Decreased expression of Bauhinia purpurea lectin is a predictor of gastric cancer recurrence

Abstract

Purpose

Molecular markers as indicators for gastric cancer recurrence are urgently required. The aim of this study was to identify lectins that can be used to predict gastric cancer recurrence after gastrectomy.

Methods

We created lectin expression profiles by microarray analysis for 60 patients, who underwent surgery for gastric cancer at the Oita University Hospital between January, 2005 and December, 2007. Lectin expression and clinicopathological factors in patients who suffered gastric cancer recurrence and those who did not were compared by univariate and multivariate analyses.

Results

Thirteen lectins showed a significant increase in binding to cancer tissues, whereas 11 lectins showed a significant decrease in binding to cancer tissues, when compared with binding to normal epithelia. Multivariate analysis revealed that lymph node metastasis and low Bauhinia purpurea lectin (BPL)-binding signals were independent predictive factors for recurrence. All patients with low BPL expression had significantly worse relapse-free survival than those with high BPL expression.

Conclusions

Our results using a novel lectin microarray system provide the first solid evidence that BPL expression is a predictor of gastric cancer recurrence.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Abbreviations

CEA:

Carcinoembryonic antigen

CA19-9:

Carbohydrate antigen 19-9

HER2:

Human epidermal growth factor receptor 2

EGFR:

Epidermal growth factor receptor

CD44:

Cluster of differentiation 44

ROC:

Receiver operating characteristic

LCA:

Lens culinaris agglutinin

MAL-I:

Maackia amurensis lectin I

SNA:

Sambucus nigra agglutinin

SSA:

Sambucus sieboldiana agglutinin

TJA-I:

Trichosanthes japonica agglutinin I

NPA:

Narcissus pseudonarcissus lectin

ConA:

Concanavalin A

GNA:

Galanthus nivalis agglutinin

HHL:

Hippeastrum hybrid lectin

ACG:

Agrocybe cylindracea galectin

TxLC-I:

Tulipa gesneriana I

MAH:

Maackia amurensis hemagglutinin

UEA-I:

Ulex europaeus agglutinin I

AOL:

Aspergillus oryzae lectin

AAL:

Aleuria aurantia lectin

BPL:

Bauhinia purpurea lectin

EEL:

Euonymus europaeus lectin

ABA:

Agaricus bisporus agglutinin

WFA:

Wisteria floribunda lectin

ACA:

Amaranthus caudatus agglutinin

DBA:

Dolichos biflorus agglutinin

SBA:

Soybean agglutinin

GSL-I-A4:

Griffonia simplicifolia

References

  1. 1.

    Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127:2893–917.

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Bang Y-J, Kim Y-W, Yang H-K, Chung HC, Park Y-K, Lee KH, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet. 2012;379:315–21.

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJH, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20.

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Sasako M, Sakuramoto S, Katai H, Kinoshita T, Furukawa H, Yamaguchi T, et al. Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol. 2011;29(33):4387–93.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Msika S, Benhamiche A, Jouve J-L, Rat P, Faivre J. Prognostic factors after curative resection of gastric cancer: a population-based study. Eur J Cancer. 2000;36:390–6.

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Dicken BJ, Graham K, Hamilton SM, Andrews S, Lai R, Listgarten J, et al. Lymphovascular invasion is associated with poor survival in gastric cancer: an application of gene-expression and tissue array techniques. Ann Surg. 2006;243:64–73.

    Article  PubMed Central  PubMed  Google Scholar 

  7. 7.

    Kunisaki C, Makino H, Kimura J, Takagawa R, Kosaka T, Ono HA, et al. Impact of lymphovascular invasion in patients with stage I gastric cancer. Surgery. 2010;147:204–11.

    Article  PubMed  Google Scholar 

  8. 8.

    Nakayama Y, Gotohda N, Shibasaki H, Nomura S, Kinoshita T, Hayashi R. Usefulness of the neutron/lymphocyte ratio measured preoperatively as a predictor of peritoneal metastasis in patients with advanced gastric cancer. Surg Today. 2014;44:2146–52.

    Article  PubMed  Google Scholar 

  9. 9.

    Takahashi Y, Takeuchi T, Sakamoto J, Touge T, Mai M, Ohkura H, et al. The usefulness of CEA and/or CA19-9 in monitoring for recurrence in gastric cancer patients: a prospective clinical study. Gastric Cancer. 2003;6:142–5.

    Article  PubMed  Google Scholar 

  10. 10.

