Evidence of galectin-1 involvement in glioma chemoresistance

Toxicology and Applied Pharmacology

Volumn 229, Issue 2, 2008, Pages 172-183

  Le Mercier, Marie ^a   Lefranc, Florence ^a,b   Mijatovic, Tatjana ^a   Debeir, Olivier ^a   Haibe Kains, Benjamin ^a,c   Bontempi, Gianluca ^a   Decaestecker, Christine ^a   Kiss, Robert ^a   Mathieu, Véronique ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b ERASME HOSPITAL   (Belgium)

^c JULES BORDET INSTITUTE   (Belgium)

Author keywords

Chemoresistance; Galectin 1; Glioma

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CYSTEINE RICH PROTEIN 61; GALECTIN 1; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; OXYGEN REGULATED PROTEIN 150; PROTEIN P53; SMALL INTERFERING RNA; TEMOZOLOMIDE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CELL MIGRATION; CELLULAR STRESS RESPONSE; CHEMOTHERAPY; DRUG RESISTANCE; ENDOPLASMIC RETICULUM; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; GLIOMA; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION;

EID: 43449117183     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.01.009     Document Type: Article

References (80)

1. Ashery U. Yizhar O. Rotblat B. Elad-Sfadia G. Barkan B. Haklai R. Kloog Y. Spatiotemporal organization of Ras signaling: rasosomes and the galectin switch Cell. Mol. Neurobiol. 26 2006 471 495
2. Blum R. Jacob-Hirsch J. Rechavi G. Kloog Y. Suppression of survivin expression in glioblastoma cells by the Ras inhibitor farnesylthiosalicylic acid promotes caspase-dependent apoptosis Mol. Cancer. Ther. 5 2006 2337 2347
3. Bolstad B.M. Irizarry R.A. Astrand M. Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias Bioinformatics 19 2003 185 193
4. Brandes A.A. State-of-the-art treatment of high-grade brain tumors Semin. Oncol. 30 2003 4 9
5. Branle F. Lefranc F. Camby I. Jeuken J. Geurts-Moespot A. Sprenger S. Sweep F. Kiss R. Salmon I. Evaluation of the efficiency of chemotherapy in in vivo orthotopic models of human glioma cells with and without 1p19q deletions and in C6 rat orthotopic allografts serving for the evaluation of surgery combined with chemotherapy Cancer 95 2002 641 655
6. Bresalier R.S. Yan P.S. Byrd J.C. Lotan R. Raz A. Expression of the endogenous galactose-binding protein galectin-3 correlates with the malignant potential of tumors in the central nervous system Cancer 80 1997 776 787
7. Camby I. Belot N. Rorive S. Lefranc F. Maurage C.A. Lahm H. Kaltner H. Hadari Y. 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 2001 12 26
8. 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 2002 585 596
9. Camby I. Decaestecker C. Lefranc F. Kaltner H. Gabius H.J. Kiss R. Galectin-1 knocking down in human U87 glioblastoma cells alters their gene expression pattern Biochem. Biophys. Res. Commun. 335 2005 27 35
10. Camby I. Le Mercier M. Lefranc F. Kiss R. Galectin-1: a small protein with major functions Glycobiology 16 2006 137R 157R
11. Case D. Irwin D. Ivester C. Harral J. Morris K. Imamura M. Roedersheimer M. Patterson A. Carr M. Hagen M. Saavedra M. Crossno J. Jr. Young K.A. Dempsey E.C. Poirier F. West J. Majka S. Mice deficient in galectin-1 exhibit attenuated physiological responses to chronic hypoxia-induced pulmonary hypertension Am. J. Physiol. Lung Cell. Mol. Physiol. 292 2007 L154 L164
12. De Angelis P.M. Svendsrud D.H. Kravik K.L. Stokke T. Cellular response to 5-fluorouracil (5-FU) in 5-FU-resistant colon cancer cell lines during treatment and recovery Mol. Cancer 5 2006 20
