Glycoconjugate Journal

, Volume 20, Issue 4, pp 227–238 | Cite as

Tumor galectinology: Insights into the complex network of a family of endogenous lectins

  • Harald Lahm
  • Sabine André
  • Andreas Hoeflich
  • Herbert Kaltner
  • Hans-Christian Siebert
  • Bernard Sordat
  • Claus-Wilhelm von der Lieth
  • Eckhard Wolf
  • Hans-Joachim Gabius
Article

Abstract

β-Galactosides of cell surface glycoconjugates are docking sites for endogenous lectins of the galectin family. In cancer cells, primarily galectins-1 and -3 have been studied to date. With the emergence of insights into their role in growth control, resistance to or induction of apoptosis and invasive behavior the notion is supported that they can be considered as functional tumor markers. In principle, the same might hold true for the other members of the galectin family. But their expression in tumors has hitherto been a subject of attention only to a very limited extent. Pursuing our concept to define the complexity of the galectin network in cancer cells and the degree of functional overlap/divergence with diagnostic/therapeutic implications, we have introduced comprehensive RT-PCR monitoring to map their galectin gene expression. The data on so far less appreciated galectins in this context such as galectins-4 and -8 vindicate this approach. They, too, attach value to extend the immunohistochemical panel accordingly. Our initial histopathological and cell biological studies, for example on colon cancer progression, prove the merit of this procedure. Aside from the detection of gene expression profiles by RT-PCR, the detailed molecular biological monitoring yielded further important information. We describe different levels of regulation of galectin production in colon cancer cells in the cases of the tandem-repeat-type galectins-8 and -9. Isoforms for them are present with insertions into the peptide linker sequence attributed to alternative splicing. Furthermore, variants with distinct amino acid substitutions (galectin-8, Po66-CBP, PCTA-1, CocaI/II and galectin-9/ecalectin) and generation of multiple mRNA species, notably those coding for truncated galectin-8 and -9 versions with only one lectin site, justify to portray these two family members not as distinct individuals but as groups. In aggregate, the ongoing work to thoroughly chart the galectin network and to disentangle the individual functional contributions is expected to make its mark on our understanding of the malignant phenotype in certain tumor types. Published in 2004.

apoptosis galectin invasion metastasis tumor diagnosis tumor marker 

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References

  1. 1.
    Hakomori S-i, Murakami WT, Glycolipids of hamster fibroblasts and derived malignant-transformed cell lines, Proc Natl Acad Sci USA 59, 254-61 (1968).PubMedCrossRefGoogle Scholar
  2. 2.
    Yogeeswaran G, Cell surface glycolipids and glycoproteins in malignant transformation, Adv Cancer Res 38, 289-350 (1983).PubMedCrossRefGoogle Scholar
  3. 3.
    Smets LA, van Beek WP, Carbohydrates of the tumor cell surface, Biochim Biophys Acta 738, 237-49 (1984).PubMedGoogle Scholar
  4. 4.
    Alhadeff JA, Malignant cell glycoproteins and glycolipids, Crit Rev Oncol Hematol 9, 37-107 (1989).PubMedGoogle Scholar
  5. 5.
    Hakomori S-i, Aberrant glycosylation in tumors and tumorassociated carbohydrate antigens, Adv Cancer Res 52, 257-331 (1989).PubMedGoogle Scholar
  6. 6.
    Dabelsteen E, Cell surface carbohydrates as prognostic markers in human carcinomas, J Pathol 179, 358-69 (1996).PubMedCrossRefGoogle Scholar
  7. 7.
    Gabius H-J, Concepts of tumor lectinology, Cancer Investig 15, 454-64 (1997).Google Scholar
  8. 8.
    Kim YJ, Varki A, Perspectives on the significance of altered glycosylation of glycoproteins in cancer, Glycoconjugate J 14, 569-76 (1997).CrossRefGoogle Scholar
  9. 9.
    Brockhausen I, Schutzbach J, Kuhns W, Glycoproteins and their relationship to human disease, Acta Anat 161, 36-78 (1998).PubMedCrossRefGoogle Scholar
  10. 10.
    Hakomori S-i, Cancer-associated glycosphingolipid antigens: Their structure, organization and function, Acta Anat 161, 79-90 (1998).PubMedCrossRefGoogle Scholar
  11. 11.
    Kobata A, A retrospective and prospective view of glycopathology, Glycoconjugate J 15, 323-31 (1998).CrossRefGoogle Scholar
  12. 12.
    Dennis JW, Granovsky M, Warren CE, Glycoprotein glycosylation and cancer progression, Biochim Biophys Acta 1473, 21-34 (1999).PubMedGoogle Scholar
  13. 13.
