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. 1999 Aug;80(11):1754–1762. doi: 10.1038/sj.bjc.6690593

Wheatgerm agglutinin-mediated toxicity in pancreatic cancer cells

R E Schwarz 1, D C Wojciechowicz 1, A I Picon 1, M A Schwarz 2,2, P B Paty 1
PMCID: PMC2363124  PMID: 10468292

Abstract

Lectin binding specificities for carbohydrate allow phenotypic and functional characterization of membrane-associated glycoproteins expressed on cancer cells. This analysis examined wheatgerm agglutinin binding to pancreatic cancer cells in vitro and the resulting toxicity. Membrane preparations of nine human pancreatic carcinoma cell lines were studied for lectin binding using wheatgerm agglutinin (WGA), concanavalin A (ConA) and phytohaemagglutinin-L (PHA-L) in a lectin blot analysis. Cell proliferation in vitro was measured by thymidine incorporation in the absence or presence of lectins at various concentrations. Sialic acid binding lectins or succinyl-WGA (succWGA) served as controls. WGA toxicity was tested after swainsonine or neuraminidase pretreatment. Binding and uptake of fluorescein-labelled lectins was studied under fluorescence microscopy. All pancreatic cell lines displayed high WGA membrane binding, primarily to sialic acid residues. Other lectins were bound with weak to moderate intensity only. Lectin toxicity corresponded to membrane binding intensity, and was profound in case of WGA (ID50 at 2.5–5 μg ml−1). WGA exposure induced chromatin condensation, nuclear fragmentation and DNA release consistent with apoptosis. Important steps for WGA toxicity included binding to sialic acid on swainsonine-sensitive carbohydrate and lectin internalization. There was rapid cellular uptake and subsequent nuclear relocalization of WGA. In contradistinction to the other lectins studied, WGA proved highly toxic to human pancreatic carcinoma cells in vitro. WGA binding to sialic acid residues of N-linked carbohydrate, cellular uptake and subsequent affinity to N-acetyl glucosamine appear to be necessary steps. Further analysis of this mechanism of profound toxicity may provide insight relevant to the treatment of pancreatic cancer. © 1999 Cancer Research Campaign

Keywords: wheatgerm agglutinin, pancreatic cancer, lectin, apoptosis, sialic acid surface binding, swainsonine

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Selected References

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  1. Adam E. J., Adam S. A. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J Cell Biol. 1994 May;125(3):547–555. doi: 10.1083/jcb.125.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aoki D., Nozawa S., Iizuka R., Kawakami H., Hirano H. Differences in lectin binding patterns of normal endometrium and endometrial adenocarcinoma, with special reference to staining with Ulex europeus agglutinin 1 and peanut agglutinin. Gynecol Oncol. 1990 Jun;37(3):338–345. doi: 10.1016/0090-8258(90)90364-q. [DOI] [PubMed] [Google Scholar]
  3. Beltinger C., Saragovi H. U., Smith R. M., LeSauteur L., Shah N., DeDionisio L., Christensen L., Raible A., Jarett L., Gewirtz A. M. Binding, uptake, and intracellular trafficking of phosphorothioate-modified oligodeoxynucleotides. J Clin Invest. 1995 Apr;95(4):1814–1823. doi: 10.1172/JCI117860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bresalier R. S., Rockwell R. W., Dahiya R., Duh Q. Y., Kim Y. S. Cell surface sialoprotein alterations in metastatic murine colon cancer cell lines selected in an animal model for colon cancer metastasis. Cancer Res. 1990 Feb 15;50(4):1299–1307. [PubMed] [Google Scholar]
