C.E., TOOSI, B.M., MCEWEN, E.J., YIZHAK, K., VIZEACOUMAR, F.S., PARAMESWARAN, S., GONEN, N., FREYWALD, T., BHANUMATHY, K.K., FREYWALD, A., VIZEACOUMAR, F.J. and RUPPIN, E., 2017. An integrated computational and experimental study uncovers FUT9 as a metabolic driver of colorectal cancer. Molecular Systems Biology, vol. 13, no. 12, pp. 956. http://doi.org/10.15252/msb.20177739. PMid:29196508. http://doi.org/10.15252/msb.20177739... ; Shi et al. (2017)SHI, G., DU, Y., LI, Y., AN, Y., HE, Z., LIN, Y., ZHANG, R., YAN, X., ZHAO, J., YANG, S., BRENDAN, P.N.K. and LIU, F., 2017. Cell recognition molecule L1 regulates cell surface glycosylation to modulate cell survival and migration. International Journal of Medical Sciences, vol. 14, no. 12, pp. 1276-1283. http://doi.org/10.7150/ijms.20479. PMid:29104485. http://doi.org/10.7150/ijms.20479...
FUT11	Kidney	High: considered a potential biomarker for ccRCC with a non-symptomatic disease course.	Zodro et al. (2014)ZODRO, E., JAROSZEWSKI, M., IDA, A., WRZESIŃSKI, T., KWIAS, Z., BLUYSSEN, H. and WESOLY, J., 2014. FUT11 as a potential biomarker of clear cell renal cell carcinoma progression based on meta-analysis of gene expression data. Tumour Biology, vol. 35, no. 3, pp. 2607-2617. http://doi.org/10.1007/s13277-013-1344-4. PMid:24318988. http://doi.org/10.1007/s13277-013-1344-4...
POFUT1	Colon/Recto	High: Colon: promotes tumorigenesis and stemness. Recto: associated to treatment management. Low: reduces tumorigenesis.	Maftah and Germot (2019)MAFTAH, A. and GERMOT, A., 2019. POFUT1 and PLAGL2 gene pair linked by a bidirectional promoter: the two in one of tumour progression in colorectal cancer? EBioMedicine, vol. 46, pp. 25-26. http://doi.org/10.1016/j.ebiom.2019.07.065. PMid:31378697. http://doi.org/10.1016/j.ebiom.2019.07.0... ; Chabanais et al. (2018)CHABANAIS, J., LABROUSSE, F., CHAUNAVEL, A., GERMOT, A. and MAFTAH, A., 2018. POFUT1 as a Promising Novel Biomarker of Colorectal Cancer. Cancers (Basel), vol. 10, no. 11, pp. 411. http://doi.org/10.3390/cancers10110411 PMid:30380753. http://doi.org/10.3390/cancers10110411...
	Liver	High: associated to cancer progression	Ma et al. (2016)MA, L., DONG, P., LIU, L., GAO, Q., DUAN, M., ZHANG, S., CHEN, S., XUE, R. and WANG, X., 2016. Overexpression of protein O-fucosyltransferase 1 accelerates hepatocellular carcinoma progression via the Notch signaling pathway. Biochemical and Biophysical Research Communications, vol. 473, no. 2, pp. 503-510. http://doi.org/10.1016/j.bbrc.2016.03.062. PMid:27003260. http://doi.org/10.1016/j.bbrc.2016.03.06...
	Breast	High: associated to poor prognostic	Wan et al. (2017)WAN, G., TIAN, L., YU, Y., LI, F., WANG, X., LI, C., DENG, S., YU, X., CAI, X., ZUO, Z. and CAO, F., 2017. Overexpression of Pofut1 and activated Notch1 may be associated with poor prognosis in breast cancer. Biochemical and Biophysical Research Communications, vol. 491, no. 1, pp. 104-111. http://doi.org/10.1016/j.bbrc.2017.07.053. PMid:28709865. http://doi.org/10.1016/j.bbrc.2017.07.05...
	Stomach	High: correlated to aggressive tumor phenotypes and poor differentiation; considered a potential biomarker and therapeutic target.	Yokota et al. (2013)YOKOTA, S., OGAWARA, K., KIMURA, R., SHIMIZU, F., BABA, T., MINAKAWA, Y., HIGO, M., KASAMATSU, A., ENDO-SAKAMOTO, Y., SHIIBA, M., TANZAWA, H. and UZAWA, K., 2013. Protein O-fucosyltransferase 1: a potential diagnostic marker and therapeutic target for human oral cancer. International Journal of Oncology, vol. 43, no. 6, pp. 1864-1870. http://doi.org/10.3892/ijo.2013.2110. PMid:24064921. http://doi.org/10.3892/ijo.2013.2110... ; Dong et al. (2017)DONG, S., WANG, Z., HUANG, B., ZHANG, J., GE, Y., FAN, Q. and WANG, Z., 2017. Bioinformatics insight into glycosyltransferase gene expression in gastric cancer: POFUT1 is a potential biomarker. Biochemical and Biophysical Research Communications, vol. 483, no. 1, pp. 171-177. http://doi.org/10.1016/j.bbrc.2016.12.172. PMid:28040433. http://doi.org/10.1016/j.bbrc.2016.12.17...
POFUT2	Colon/Recto	High: associated to poor prognosis in colon adenocarcinoma	Wang et al. (2023)WANG, P., LIU, X., YU, J., MENG, Z., LV, Z., SHANG, C., GENG, Q., WANG, D., XUE, D. and LI, L., 2023. Fucosyltransferases regulated by fusobacterium nucleatum and act as novel biomarkers in colon adenocarcinoma. Journal of Inflammation Research, vol. 16, pp. 747-768. http://doi.org/10.2147/JIR.S396484. PMid:36852302. http://doi.org/10.2147/JIR.S396484...

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