    Reuter G, Gabius H-J, Eukaryotic glycosylation—whim of nature or multipurpose tool? Cell Mol Life Sci 55, 368-422 (1999).PubMedCrossRefGoogle Scholar
  14. 14.
    Scanlin TF, Glick MC, Terminal glycosylation and disease: Influence on cancer and cystic fibrosis, Glycoconjugate J 17, 617-26 (2000).CrossRefGoogle Scholar
  15. 15.
    Coon JS, Weinstein RS, Blood group-related antigens as markers of malignant potential and heterogeneity in human carcinomas, Hum Pathol 17, 1089-106 (1986).PubMedGoogle Scholar
  16. 16.
    Caselitz J, Lectins and blood group substances as “tumor markers”, Curr Top Pathol 77, 245-77 (1987).PubMedGoogle Scholar
  17. 17.
    Damjanov I, Lectin cytochemistry and histochemistry, Lab Invest 57, 5-20 (1987).PubMedGoogle Scholar
  18. 18.
    Walker RA, The use of lectins in histopathology, Pathol Res Pract 185, 826-35 (1989).PubMedGoogle Scholar
  19. 19.
    Rüdiger H, Gabius H-J, Plant lectins, Glycoconjugate J 18, 589- 613 (2001).CrossRefGoogle Scholar
  20. 20.
    Gabius H-J, André S, Kaltner H, Siebert H-C, The sugar code: Functional lectinomics, Biochim Biophys Acta 1572, 165-77 (2002).PubMedGoogle Scholar
  21. 21.
    Laine RA, The information-storing potential of the sugar code. In Glycosciences: Status and Perspectives, edited by Gabius H-J, Gabius S (Chapman & Hall, London, Weinheim, 1997), pp. 1-14.Google Scholar
  22. 22.
    Kaltner H, Stierstorfer B, Animal lectins as cell adhesion molecules, Acta Anat 161, 162-79 (1998).PubMedCrossRefGoogle Scholar
  23. 23.
    Gabius H-J, Biological information transfer beyond the genetic code: The sugar code, Naturwissenschaften 87, 108-21 (2000).PubMedCrossRefGoogle Scholar
  24. 24.
    Hirabayashi J, Kasai K-i, Glycomics, coming of age! Trends Glycosci Glycotechnol 12, 1-5 (2000).Google Scholar
  25. 25.
    Rüdiger H, Siebert H-C, Solís D, Jiménez-Barbero J, Romero A, von der Lieth C-W, Díaz-Mauriño T, Gabius H-J, Medicinal chemistry based on the sugar code: Fundamentals of lectinology and experimental strategies with lectins as targets, Curr Med Chem 7, 389-416 (2000).PubMedGoogle Scholar
  26. 26.
    Gabius H-J, Engelhardt R, Cramer F, Endogenous tumor lectins: A new class of tumor markers and targets for therapy? Med Hypotheses 18, 47-50 (1985).PubMedCrossRefGoogle Scholar
  27. 27.
    Siebert H-C, André S, Asensio JL, Cañada FJ, Dong X, Espinosa J-F, Frank M, Gilleron M, Kaltner H, Kozár T, Bovin NV, von der Lieth C-W, Vliegenthart JFG, Jiménez-Barbero J, Gabius H-J, A new combined computational and NMR-spectroscopical strategy for the identification of additional conformational constraints of the bound ligand in an aprotic solvent, ChemBioChem 1, 181-95 (2000).PubMedCrossRefGoogle Scholar
  28. 28.
    Loris R, Principles of structures of animal and plant lectins, Biochim Biophys Acta 1572, 198-208 (2002).PubMedGoogle Scholar
  29. 29.
    Gabius H-J, Gabius S, Zemlyanukhina TV, Bovin NV, Brinck U, Danguy A, Joshi SS, Kayser K, Schottelius J, Sinowatz F, Tietze LF, Vidal-Vanaclocha F, Zanetta J-P, Reverse lectin histochemistry: Design and application of glycoligands for detection of cell and tissue lectins, Histol Histopathol 8, 369-83 (1993).PubMedGoogle Scholar
  30. 30.
    Danguy A, Decaestecker C, Genten F, Salmon I, Kiss R, Application of lectins and neoglycoconjugates in histology and pathology, Acta Anat 161, 206-18 (1998).PubMedCrossRefGoogle Scholar
  31. 31.
    Gabius H-J, Glycohistochemistry: The why and how of detection and localization of endogenous lectins, Anat Histol Embryol 30, 3-31 (2001).PubMedCrossRefGoogle Scholar
  32. 32.