  5. Burrus G. R., Schmidt W. N., Briggs J. A., Hnilica L. S., Briggs R. C. Lectin-binding proteins in nuclear preparations from rat liver and malignant tumors. Cancer Res. 1988 Feb 1;48(3):551–555. [PubMed] [Google Scholar]
  6. Bustamante J. O., Liepins A., Hanover J. A. Nuclear pore complex ion channels (review). Mol Membr Biol. 1994 Jul-Sep;11(3):141–150. doi: 10.3109/09687689409162232. [DOI] [PubMed] [Google Scholar]
  7. Ching C. K., Black R., Helliwell T., Savage A., Barr H., Rhodes J. M. Use of lectin histochemistry in pancreatic cancer. J Clin Pathol. 1988 Mar;41(3):324–328. doi: 10.1136/jcp.41.3.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dansey R., Murray J., Ninin D., Bezwoda W. R. Lectin binding in human breast cancer: clinical and pathologic correlations with fluorescein-conjugated peanut, wheat germ and concanavalin A binding. Oncology. 1988;45(4):300–302. doi: 10.1159/000226627. [DOI] [PubMed] [Google Scholar]
  9. Dargemont C., Schmidt-Zachmann M. S., Kühn L. C. Direct interaction of nucleoporin p62 with mRNA during its export from the nucleus. J Cell Sci. 1995 Jan;108(Pt 1):257–263. doi: 10.1242/jcs.108.1.257. [DOI] [PubMed] [Google Scholar]
  10. Dennis J. W. Different metastatic phenotypes in two genetic classes of wheat germ agglutinin-resistant tumor cell mutants. Cancer Res. 1986 Sep;46(9):4594–4600. [PubMed] [Google Scholar]
  11. Dennis J. W. Effects of swainsonine and polyinosinic:polycytidylic acid on murine tumor cell growth and metastasis. Cancer Res. 1986 Oct;46(10):5131–5136. [PubMed] [Google Scholar]
  12. Dennis J. W., Koch K., Beckner D. Inhibition of human HT29 colon carcinoma growth in vitro and in vivo by swainsonine and human interferon-alpha 2. J Natl Cancer Inst. 1989 Jul 5;81(13):1028–1033. doi: 10.1093/jnci/81.13.1028. [DOI] [PubMed] [Google Scholar]
  13. Dennis J. W., Laferte S. Co-reversion of a lectin-resistant mutation and non-metastatic phenotype in murine tumor cells. Int J Cancer. 1986 Sep 15;38(3):445–450. doi: 10.1002/ijc.2910380322. [DOI] [PubMed] [Google Scholar]
  14. Dennis J. W., Laferte S. Tumor cell surface carbohydrate and the metastatic phenotype. Cancer Metastasis Rev. 1987;5(3):185–204. doi: 10.1007/BF00046998. [DOI] [PubMed] [Google Scholar]
  15. Dennis J. W., Laferté S., Fukuda M., Dell A., Carver J. P. Asn-linked oligosaccharides in lectin-resistant tumor-cell mutants with varying metastatic potential. Eur J Biochem. 1986 Dec 1;161(2):359–373. doi: 10.1111/j.1432-1033.1986.tb10455.x. [DOI] [PubMed] [Google Scholar]
  16. Dennis J. W., Laferté S., Waghorne C., Breitman M. L., Kerbel R. S. Beta 1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science. 1987 May 1;236(4801):582–585. doi: 10.1126/science.2953071. [DOI] [PubMed] [Google Scholar]
  17. Dennis J. W. Partial reversion of the metastatic phenotype in a wheat germ agglutinin-resistant mutant of the murine tumor cell line MDAY-D2 selected with Bandeiraea simplicifolia seed lectin. J Natl Cancer Inst. 1985 May;74(5):1111–1120. [PubMed] [Google Scholar]
  18. Finne J., Burger M. M., Prieels J. P. Enzymatic basis for a lectin-resistant phenotype: increase in a fucosyltransferase in mouse melanoma cells. J Cell Biol. 1982 Feb;92(2):277–282. doi: 10.1083/jcb.92.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Finne J., Tao T. W., Burger M. M. Carbohydrate changes in glycoproteins of a poorly metastasizing wheat germ agglutinin-resistant melanoma clone. Cancer Res. 1980 Jul;40(7):2580–2587. [PubMed] [Google Scholar]