    Jørgensen JT, Hersom M. HER2 as a prognostic marker in gastric cancer—a systematic analysis of data from the literature. J Cancer. 2012;3:137–44.

    Article  PubMed Central  PubMed  Google Scholar 

  11. 11.

    Terashima M, Kitada K, Ochiai A, Ichikawa W, Kurahashi I, Sakuramoto S, et al. Impact of expression of human epidermal growth factor receptors EGFR and ERBB2 on survival in stage II/III gastric cancer. Clin Cancer Res. 2012;18:5992–6000.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Shimada Y, Yamasaki S, Hashimoto Y, Ito T, Kawamura J, Soma T, et al. Clinical significance of dysadherin expression in gastric cancer patients. Clin Cancer Res. 2004;10:2818–23.

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Yamamichi K, Uehara Y, Kitamura N, Nakane Y, Hioki K. Increased expression of CD44v6 mRNA significantly correlates with distant metastasis and poor prognosis in gastric cancer. Int J Cancer (Pred Oncol). 1998;79:256–62.

    CAS  Article  Google Scholar 

  14. 14.

    Kodera Y, Nakanishi H, Ito S, Yamamura Y, Fujiwara M, Koike M, et al. Prognostic significance of intraperitoneal cancer cells in gastric carcinoma: detection of cytokeratin 20 mRNA in peritoneal washes, in addition to detection of carcinoembryonic antigen. Gastric Cancer. 2005;8:142–8.

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology. 1993;3:97–130.

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Park JH, Nishidate T, Kijima K, Ohashi T, Takegawa K, Fujikane T, et al. Critical roles of mucin 1 glycosylation by transactivated polypeptide N-acetylgalactosaminyltransferase 6 in mammary carcinogenesis. Cancer Res. 2010;70:2759–69.

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Lange T, Ullrich S, Muller I, Nentwich MF, Stubke K, Feldhaus S, et al. Human prostate cancer in a clinically relevant xenograft mouse model: identification of beta(1,6)-branched oligosaccharides as a marker of tumor progression. Clin Cancer Res. 2012;18:1364–73.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Chen G, Wang Y, Qiu L, Qiu X, Liu H, Wang X, et al. Human IgG Fc-glycosylation profiling reveals associations with age, sex, female sex hormones and thyroid cancer. J Proteomics. 2012;75:2824–34.

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Saldova R, Dempsey E, Perez-Garay M, Marino K, Watson JA, Blanco-Fernandez A, et al. 5-AZA-2′-deoxycytidine induced demethylation influences N-glycosylation of secreted glycoproteins in ovarian cancer. Epigenetics. 2011;6:1362–72.

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Fry SA, Afrough B, Lomax-Browne HJ, Timms JF, Velentzis LS, Leathem AJ. Lectin microarray profiling of metastatic breast cancers. Glycobiology. 2011;21:1060–70.

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Matsuda A, Kuno A, Ishida H, Kawamoto T, Shoda J, Hirabayashi J. Development of an all-in-one technology for glycan profiling targeting formalin-embedded tissue sections. Biochem Biophys Res Commun. 2008;370:259–63.

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Nishijima Y, Toyoda M, Yamazaki-Inoue M, Sugiyama T, Miyazawa M, Muramatsu T, et al. Glycan profiling of endometrial cancers using lectin microarray. Genes Cells. 2012;17:826–36.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Nakajima T, Inomata M, Iha H, Hiratsuka T, Etoh T, Shiraishi N, et al (2015) Establishment of new predictive markers for distant recurrence of colorectal cancer using lectin microarray analysis. Cancer Medicine (in press).

  24. 24.

    Sobin LH, Gospodarowicz MK, Wittekind C. International Union Against Cancer (UICC) TNM classification of malignant tumors, 7th edition, Oxford. UK: Wiley-Blackwell; 2009.

    Google Scholar 

  25. 25.

    Huang W-L, Li Y-G, Lv Y-C, Guan X-H, Ji H-F, Chi B-R. Use of lectin microarray to differentiate gastric cancer from gastric ulcer. World J Gastroenterol. 2014;20(18):5474–82.

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  26. 26.

    Vanderschaeghe D, Festjens N, Delanghe J, Callewaert N. Glycome profiling using modern glycomics technology: technical aspects and applications. Biol Chem. 2010;391:149–61.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Wu AM, Kabat EA, Gruezo FG, Allen HJ. Immunochemical studies on the combining site of the D-Galactopyranose and 2-Acetamid-2-deoxy-D-Galactopyranose specific lectin isolated from Bauhinia purpurea alba seeds. Arch Biochem Biophys. 1980;204:622–39.