    Lee JS, Ro JY, Sahin AA, Hong WK, Brown BW, Mountain CF, Hittelman WN, Expression of blood-group antigen A—a favorable prognostic factor in non-small-cell lung cancer, N Engl J Med 324, 1084-90 (1991).PubMedCrossRefGoogle Scholar
  33. 33.
    Kayser K, Bovin NV, Korchagina EY, Zeilinger C, Zeng F-Y, Gabius H-J, Correlation of expression of binding sites for synthetic blood group A-, B-, and H-trisaccharides and for sarcolectin with survival of patients with bronchial carcinoma, Eur J Cancer 30A, 653-7 (1994).PubMedCrossRefGoogle Scholar
  34. 34.
    Graziano SL, Tatum AH, Gonchoroff NJ, Newman NB, Kohman LJ, Blood group antigen A and flow cytometric analysis in resected early-stage non-small cell lung cancer, Clin Cancer Res 3, 87-93 (1997).PubMedGoogle Scholar
  35. 35.
    Gabius H-J, Wosgien B, Brinck U, Schauer A, Localization of endogenous ?-galactoside-specific lectins by neoglycoproteins, lectin-binding tissue glycoproteins and antibodies and of accessible lectin-specific ligands by a mammalian lectin in human breast cancer, Pathol Res Pract 187, 839-47 (1991).PubMedGoogle Scholar
  36. 36.
    Gabius H-J, Kohnke-Godt B, Leichsenring M, Bardosi A, Heparin-binding lectin of human placenta as a tool for histochemical ligand localization and ligand isolation, J Histochem Cytochem 39, 1249-56 (1991).PubMedGoogle Scholar
  37. 37.
    Amado M, Almeida R, Schwientek T, Clausen H, Identification and characterization of large galactosyltransferase gene families: Galactosyltransferases for all functions, Biochim Biophys Acta 1473, 35-53 (1999).PubMedGoogle Scholar
  38. 38.
    Furukawa K, Sato T, β1,4-Galactosylation of N-glycans is a complex process, Biochim Biophys Acta 1473, 54-66 (1999).PubMedGoogle Scholar
  39. 39.
    Gastinel LN, Galactosyltransferases: A structural overview of their function and reaction mechanisms, Trends Glycosci Glycotechnol 13, 131-45 (2001).Google Scholar
  40. 40.
    Teichberg VI, Silman I, Beitsch DD, Resheff G, A β-galactoside binding protein from electric organ tissue of Electrophorus electricus, Proc Natl Acad Sci USA 72, 1383-7 (1975).CrossRefGoogle Scholar
  41. 41.
    Gabius H-J, Engelhardt R, Cramer F, Bätge R, Nagel GA, Pattern of endogenous lectins in a human epithelial tumor, Cancer Res 45, 253-7 (1985).PubMedGoogle Scholar
  42. 42.
    Cooper DNW, Galectinomics: Finding themes in complexity, Biochim Biophys Acta 1572, 209-31 (2002).PubMedGoogle Scholar
  43. 43.
    Kopitz J, von Reitzenstein C, Burchert M, Cantz M, Gabius H-J, Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture, J Biol Chem 273, 11205-11 (1998).PubMedCrossRefGoogle Scholar
  44. 44.
    Gabius H-J, Probing the cons and pros of lectin-induced immunomodulation: Case studies for the mistletoe lectin and galectin-1, Biochimie 83, 659-66 (2001).PubMedCrossRefGoogle Scholar
  45. 45.
    Kopitz J, von Reitzenstein C, André S, Kaltner H, Uhl J, Ehemann V, Cantz M, Gabius H-J, Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3, J Biol Chem 276, 35917-23 (2001).PubMedCrossRefGoogle Scholar
  46. 46.
    Liu F-T, Patterson RJ, Wang JL, Intracellular functions of galectins, Biochim Biophys Acta 1572, 263-73 (2002).PubMedGoogle Scholar
  47. 47.
    Rabinovich GA, Rubinstein N, Toscano M, Role of galectins in inflammatory and immunomodulatory processes, Biochim Biophys Acta 1572, 274-84 (2002).PubMedGoogle Scholar
  48. 48.
    Gabius H-J, Brehler R, Schauer A, Cramer F, Localization of endogenous lectins in normal human breast, benign breast lesions and mammary carcinomas, Virch Arch [Cell Pathol] 52, 107-15 (1986).CrossRefGoogle Scholar
  49. 49.
    Itzkowitz SH, Galectins: Multipurpose carbohydrate-binding proteins implicated in tumor biology, Gastroenterology 113, 2003-5 (1997).PubMedGoogle Scholar
  50. 50.
    Ohannesian DW, Lotan R, Galectins in tumor cells. In Glycosciences: Status and Perspectives, edited by Gabius H-J, Gabius S (Chapman & Hall, London-Weinheim, 1997), pp. 459-69.Google Scholar
  51. 51.