  20. Gorelik E., Duty L., Anaraki F., Galili U. Alterations of cell surface carbohydrates and inhibition of metastatic property of murine melanomas by alpha 1,3 galactosyltransferase gene transfection. Cancer Res. 1995 Sep 15;55(18):4168–4173. [PubMed] [Google Scholar]
  21. Gorelik E., Kim M., Duty L., Henion T., Galili U. Control of metastatic properties of BL6 melanoma cells by H-2Kb gene: immunological and nonimmunological mechanisms. Clin Exp Metastasis. 1993 Nov;11(6):439–452. doi: 10.1007/BF00054935. [DOI] [PubMed] [Google Scholar]
  22. Heese-Peck A., Cole R. N., Borkhsenious O. N., Hart G. W., Raikhel N. V. Plant nuclear pore complex proteins are modified by novel oligosaccharides with terminal N-acetylglucosamine. Plant Cell. 1995 Sep;7(9):1459–1471. doi: 10.1105/tpc.7.9.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ho J. J., Chung Y. S., Fujimoto Y., Bi N., Ryan W., Yuan S. Z., Byrd J. C., Kim Y. S. Mucin-like antigens in a human pancreatic cancer cell line identified by murine monoclonal antibodies SPan-1 and YPan-1. Cancer Res. 1988 Jul 15;48(14):3924–3931. [PubMed] [Google Scholar]
  24. Hohenberger P., Liewald F., Schlag P., Herfarth C. Lectins and immunohistochemistry of colorectal cancer, its recurrences and metastases. Eur J Surg Oncol. 1990 Aug;16(4):289–297. [PubMed] [Google Scholar]
  25. Ishikawa M., Dennis J. W., Man S., Kerbel R. S. Isolation and characterization of spontaneous wheat germ agglutinin-resistant human melanoma mutants displaying remarkably different metastatic profiles in nude mice. Cancer Res. 1988 Feb 1;48(3):665–670. [PubMed] [Google Scholar]
  26. Ishikawa M., Kerbel R. S. Characterization of a metastasis-deficient lectin-resistant human melanoma mutant. Int J Cancer. 1989 Jan 15;43(1):134–139. doi: 10.1002/ijc.2910430125. [DOI] [PubMed] [Google Scholar]
  27. Jett M., Jamieson G. A. Comparison of binding sites for wheat germ agglutinin on Raji lymphoblastoid cells and their isolated nuclei and plasma membranes. Biochemistry. 1981 Sep 1;20(18):5221–5226. doi: 10.1021/bi00521a019. [DOI] [PubMed] [Google Scholar]
  28. Kakeji Y., Maehara Y., Tsujitani S., Baba H., Ohno S., Watanabe A., Sugimachi K. Helix pomatia agglutinin binding activity and lymph node metastasis in patients with gastric cancer. Semin Surg Oncol. 1994 Mar-Apr;10(2):130–134. doi: 10.1002/ssu.2980100214. [DOI] [PubMed] [Google Scholar]
  29. Kameda Y., Hirota C., Miyauchi R. Staining of pancreatic centroacinar cells, liver bile canaliculi and testicular Leydig cells with a monoclonal antibody against adrenocortical cells. Cell Tissue Res. 1993 Jun;272(3):407–416. doi: 10.1007/BF00318547. [DOI] [PubMed] [Google Scholar]
  30. Kellokumpu I., Karhi K., Andersson L. C. Lectin-binding sites in normal, hyperplastic, adenomatous and carcinomatous human colorectal mucosa. Acta Pathol Microbiol Immunol Scand A. 1986 Jul;94(4):271–280. doi: 10.1111/j.1699-0463.1986.tb02994.x. [DOI] [PubMed] [Google Scholar]
  31. Kerbel R. S., Dennis J. W., Largarde A. E., Frost P. Tumor progression in metastasis: an experimental approach using lectin resistant tumor variants. Cancer Metastasis Rev. 1982;1(2):99–140. doi: 10.1007/BF00048223. [DOI] [PubMed] [Google Scholar]
  32. Kim M., Rao M. V., Tweardy D. J., Prakash M., Galili U., Gorelik E. Lectin-induced apoptosis of tumour cells. Glycobiology. 1993 Oct;3(5):447–453. doi: 10.1093/glycob/3.5.447. [DOI] [PubMed] [Google Scholar]
