A lectin-based approach to detecting carcinogenesis in breast tissue

Wi,Ga  Ram; Moon,Byung‑In; Kim,Hyoung  Jin; Lim,Woosung; Lee,Anbok; Lee,Jun  Woo; Kim,Hong‑Jin

doi:10.3892/ol.2016.4456

A lectin-based approach to detecting carcinogenesis in breast tissue

Authors:
- Ga Ram Wi
- Byung‑In Moon
- Hyoung Jin Kim
- Woosung Lim
- Anbok Lee
- Jun Woo Lee
- Hong‑Jin Kim
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Affiliations: Laboratory of Virology, College of Pharmacy, Chung‑Ang University, Dongjak‑Gu, Seoul 156‑756, Republic of Korea, Breast and Thyroid Cancer Center, Ewha Womans University College of Medicine, Yangcheon‑Gu, Seoul 06974, Republic of Korea
Published online on: April 18, 2016 https://doi.org/10.3892/ol.2016.4456
Pages: 3889-3895

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Abstract

It has been suggested that the diversity of glycosylation structures that form during cancer progression and the sensitivity with which they are able to be detected have great potential for cancer screening. However, the large majority of breast cancer research has instead focused on the development of protein or nucleic acid markers. In the present study, alterations in glycosylation in breast cancer tissue were analyzed using enzyme‑linked lectin assays (ELLAs), which have potential for high‑throughput screening. Cancer tissues (CCs) and normal tissues (CNs) were collected from women with breast cancer ranging from stage 0 to IIIA. The specimens were divided into two groups, stage 0‑I and stage II‑III, and the levels of four types of lectin in stage 0‑I and stage II‑III CCs and CNs were compared by ELLA. The results demonstrated that, relative to CNs, the CCs contained significantly enhanced levels of mannosylation (stage 0‑I, P<0.001; stage II‑III, P<0.001), galactosylation (stage 0‑I, P<0.05; stage II‑III, P<0.001), sialylation (stage 0‑I, P<0.001; stage II‑III, P<0.01) and fucosylation (stage 0‑I, P<0.01; stage II‑III, P<0.01). Furthermore, stage II‑III CCs had higher levels of mannosylation (P<0.05) and galactosylation (P<0.01) than stage 0‑I CCs. The sensitivity of the ELLA system ranged from 71‑100% when specificity was set at 100%. These results demonstrate that enhanced glycosylation levels identified by ELLA are associated with the development of breast tumors, and provide evidence of the exceptional sensitivity and specificity of the ELLA system in the detection of breast cancer. This approach is anticipated to contribute highly to the development of reliable diagnostic procedures for breast cancer.