    André S, Kojima S, Yamazaki N, Fink C, Kaltner H, Kayser K, Gabius H-J, Galectins-1 and-3 and their ligands in tumor biology, J Cancer Res Clin Oncol 125, 461-74 (1999).PubMedCrossRefGoogle Scholar
  52. 52.
    Danguy A, Camby I, Kiss R, Galectins and cancer, Biochim Biophys Acta 1572, 285-93 (2002).PubMedGoogle Scholar
  53. 53.
    Lahm H, André S, Hoeflich A, Fischer JR, Sordat B, Kaltner H, Wolf E, Gabius H-J, Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures, J Cancer Res Clin Oncol 127, 375-86 (2001).PubMedCrossRefGoogle Scholar
  54. 54.
    Lahm H, André S, Hoeflich A, Fischer JR, Sordat B, Kaltner H, Wolf E, Gabius H-J, Molecular biological fingerprinting of human lectin expression byRT-PCR, Methods Enzymol 362, 287-97 (2003).PubMedGoogle Scholar
  55. 55.
    Polyak K, Xia Y, Zweier JL, Kinzler KM, Vogelstein B, A model for p53-induced apoptosis, Nature 389, 300-5 (1997).PubMedCrossRefGoogle Scholar
  56. 56.
    Hippo Y, Yashiro M, Ishii M, Taniguchi H, Tsutsumi S, Hirakawa K, Kodama T, Aburatani H, Differential gene expression pro-files of scirrhous gastric cancer cells with high metastatic potential to peritoneum or lymph nodes, Cancer Res 61, 889-95 (2001).PubMedGoogle Scholar
  57. 57.
    Nagy N, Bronckart Y, Camby I, Legendre H, Lahm H, Kaltner H, Hadari Y, Van Ham P, Yeaton P, Pector J-C, Zick Y, Salmon I, Danguy A, Kiss R, Gabius H-J, Galectin-8 expression decreases in cancer compared with normal and dysplastic human colon tissue and acts significantly on human colon cancer cell migration as a suppressor, Gut 50, 392-401 (2002).PubMedCrossRefGoogle Scholar
  58. 58.
    Nagy N, Legendre H, Engels O, André S, Kaltner H, Wasano K, Zick Y, Pector J-C, Decaestecker C, Gabius H-J, Salmon I, Kiss R, Refined prognostic evaluation in colon carcinoma using immunohistochemical galectin fingerprinting, Cancer 97, 1849-58 (2003).PubMedCrossRefGoogle Scholar
  59. 59.
    Kayser K, Zink S, Schneider T, Dienemann H, André S, Kaltner H, Schüring M-P, Zick Y, Gabius H-J, Benign metastasizing leiomyoma of the uterus: Documentation of clinical, immunohistochemical and lectin-histochemical data for ten cases, Virchows Arch 437, 284-92 (2000).PubMedCrossRefGoogle Scholar
  60. 60.
    Camby I, Belot N, Rorive S, Lefranc F, Maurage C-A, Lahm H, Kaltner H, Hadari YR, Ruchoux M-M, Brotchi J, Zick Y, Salmon I, Gabius H-J, Kiss R, Galectins are differentially expressed in supratentorial pilocytic astrocytomas, astrocytomas, anaplastic astrocytomas and glioblastomas, and significantly modulate tumor astrocyte migration, Brain Pathol 11, 12-26 (2001).PubMedCrossRefGoogle Scholar
  61. 61.
    Danguy A, Rorive S, Decaestecker C, Bronckart Y, Kaltner H, Hadari YR, Goren R, Zick Y, Pétein M, Salmon I, Gabius H-J, Kiss R, Immunohistochemical profile of galectin-8 expression in benign and malignant tumors of epithelial, mesenchymatous and adipous origins, and of the nervous system, Histol Histopathol 16, 861-8 (2001).PubMedGoogle Scholar
  62. 62.
    Sheikholeslam-Zadeh R, Decaestecker C, Delbrouck C, Danguy A, Salmon I, Zick Y, Kaltner H, Hassid S, Gabius H-J, Kiss R, Choufani G, The levels of expression of galectin-3, but not of Galectins-1 and-8, correlate with apoptosis in human cholesteatomas, Laryngoscope 111, 1042-7 (2001).PubMedCrossRefGoogle Scholar
  63. 63.
    Wollina U, Graefe T, Feldrappe S, André S, Wasano K, Kaltner H, Zick Y, Gabius H-J, Galectin fingerprinting by immuno-and lectin histochemistry in cutaneous lymphoma, J Cancer Res Clin Oncol 128, 103-10 (2002).PubMedCrossRefGoogle Scholar
  64. 64.