  33. Kita K., Omata S., Horigome T. Purification and characterization of a nuclear pore glycoprotein complex containing p62. J Biochem. 1993 Mar;113(3):377–382. doi: 10.1093/oxfordjournals.jbchem.a124054. [DOI] [PubMed] [Google Scholar]
  34. Kramer R. H., Canellakis E. S. The surface glycoproteins of the HeLa cell. Internalization of wheat germ agglutinin-receptors. Biochim Biophys Acta. 1979 Mar 8;551(2):328–348. doi: 10.1016/0005-2736(89)90010-2. [DOI] [PubMed] [Google Scholar]
  35. Kurisu M., Yamazaki M., Mizuno D. Induction of macrophage-mediated tumor lysis by the lectin wheat germ agglutinin. Cancer Res. 1980 Oct;40(10):3798–3803. [PubMed] [Google Scholar]
  36. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  37. Langkilde N. C., Hastrup J., Olsen S., Wolf H., Orntoft T. F. Immunohistochemistry and cytochemistry of experimental rat bladder cancer: binding of the lectins PNA and WGA and of a Le(Y) mouse monoclonal antibody. J Urol. 1989 Apr;141(4):981–986. doi: 10.1016/s0022-5347(17)41082-2. [DOI] [PubMed] [Google Scholar]
  38. Langkilde N. C., Wolf H., Orntoft T. F. Binding of wheat and peanut lectins to human transitional cell carcinomas. Correlation with histopathologic grade, invasion, and DNA ploidy. Cancer. 1989 Aug 15;64(4):849–853. doi: 10.1002/1097-0142(19890815)64:4<849::aid-cncr2820640415>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
  39. Langkilde N. C., Wolf H., Orntoft T. F. Lectinohistochemistry of human bladder cancer: loss of lectin binding structures in invasive carcinomas. APMIS. 1989 Apr;97(4):367–373. doi: 10.1111/j.1699-0463.1989.tb00802.x. [DOI] [PubMed] [Google Scholar]
  40. Lustig S., Fishman P., Djaldetti M., Pluznik D. H. Topographic changes of membrane receptors for wheat germ agglutinin during the cell cycle and their relation to cytolysis. Exp Cell Res. 1980 Oct;129(2):321–328. doi: 10.1016/0014-4827(80)90499-1. [DOI] [PubMed] [Google Scholar]
  41. Maison C., Horstmann H., Georgatos S. D. Regulated docking of nuclear membrane vesicles to vimentin filaments during mitosis. J Cell Biol. 1993 Dec;123(6 Pt 1):1491–1505. doi: 10.1083/jcb.123.6.1491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Maylié-Pfenninger M. F., Jamieson J. D. Distribution of cell surface saccharides on pancreatic cells. II. Lectin-labeling patterns on mature guinea pig and rat pancreatic cells. J Cell Biol. 1979 Jan;80(1):77–95. doi: 10.1083/jcb.80.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. McClay D. R., Wessel G. M., Marchase R. B. Intercellular recognition: quantitation of initial binding events. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4975–4979. doi: 10.1073/pnas.78.8.4975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Meikrantz W., Smith D. M., Sladicka M. M., Schlegel R. A. Nuclear localization of an O-glycosylated protein phosphotyrosine phosphatase from human cells. J Cell Sci. 1991 Mar;98(Pt 3):303–307. doi: 10.1242/jcs.98.3.303. [DOI] [PubMed] [Google Scholar]
  45. Michaud N., Goldfarb D. S. Most nuclear proteins are imported by a single pathway. Exp Cell Res. 1993 Sep;208(1):128–136. doi: 10.1006/excr.1993.1230. [DOI] [PubMed] [Google Scholar]
  46. Miller M. W., Hanover J. A. Functional nuclear pores reconstituted with beta 1-4 galactose-modified O-linked N-acetylglucosamine glycoproteins. J Biol Chem. 1994 Mar 25;269(12):9289–9297. [PubMed] [Google Scholar]