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1	Donepudi MS, Kondapalli K, Amos SJ and Venkanteshan P: Breast cancer statistics and markers. J Cancer Res Ther. 10:506–511. 2014.PubMed/NCBI
2	Cancer Genome Atlas Network: Comprehensive molecular portraits of human breast tumours. Nature. 490:61–70. 2012. View Article : Google Scholar : PubMed/NCBI
3	Kolb TM, Lichy J and Newhouse JH: Comparison of the performance of screening mammography, physical examination and breast US and evaluation of factors that influence them: An analysis of 27, 825 patient evaluations. Radiology. 225:165–175. 2002. View Article : Google Scholar : PubMed/NCBI
4	Alexander H, Stegner AL, Wagner-Mann C, Du Bois GC, Alexander S and Sauter ER: Proteomic analysis to identify breast cancer biomarkers in nipple aspirate fluid. Clin Cancer Res. 10:7500–7510. 2004. View Article : Google Scholar : PubMed/NCBI
5	Ahmed HG: Impact of implementing grading fine needle aspiration cytology in diagnosis of breast cancer amongst sudanese women. Oman Med J. 26:99–103. 2011. View Article : Google Scholar : PubMed/NCBI
6	Polyak K: Heterogeneity in breast cancer. J Clin Invest. 121:3786–3788. 2011. View Article : Google Scholar : PubMed/NCBI
7	Esteva FJ and Hortobagyi GN: Prognostic molecular markers in early breast cancer. Breast Cancer Res. 6:109–118. 2004. View Article : Google Scholar : PubMed/NCBI
8	Malhotra GK, Zhao X, Band H and Band V: Histological, molecular and functional subtypes of breast cancers. Cancer Biol Ther. 10:955–960. 2010. View Article : Google Scholar : PubMed/NCBI
9	Grunewald S, Matthijs G and Jaeken J: Congenital disorders of glycosylation: A review. Pediatr Res. 52:618–624. 2002. View Article : Google Scholar : PubMed/NCBI
10	Li M, Song L and Qin X: Glycan changes: Cancer metastasis and anti-cancer vaccines. J Biosci. 35:665–673. 2010. View Article : Google Scholar : PubMed/NCBI
11	Reis CA, Osorio H, Silva L, Gomes C and David L: Alterations in glycosylation as biomarkers for cancer detection. J Clin Pathol. 63:322–329. 2010. View Article : Google Scholar : PubMed/NCBI
12	Peracaula R, Barrabés S, Sarrats A, Rudd PM and de Llorens R: Altered glycosylation in tumours focused to cancer diagnosis. Dis Markers. 25:207–218. 2008. View Article : Google Scholar : PubMed/NCBI
13	van de Vijver MJ: Molecular tests as prognostic factors in breast cancer. Virchows Arch. 464:283–291. 2014. View Article : Google Scholar : PubMed/NCBI
14	Hirabayashi J: Concept, strategy and realization of lectin-based glycan profiling. J Biochem. 144:139–147. 2008. View Article : Google Scholar : PubMed/NCBI
15	Thompson R, Creavin A, O'Connell M, O'Connor B and Clarke P: Optimization of the enzyme-linked lectin assay for enhanced glycoprotein and glycoconjugate analysis. Anal Biochem. 413:114–122. 2011. View Article : Google Scholar : PubMed/NCBI
16	Kim HJ, Lee SJ and Kim HJ: Antibody-based enzyme-linked lectin assay (ABELLA) for the sialylated recombinant human erythropoietin present in culture supernatant. J Pharm Biomed Anal. 48:716–721. 2008. View Article : Google Scholar : PubMed/NCBI
17	Kim HJ, Lee DH, Kim DK, Han GB and Kim HJ: The glycosylation and in vivo stability of human granulocyte-macrophage colony-stimulating factor produced in rice cells. Biol Pharm Bull. 31:290–294. 2008. View Article : Google Scholar : PubMed/NCBI
18	Kim HJ, Kim SC, Ju W, Kim YH, Yin SY and Kim HJ: Aberrant sialylation and fucosylation of intracellular proteins in cervical tissue are critical markers of cervical carcinogenesis. Oncol Rep. 31:1417–1422. 2014.PubMed/NCBI
19	Harris JR: Natural history and staging of breast cancer. Diseases of the Breast. Harris JR, Lippman ME, Morrow M and Osborne CK: (1st). Lippincott-Raven. (Baltimore, PA). 457–459. 1996.
20	Chen GY, Chen CY, Chang MDT, Matsuura Y and Hu YC: Concanavalin A affinity chromatography for efficient baculovirus purification. Biotechnol Prog. 25:1669–1677. 2009.PubMed/NCBI
21	Clark D and Mao L: Cancer biomarker discovery: Lectin-based strategies targeting glycoproteins. Dis Markers. 33:1–10. 2012. View Article : Google Scholar : PubMed/NCBI
22	Hirabayashi J, Kuno A and Tateno H: Lectin-based structural glycomics: A practical approach to complex glycans. Electrophoresis. 32:1118–1128. 2011. View Article : Google Scholar : PubMed/NCBI
23	Renkonen J, Paavonen T and Renkonen R: Endothelial and epithelial expression of sialyl Lewis(x) and sialyl Lewis(a) in lesions of breast carcinoma. Int J Cancer. 74:296–300. 1997. View Article : Google Scholar : PubMed/NCBI
24	Imai J, Ghazizadeh M, Naito Z and Asano G: Immunohistochemical expression of T, Tn and sialyl-Tn antigens and clinical outcome in human breast carcinoma. Anticancer Res. 21(2B): 1327–1334. 2001.PubMed/NCBI
25	Jeschke U, Mylonas I, Shabani N, Kunert-Keil C, Schindlbeck C, Gerber B and Friese K: Expression of sialyl lewis X, sialyl Lewis A, E-cadherin and cathepsin-D in human breast cancer: Immunohistochemical analysis in mammary carcinoma in situ, invasive carcinomas and their lymph node metastasis. Anticancer Res. 25(3A): 1615–1622. 2005.PubMed/NCBI
26	Christiansen MN, Chik J, Lee L, Anugraham M, Abrahams JL and Packer NH: Cell surface protein glycosylation in cancer. Proteomics. 14:525–546. 2014. View Article : Google Scholar : PubMed/NCBI
27	Häuselmann I and Borsig L: Altered tumor-cell glycosylation promotes metastasis. Front Oncol. 4:282014. View Article : Google Scholar : PubMed/NCBI
28	Miyoshi E, Moriwaki K, Terao N, Tan CC, Terao M, Nakagawa T, Matsumoto H, Shinzaki S and Kamada Y: Fucosylation is a promising target for cancer diagnosis and therapy. Biomolecules. 2:34–45. 2012. View Article : Google Scholar : PubMed/NCBI
29	Van Elssen CH, Frings PW, Bot FJ, Van de Vijver KK, Huls MB, Meek B, Hupperets P, Germeraad WT and Bos GM: Expression of aberrantly glycosylated Mucin-1 in ovarian cancer. Histopathology. 57:597–606. 2010. View Article : Google Scholar : PubMed/NCBI
30	Liu H, Zhang N, Wan D, Cui M, Liu Z and Liu S: Mass spectrometry-based analysis of glycoproteins and its clinical applications in cancer biomarker discovery. Clin Proteomics. 11:142014. View Article : Google Scholar : PubMed/NCBI
31	Holst S, Stavenhagen K, Balog CI, Koeleman CA, McDonnell LM, Mayboroda OA, Verhoeven A, Mesker WE, Tollenaar RA, Deelder AM and Wuhrer M: Investigations on aberrant glycosylation of glycosphingolipids in colorectal cancer tissues using liquid chromatography and matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF-MS). Mol Cell Proteomics. 12:3081–3093. 2013. View Article : Google Scholar : PubMed/NCBI
32	de Leoz ML, Young LJ, An HJ, Kronewitter SR, Kim J, Miyamoto S, Borowsky AD, Chew HK and Lebrilla CB: High-mannose glycans are elevated during breast cancer progression. Mol Cell Proteomics. 10:M110.0027172011. View Article : Google Scholar : PubMed/NCBI
33	Weedon-Fekjaer H, Romundstad PR and Vatten LJ: Modern mammography screening and breast cancer mortality: Population study. BMJ. 348:g37012014. View Article : Google Scholar : PubMed/NCBI
34	Papanicolaou GN, Holmquist DG, Bader GM and Falk EA: Exioliative cytology of the human mammary gland and its value in the diagnosis of cancer and other diseases of the breast. Cancer. 11:377–409. 1958. View Article : Google Scholar : PubMed/NCBI
35	Harigopal M and Chhieng DC: Breast cytology: Current issues and future directions. The Open Breast Cancer Journal. 2:81–89. 2010.