    Gabius H-J, Animal lectins, Eur J Biochem 243, 543–76 (1997).PubMedCrossRefGoogle Scholar
  65. 65.
    Dahms NM, Hancock MK, P-type lectins, Biochim Biophys Acta 1572, 317-40.Google Scholar
  66. 66.
    Kilpatrick DC, Animal Lectins: An historical introduction and overview, Biochim Biophys Acta 1572, 187-97 (2002).PubMedGoogle Scholar
  67. 67.
    Wada J, Kanwar YS, Identification and characterization of galectin-9, a novel ?-galactoside-binding mammalian lectin, J Biol Chem 272, 6078-86 (1997).PubMedCrossRefGoogle Scholar
  68. 68.
    Suk K, Hwang D-Y, Lee M-S, Natural autoantibody to galectin-9 in normal human serum, J Clin Immunol 19, 158-65 (1999).PubMedCrossRefGoogle Scholar
  69. 69.
    Lahm H, Hoeflich A, André S, Sordat B, Kaltner H, Wolf E, Gabius H-J, Gene expression of galectin-9/ecalectin, a potent eosinophil chemoattractant, and/or the insertional isoform in human colorectal carcinoma cell lines and detection of frame-shift mutations for protein sequence truncations in the second functional lectin domain, Int J Oncol 17, 519-24 (2000).PubMedGoogle Scholar
  70. 70.
    Türeci Ö, Schmitt H, Fadle N, Pfreundschuh M, Sahin U, Molecular definition of a novel galectin which is immunogenic in patients with Hodgkin's disease, J Biol Chem 272, 6416-22 (1997).PubMedCrossRefGoogle Scholar
  71. 71.
    Matsumoto R, Matsumoto H, Seki M, Hata M, Asano Y, Kanegasaki S, Stevens RL, Hirashima M, Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T-lymphocytes, J Biol Chem 273, 16976-84 (1998).PubMedCrossRefGoogle Scholar
  72. 72.
    Matsushita N, Nishi N, Seki M, Matsumoto R, Kuwabara I, Liu F-T, Hata Y, Nakamura T, Hirashima M, Requirement of divalent galactoside-binding activity of ecalectin/galectin-9 for eosinophil chemoattraction, J Biol Chem 275, 8355-60 (2000).PubMedCrossRefGoogle Scholar
  73. 73.
    Brewer CF, Binding and cross-linking properties of galectins, Biochim Biophys Acta 1572, 255-62 (2002).Google Scholar
  74. 74.
    Dazord L, Bourel D, Martin A, Lecorre R, Bourguet P, Bohy J, Saccavini JC, Delaval P, Louvet M, Toujas L, A monoclonal antibody (Po66) directed against human lung squamous cell carcinoma immunolocalization of tumour xenografts in nude mice, Cancer Immunol Immunother 24, 263-8 (1987).PubMedCrossRefGoogle Scholar
  75. 75.
    Brichory F, Collet B, Pineau C, Desrues B, Toujas L, Pennec JP, Dazord L, Purification of a tumoral marker recognized by monoclonal antibody Po66 and associated with human lung squamous cell carcinoma, Int J Biol Markers 11, 148-52 (1996).PubMedGoogle Scholar
  76. 76.
    Su ZZ, Lin J, Shen R, Fischer PE, Goldstein NI, Fischer PB, Surface-epitope masking and expression cloning identifies the human prostate carcinoma tumor antigen gene PCTA-1 a member of the galectin gene family, Proc Natl Acad Sci USA 93, 7252-7 (1996).PubMedCrossRefGoogle Scholar
  77. 77.
    Hadari Y, Eisenstein M, Zakut R, Zick Y, Galectin-8: On the road from structure to function, Trends Glycosci Glycotechnol 9, 103-12 (1995).Google Scholar
  78. 78.
    Bassen R, Brichory F, Caulet-Maugendre S, Bidon N, Delaval P, Desrues B, Dazord L, Expression of Po66-CBP, a type-8 galectin, in different healthy, tumoral and peritumoral tissues, Anticancer Res 19, 5429-33 (1999).PubMedGoogle Scholar
  79. 79.
    Bidon N, Brichory F, Hanash S, Bourguet P, Dazord L, Le Pennec JP, Two messenger RNAs and five isoforms for Po66-CBP, a galectin-8 homolog in a human lung carcinoma cell line, Gene 274, 253-62 (2001).PubMedCrossRefGoogle Scholar
  80. 80.
    Gopalkrishnan RV, Roberts T, Tuli S, Kang D, Christiansen KA, Fisher PB, Molecular characterization of prostate carcinoma tumor antigen-1, PCTA-1, a human galectin-8 related gene, Oncogene 19, 4405-16 (2000).PubMedCrossRefGoogle Scholar
  81. 81.