  47. Mody R., Joshi S., Chaney W. Use of lectins as diagnostic and therapeutic tools for cancer. J Pharmacol Toxicol Methods. 1995 Feb;33(1):1–10. doi: 10.1016/1056-8719(94)00052-6. [DOI] [PubMed] [Google Scholar]
  48. Monsigny M., Roche A. C., Sene C., Maget-Dana R., Delmotte F. Sugar-lectin interactions: how does wheat-germ agglutinin bind sialoglycoconjugates? Eur J Biochem. 1980 Feb;104(1):147–153. doi: 10.1111/j.1432-1033.1980.tb04410.x. [DOI] [PubMed] [Google Scholar]
  49. Monsigny M., Sene C., Obrenovitch A., Roche A. C., Delmotte F., Boschetti E. Properties of succinylated wheat-germ agglutinin. Eur J Biochem. 1979 Jul;98(1):39–45. doi: 10.1111/j.1432-1033.1979.tb13157.x. [DOI] [PubMed] [Google Scholar]
  50. Moore M. S., Blobel G. The two steps of nuclear import, targeting to the nuclear envelope and translocation through the nuclear pore, require different cytosolic factors. Cell. 1992 Jun 12;69(6):939–950. doi: 10.1016/0092-8674(92)90613-h. [DOI] [PubMed] [Google Scholar]
  51. Muresan V., Constantinescu M. C. Distribution of sialoglycoconjugates on the luminal surface of the endothelial cell in the fenestrated capillaries of the pancreas. J Histochem Cytochem. 1985 May;33(5):474–476. doi: 10.1177/33.5.3989274. [DOI] [PubMed] [Google Scholar]
  52. Ogawara M., Sone S., Ogura T. Human alveolar macrophages: wheat germ agglutinin-dependent tumor cell killing. Jpn J Cancer Res. 1987 Mar;78(3):288–295. [PubMed] [Google Scholar]
  53. Ogawara M., Utsugi T., Yamazaki M., Sone S. Induction of human monocyte-mediated tumor cell killing by a plant lectin, wheat germ agglutinin. Jpn J Cancer Res. 1985 Nov;76(11):1107–1114. [PubMed] [Google Scholar]
  54. Radu A., Blobel G., Wozniak R. W. Nup155 is a novel nuclear pore complex protein that contains neither repetitive sequence motifs nor reacts with WGA. J Cell Biol. 1993 Apr;121(1):1–9. doi: 10.1083/jcb.121.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Ronzio R. A., Kronquist K. E., Lewis D. S., MacDonald R. J., Mohrlok S. H., O'Donnell J. J., Jr Glycoprotein synthesis in the adult rat pancreas. IV. Subcellular distribution of membrane glycoproteins. Biochim Biophys Acta. 1978 Mar 21;508(1):65–84. doi: 10.1016/0005-2736(78)90189-x. [DOI] [PubMed] [Google Scholar]
  56. Schumacher U., Adam E., Flavell D. J., Boehm D., Brooks S. A., Leathem A. J. Glycosylation patterns of the human colon cancer cell line HT-29 detected by Helix pomatia agglutinin and other lectins in culture, in primary tumours and in metastases in SCID mice. Clin Exp Metastasis. 1994 Nov;12(6):398–404. doi: 10.1007/BF01755883. [DOI] [PubMed] [Google Scholar]
  57. Schwarz R. E., Wojciechowicz D. C., Park P. Y., Paty P. B. Phytohemagglutinin-L (PHA-L) lectin surface binding of N-linked beta 1-6 carbohydrate and its relationship to activated mutant ras in human pancreatic cancer cell lines. Cancer Lett. 1996 Oct 22;107(2):285–291. doi: 10.1016/0304-3835(96)04386-8. [DOI] [PubMed] [Google Scholar]
  58. Skutelsky E., Alroy J., Ucci A. A., Carpenter J. L., Moore F. M. Modulation of carbohydrate residues in regenerative nodules and neoplasms of canine and feline pancreas. Am J Pathol. 1987 Jan;126(1):25–32. [PMC free article] [PubMed] [Google Scholar]
  59. Sowa M., Kato Y., Yamamoto S., Satake K., Kamino K., Umeyama K. A comparative study of experimental and human pancreatic carcinoma with special reference to histochemical findings. Jpn J Surg. 1987 Nov;17(6):493–506. doi: 10.1007/BF02470754. [DOI] [PubMed] [Google Scholar]