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Yamamoto K, Maruyama IN, Osawa T. Cybrog lectins: novel leguminous lectins with unique specificities. J Biochem. 2000;127:137–42.

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Iramura T, Osawa T. Studies on a hemagglutinin from Bauhinia purpurea alba seeds. Arch Biochem Biophys. 1972;151:475–81.

    Article  Google Scholar 

  30. 30.

    Shiratsu K, Higuchi K, Nakayama J. Loss of gastric gland mucin-specific O-glycan is associated with progression of differentiated-type adenocarcinoma of the stomach. Cancer Sci. 2014;105:126–33.

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Karasawa F, Shiota A, Goso Y, Kobayashi M, Sato Y, Masumoto J, et al. Essential role of gastric gland mucin in preventing gastric cancer in mice. J Clin Invest. 2012;122:923–34.

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  32. 32.

    Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006;441:431–6.

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Takahashi H, Ogata H, Nishigaki R, Broide DH, Karin M. Tobacco smoke promotes lung tumorigenesis by triggering IKKb and JNK1 dependent inflammation. Cancer Cell. 2010;17(1):89–97.

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  34. 34.

    Grivennikov SI, Greten FR, Karin M. Immunity, Inflammation, and Cancer. Cell. 2010;140(6):883–99.

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  35. 35.

    Ohkura H. Tumor markers in monitoring response to chemotherapy for patients with gastric cancer. Jpn J Clin Oncol. 1999;29:525–6.

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Yamao T, Kai S, Kazami A, Koizumi K, Handa T, Takemoto N, Maruyama M. Tumor markers CEA, CA19-9 and CA125 in monitoring of response to systemic chemotherapy in patients with advanced gastric cancer. Jpn J Clin Oncol. 1999;29:550–5.

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Pectasides D, Mylonakis A, Kostopoulou M, Papadopoulou M, Triantafillis D, Varthalitis J, et al. CEA, CA 19-9, and CA-50 in monitoring gastric carcinoma. Am J Clin Oncol. 1997;20:348–53.

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Kodama I, Koufuji K, Kawabata S, Tetsu S, Tsuji Y, Takeda J, Kakegawa T. The clinical efficacy of CA 72-4 as serum marker for gastric cancer in comparison with CA19-9 and CEA. Int Surg. 1995;80:45–8.

    CAS  PubMed  Google Scholar 

  39. 39.

    Adachi Y, Yasuda K, Inomata M, Sato K, Shiraishi N, Kitano S. Pathology and prognosis of gastric carcinoma: well versus poorly differentiated type. Cancer. 2000;89(7):1418–24.

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Li C, Oh SJ, Kim S, Hyung WJ, Yan M, Zhu ZG, Noh SH. Macroscopic Borrmann type as a simple prognostic indicator in patients with advanced gastric cancer. Oncology. 2009;77(3–4):197–204.

    Article  PubMed  Google Scholar 

  41. 41.

    Baiocchi GL, Tiberio GA, Minicozzi AM, Morgagni P, Marrelli D, Bruno L, et al. A multicentric Western analysis of prognostic factors in advanced, node-negative gastric cancer patients. Ann Surg. 2010;252(1):70–3.

    Article  PubMed  Google Scholar 

  42. 42.

    Adachi Y, Oshiro T, Mori M, Maehara Y, Sugimachi K. Tumor size as a simple prognostic indicator for gastric carcinoma. Ann Surg Oncol. 1997;4(2):137–40.

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported, in part, by Grants-in-Aid for Scientific Research from the Japanese Society for the Promotion of Science (24591953). We thank Ms. Mayumi Takeda, Ms. Hiroko Taguchi, Ms. Yuiko Aso, and Ms. Maki Fujinaga for technical assistance.

Conflict of interest

T. Futsukaichi and his coauthors declare no conflicts of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tsuyoshi Etoh.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Futsukaichi, T., Etoh, T., Nakajima, K. et al. Decreased expression of Bauhinia purpurea lectin is a predictor of gastric cancer recurrence. Surg Today 45, 1299–1306 (2015). https://doi.org/10.1007/s00595-015-1127-1

Download citation

Keywords

  • Bauhinia purpurea lectin
  • Lectin microarray
  • Gastric cancer
  • Recurrence
  • Glycan