    Hadari YR, Arbel-Goren R, Levy Y, Amsterdam A, Alon R, Zakut R, Zick Y, Galectin-8 binding to integrins inhibits cell adhesion and induces apoptosis, J Cell Sci 113, 2385-97 (2000).PubMedGoogle Scholar
  82. 82.
    Bidon N, Brichory F, Bourguet P, Le Pennec JP, Dazord L, Galectin-8: A complex sub-family of galectins (Review), Int J Mol Med 8, 245-50 (2001).PubMedGoogle Scholar
  83. 83.
    Cajot JF, Sordat I, Silvestre T, Sordat B, Differential display cloning identifies motility-related protein (MRP1/CD9) as highly expressed in primary compared to metastatic human colon carcinoma cells, Cancer Res 57, 2953-7 (1997).Google Scholar
  84. 84.
    Siebert H-C, Adar R, Arango R, Burchert M, Kaltner H, Kayser G, Tajkhorshid E, von der Lieth C-W, Kaptein R, Sharon N, Vliegenthart JFG, Gabius H-J, Involvement of laser photo CIDNP (chemically induced dynamic nuclear polarization)-reactive amino acid side chains in ligand binding by galactosidespecific lectins in solution. Similarities in the role of tryptophan/ tyrosine residues for ligand binding between a plant agglutinin and mammalian/avian galectins and the detection of an influence of single-site mutagenesis on surface presentation of spatially separated residues, Eur J Biochem 249, 27-38 (1997).PubMedCrossRefGoogle Scholar
  85. 85.
    von der Lieth C-W, Siebert H-C, Kozár T, Burchert M, Frank M, Gilleron M, Kaltner H, Kayser G, Tajkhorshid E, Bovin NV, Vliegenthart JFG, Gabius H-J, Lectin ligands: New insights into their conformations and their dynamic behavior and the discovery of conformer selection by lectins, Acta Anat 161, 91-109 (1998).PubMedCrossRefGoogle Scholar
  86. 86.
    Caulet-Maugendre S, Birolleau S, Corbineau H, Bassen R, Desrues B, Bidon N, Delaval P, Ramee MP, Brichory F, Dazord Galectins in cancer cells 237 L, Immunohistochemical expression of the intracellular component of galectin-8 in squamous cell metaplasia of the bronchial epithelium in neoplastic and benign processes, Pathol Res Pract 197, 797-801 (2001).PubMedCrossRefGoogle Scholar
  87. 87.
    Henno S, Brichory F, Langanay T, Desrues B, Bidon N, Delaval P, Ramee MP, Dazord L, Caulet-Maugendre S, Expression of Po66-CBP, a galectin-8, in different types of primary and secondary broncho-pulmonary tumors, Oncol Rep 9, 177-80 (2002).PubMedGoogle Scholar
  88. 88.
    Paz A, Haklai R, Elad-Sfadia G, Ballan E, Kloog Y, Galectin-1 binds oncogenic H-Ras to mediate Ras membrane anchorage and cell transformation, Oncogene 20, 7486-93 (2001).PubMedCrossRefGoogle Scholar
  89. 89.
    Elad-Sfadia G, Haklai R, Ballan E, Gabius H-J, Kloog Y, Galectin-1 augments Ras activation and diverts Ras signals to Raf-1 at the expense of phosphoinositide 3-kinase, J Biol Chem 277, 37169-75 (2002).PubMedCrossRefGoogle Scholar
  90. 90.
    Levy Y, Arbel-Goren R, Hadari YR, Eshhar S, Ronen D, Elhanany E, Geiger B, Zick Y, Galectin-8 functions as a matricellular modulator of cell adhesion, J Biol Chem 276, 31285-95 (2001).PubMedCrossRefGoogle Scholar
  91. 91.
    Gorski JP, Liu F-T, Artigues A, Castagna LF, Osdoby P, New alternatively spliced form of galectin-3, a member of the ?-galactoside-binding animal lectin family, contains a predicted transmembrane-spanning domain and a leucine zipper motif, J Biol Chem 277, 18840-8 (2002).PubMedCrossRefGoogle Scholar
  92. 92.
    Ariizumi K, Shen GL, Shikano S, Ritter R, 3rd, Zukas P, Edelbaum D, Morita A, Takashima A, Cloning of a second dendritic cell-associated C-type lectin (dectin-2) and its alternatively spliced isoforms, J Biol Chem 275, 11957-63 (2000).PubMedCrossRefGoogle Scholar
  93. 93.