  60. Stanley P., Sudo T., Carver J. P. Differential involvement of cell surface sialic acid residues in wheat germ agglutinin binding to parental and wheat germ agglutinin-resistant Chinese hamster ovary cells. J Cell Biol. 1980 Apr;85(1):60–69. doi: 10.1083/jcb.85.1.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sterne-Marr R., Blevitt J. M., Gerace L. O-linked glycoproteins of the nuclear pore complex interact with a cytosolic factor required for nuclear protein import. J Cell Biol. 1992 Jan;116(2):271–280. doi: 10.1083/jcb.116.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Takahashi H., Oyaizu T., Fujita Y., Tsubura A. Lectin-binding profiles in MNNG-induced shrew esophageal carcinomas. Anticancer Res. 1994 Jul-Aug;14(4A):1569–1572. [PubMed] [Google Scholar]
  63. Tao T. W., Calderwood S., Hahn G. M. Stable heat-resistant clones selected from wild-type and surface variants of B-16 melanoma. Int J Cancer. 1983 Nov 15;32(5):533–535. doi: 10.1002/ijc.2910320502. [DOI] [PubMed] [Google Scholar]
  64. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Vannier-Santos M. A., Saraiva E. M., de Souza W. Nuclear and cytoplasmic lectin binding sites in promastigotes of Leishmania. J Histochem Cytochem. 1991 Jun;39(6):793–800. doi: 10.1177/39.6.2033238. [DOI] [PubMed] [Google Scholar]
  66. Walker R. A. The binding of peroxidase-labelled lectins to human breast epithelium. II--The reactivity of breast carcinomas to wheat germ agglutinin. J Pathol. 1984 Oct;144(2):101–108. doi: 10.1002/path.1711440205. [DOI] [PubMed] [Google Scholar]
  67. Welch D. R., McClure S. A., Aeed P. A., Bahner M. J., Adams L. D. Tumor progression- and metastasis-associated proteins identified using a model of locally recurrent rat mammary adenocarcinomas. Clin Exp Metastasis. 1990 Nov-Dec;8(6):533–551. doi: 10.1007/BF00135876. [DOI] [PubMed] [Google Scholar]
  68. Willemer S., Köhler H., Naumann R., Kern H. F., Adler G. Glycoconjugate pattern of membranes in the acinar cell of the rat pancreas. Histochemistry. 1990;93(3):319–326. doi: 10.1007/BF00266395. [DOI] [PubMed] [Google Scholar]
  69. Willmott N., Simpson S. Wheat germ agglutinin binding to cells derived from in vivo grown solid tumors. Anticancer Res. 1983 Nov-Dec;3(6):401–406. [PubMed] [Google Scholar]
  70. Wojciechowicz D. C., Park P. Y., Paty P. B. Beta 1-6 branching of N-linked carbohydrate is associated with K-ras mutation in human colon carcinoma cell lines. Biochem Biophys Res Commun. 1995 Jul 26;212(3):758–766. doi: 10.1006/bbrc.1995.2034. [DOI] [PubMed] [Google Scholar]
  71. Wright C. S. Crystal structure of a wheat germ agglutinin/glycophorin-sialoglycopeptide receptor complex. Structural basis for cooperative lectin-cell binding. J Biol Chem. 1992 Jul 15;267(20):14345–14352. [PubMed] [Google Scholar]
  72. Yagel S., Feinmesser R., Waghorne C., Lala P. K., Breitman M. L., Dennis J. W. Evidence that beta 1-6 branched Asn-linked oligosaccharides on metastatic tumor cells facilitate invasion of basement membranes. Int J Cancer. 1989 Oct 15;44(4):685–690. doi: 10.1002/ijc.2910440422. [DOI] [PubMed] [Google Scholar]
  73. Yoneda Y., Imamoto-Sonobe N., Yamaizumi M., Uchida T. Reversible inhibition of protein import into the nucleus by wheat germ agglutinin injected into cultured cells. Exp Cell Res. 1987 Dec;173(2):586–595. doi: 10.1016/0014-4827(87)90297-7. [DOI] [PubMed] [Google Scholar]

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