    Hernanz-Falcon P, Arce I, Roda-Navarro P, Fernandez-Ruiz E, Cloning of human DECTIN-1, a novel C-type lectin-like receptor gene expressed on dendritic cells, Immunogenetics 53, 288-95 (2001) Erratum in: Immunogenetics 53(6) 518 (2001).CrossRefGoogle Scholar
  94. 94.
    Mummidi S, Catano G, Lam L, Hoefle A, Telles V, Begum K, Jimenez F, Ahuja SS, Ahuja SK, Extensive repertoire of membrane-bound and soluble dendritic cell-specific ICAM-3-grabbing nonintegrin 1 (DC-SIGN1) and DC-SIGN2 isoforms, J Biol Chem 276, 33196-212 (2001).PubMedCrossRefGoogle Scholar
  95. 95.
    Yokota K, Takashima A, Bergstresser PR, Ariizumi K, Identification of a human homologue of the dendritic cell-associated C-type lectin-1, dectin-1, Gene 272, 51-60 (2001).PubMedCrossRefGoogle Scholar
  96. 96.
    Gunnersen JM, Spirkoska V, Smith PE, Danks RA, Tan SS, Growth and migration markers of rat C6 glioma cells identified by serial analysis of gene expression, Glia 32, 146-54 (2000).PubMedCrossRefGoogle Scholar
  97. 97.
    Yamaoka K, Mishima K, Nagashima Y, Asai A, Sanai Y, Kirino T, Expression of galectin-1 mRNA correlates with the malignant potential of human gliomas and expression of antisense galectin-1 inhibits the growth of 9 glioma cells, J Neurosci Res 59, 722-30 (2000).PubMedCrossRefGoogle Scholar
  98. 98.
    Rorive S, Belot N, Decaestecker C, Lefranc F, Gordower L, Micik S, Maurage C-A, Kaltner H, Ruchoux M-M, Danguy A, Gabius H-J, Salmon I, Kiss R, Camby I, Galectin-1 is highly expressed in human gliomas with relevance for modulation of invasion of tumor astrocytes into the brain parenchyma, GLIA 33, 241-55 (2001).PubMedCrossRefGoogle Scholar
  99. 99.
    Camby I, Belot N, Lefranc F, Sadeghi N, de Launoit Y, Kaltner H, Musette S, Darro F, Danguy A, Salmon I, Gabius H-J, Kiss R, Galectin-1 modulates human glioblastoma cell migration into the brain through modifications to the actin cytoskeleton and levels of expression of small GTPases, J Neuropathol Exp Neurol 61, 585-96 (2002).PubMedGoogle Scholar
  100. 100.
    Rappl G, Abken H, Muche JM, Sterry W, Tilgen W, André S, Kaltner H, Ugurel S, Gabius H-J, Reinhold U, CD4+CD7-leukemic T cells from patients with Sézary syndrome are protected from galectin-1-triggeredTcell death, Leukemia 16, 840-5 (2002).PubMedCrossRefGoogle Scholar
  101. 101.
    André S, Cejas Ortega PJ, Alamino Perez M, Roy R, Gabius H-J, Lactose-containing starburst dendrimers: Influence of dendrimer generation and binding-site orientation of receptors (plant/animal lectins and immunoglobulins) on binding properties, Glycobiology 9, 1253-61 (1999).PubMedCrossRefGoogle Scholar
  102. 102.
    André S, Frisch B, Kaltner H, Desouza DL, Schuber F, Gabius H-J, Lectin-mediated drug targeting. Selection of valency, sugar type (Gal/Lac) and spacer length for cluster glycosides as parameters to distinguish ligand binding to C-type asialoglycoprotein receptors and galectins, Pharmaceut Res 17, 985-90 (2000).CrossRefGoogle Scholar
  103. 103.
    Yamazaki N, Kojima S, Bovin NV, André S, Gabius S, Gabius H-J, Endogenous lectins as targets for drug delivery, Adv Drug Deliv Rev 43, 225-44 (2000).PubMedCrossRefGoogle Scholar
  104. 104.
    André S, Pieters RJ, Vrasidas I, Kaltner H, Kuwabara I, Liu F-T, Liskamp RMJ, Gabius H-J, Wedgelike glycodendrimers as inhibitors of binding of mammalian galectins to various glycoproteins, lactose maxiclusters and cell surface glycoconjugates, ChemBioChem 2, 822-30 (2001).PubMedCrossRefGoogle Scholar
  105. 105.
    Nangia-Makker P, Conklin J, Hogan V, Raz A, Carbohydratebinding proteins in cancer, and their ligands as therapeutic agents, Trends Mol Med 8, 187-92 (2002).PubMedCrossRefGoogle Scholar
  106. 106.
    Sörme P, Qian Y, Nyholm PG, Leffler H, Nilsson UJ, Low micromolar inhibitors of galectin-3 based on 3'-derivatization of N-acetyllactosamine, ChemBioChem 3, 183-9 (2002).PubMedCrossRefGoogle Scholar
  107. 107.
    Vrasidas I, André S, Valentini P, Böck C, Lensch M, Kaltner H, Liskamp RMJ, Gabius H-J, Pieters RJ, Rigidified multivalent lactose molecules and their interactions with mammalian galectins: A route to selective inhibitors, Org Biomol Chem 1, 803-10 (2003).PubMedCrossRefGoogle Scholar
  108. 108.
    Yilmaz A, Gaide A-C, Sordat B, Borbenyi Z, Lahm H, Imam A, Schreyer M, Odartchenko N, Malignant progression of SV40-immortalised human milk epithelial cells, Br J Cancer 68, 868-73 (1993).PubMedGoogle Scholar
  109. 109.
    Carrel S, Sordat B, Merenda C, Establishment of a cell line (Co-115) from a human colon carcinoma transplanted into nude mice, Cancer Res 36, 3978-84 (1976).PubMedGoogle Scholar
  110. 110.
    Cajot JF, Sordat I, Silvestre T, Sordat B, Differential display cloning identifies motility-related protein (MRP1/CD9) as highly expressed in primary compared to metastatic human colon carcinoma cells, Cancer Res 57, 2593-7 (1997).PubMedGoogle Scholar
  111. 111.
    Bepler G, Rotsch M, Jacques G, Haeder M, Heymanns J, Hartogh G, Kiefer P, Havemann K, Peptides and growth factors in small cell lung cancer: Production, binding sites and growth effects, J Cancer Res Clin Oncol 114, 235-44 (1988).PubMedCrossRefGoogle Scholar
  112. 112.
    Bepler G, Bading H, Heimann B, Kiefer P, Havemann K, Moelling K, Expression of p64 c-myc and neuroendocrine properties define three subclasses of small cell lung cancer, Oncogene 4, 45-50 (1989).PubMedGoogle Scholar
  113. 113.
    Wörmann B, Anderson JM, Liberty JA, Gajl-Peczalska K, Brunning RD, Silberman TL, Arthur DC, Lebien TW, Establishment of a leukemic cell model for studying human pre-B to B-cell differentiation, J Immunol 142, 110-7 (1989).PubMedGoogle Scholar
  114. 114.
    Gabius S, Joshi SS, Gabius H-J, Sharp JG, Establishment, characterization and determination of cell surface sugar receptor 238 Lahm et al. (lectin) expression by neoglycoenzymes of a human myeloid marker-expressing B lymphoblastoid cell line, Anticancer Res 11, 793-800 (1991).PubMedGoogle Scholar
  115. 115.
    Stacchini A, Aragno M, Vallario A, Alfarano A, Circosta P, Gottardi D, Faldella A, Rege-Chambrin G, Thunberg U, Nilsson K, Caligaris-Cappio F, MEC1 and MEC2: Two new cell lines from B-chronic lymphocytic leukemia in prolymphocytoid transformation, Leukemia Res 23, 127-36 (1999).CrossRefGoogle Scholar
  116. 116.
    Hasselmann DO, Rappl G, Tilgen W, Reinhold U, Extracellular tyrosinase mRNA within apoptotic bodies is protected from degradation in human serum, Clin Chem 47, 1488-9 (2001).PubMedGoogle Scholar
  117. 117.
    Cattel L, Delprino L, Brusa P, Dosio F, Comoglio PM, Prat M, Comparison of blocked and non-blocked ricin-antibody immunotoxins against human gastric carcinoma and colorectal adenocarcinoma cell lines, Cancer Immunol Immunother 27, 233-40 (1988).PubMedCrossRefGoogle Scholar
  118. 118.
    Bosserhoff AK, Gläßl A, Stolz W, Buettner R, Detection of telomerase activity in skin, melanocytic nevi, and melanoma by telomerase PCR ELISA, Biochemica 3, 16-8 (1997)Google Scholar
  119. 119.
    Bazzoni F, Regalia E, Triggering of antitumor activity through melanoma-specific transduction of a constitutively active tumor necrosis factor (TNF) R1 chimeric receptor in the absence of TNF-α, Cancer Res 61, 1050-7 (2001).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Harald Lahm
    • 1
  • Sabine André
  • Andreas Hoeflich
  • Herbert Kaltner
  • Hans-Christian Siebert
  • Bernard Sordat
  • Claus-Wilhelm von der Lieth
  • Eckhard Wolf
  • Hans-Joachim Gabius
  1. 1.Immunology-Molecular Biology Laboratory (IML)Thoraxklinik Heidelberg gGmbHHeidelberg

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