13. Eisele L. Klein-Hitpass L. Chatzimanolis N. Opalka B. Boes T. Seeber S. Moritz T. Flasshove M. Differential expression of drug-resistance-related genes between sensitive and resistant blasts in acute myeloid leukemia Acta. Haematol. 117 2007 8 15
14. Elad-Sfadia G. Haklai R. Balan E. Kloog Y. Galectin-3 augments K-Ras activation and triggers a Ras signal that attenuates ERK but not phosphoinositide 3-kinase activity J. Biol. Chem. 279 2004 34922 34930
15. Fels D.R. Koumenis C. The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth Cancer Biol. Ther. 5 2006 723 728
16. Gentleman R.C. Carey V.J. Bates D.M. Bolstad B. Dettling M. Dudoit S. Ellis B. Gautier L. Ge Y. Gentry J. Hornik K. Hothorn T. Huber W. Iacus S. Irizarry R. Leisch F. Li C. Maechler M. Rossini A.J. Sawitzki G. Smith C. Smyth G. Tierney L. Yang J.Y. Zhang J. Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
17. Goldberg L. Kloog Y. A Ras inhibitor tilts the balance between Rac and Rho and blocks phosphatidylinositol 3-kinase-dependent glioblastoma cell migration Cancer Res. 66 2006 11709 11717
18. Griffin R.J. Gaffney P. Mayo K. McNiel E. Ondrey F. Dings R.P.M. Galectin-1 as a Prognostic Marker and Therapeutic Target in Head and Neck Malignancies. 2007 2007 AACR Annual Meeting Los Angeles CA
19. Hayot C. Debeir O. Van Ham P. Van Damme M. Kiss R. Decaestecker C. Characterization of the activities of actin-affecting drugs on tumor cell migration Toxicol. Appl. Pharmacol. 211 2006 30 40
20. Hori O. Ichinoda F. Yamaguchi A. Tamatani T. Taniguchi M. Koyama Y. Katayama T. Tohyama M. Stern D.M. Ozawa K. Kitao Y. Ogawa S. Role of Herp in the endoplasmic reticulum stress response Genes Cells 9 2004 457 469
21. Ingrassia L. Camby I. Lefranc F. Mathieu V. Nshimyumukiza P. Darro F. Kiss R. Anti-galectin compounds as potential anti-cancer drugs Curr. Med. Chem. 13 2006 3513 3527
22. Jin R. De Smaele E. Zazzeroni F. Nguyen D.U. Papa S. Jones J. Cox C. Gelinas C. Franzoso G. Regulation of the gadd45beta promoter by NF-kappaB DNA Cell. Biol. 21 2002 491 503
23. Kanzawa T. Germano I.M. Komata T. Ito H. Kondo Y. Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells Cell Death Differ. 11 2004 448 457
24. Kapoor G.S. O'Rourke D.M. Receptor tyrosine kinase signaling in gliomagenesis: pathobiology and therapeutic approaches Cancer Biol. Ther. 2 2003 330 342
25. Kardosh A. Soriano N. Pyrko P. Liu Y.T. Jabbour M. Hofman F.M. Schonthal A.H. Reduced survivin expression and tumor cell survival during chronic hypoxia and further cytotoxic enhancement by the cyclooxygenase-2 inhibitor celecoxib J. Biomed. Sci. 14 2007 647 662
26. Kim R. Emi M. Tanabe K. Murakami S. Role of the unfolded protein response in cell death Apoptosis 11 2006 5 13
27. Kitao Y. Ozawa K. Miyazaki M. Tamatani M. Kobayashi T. Yanagi H. Okabe M. Ikawa M. Yamashima T. Stern D.M. Hori O. Ogawa S. Expression of the endoplasmic reticulum molecular chaperone (ORP150) rescues hippocampal neurons from glutamate toxicity J. Clin. Invest. 108 2001 1439 1450
28. Kitao Y. Hashimoto K. Matsuyama T. Iso H. Tamatani T. Hori O. Stern D.M. Kano M. Ozawa K. Ogawa S. ORP150/HSP12A regulates Purkinje cell survival: a role for endoplasmic reticulum stress in cerebellar development J. Neurosci. 24 2004 1486 1496
29. Kondo Y. Kanzawa T. Sawaya R. Kondo S. The role of autophagy in cancer development and response to therapy Nat. Rev. Cancer 5 2005 726 734
30. Kroemer G. Jaattela M. Lysosomes and autophagy in cell death control Nat. Rev. Cancer 5 2005 886 897
31. Lawson H.C. Sampath P. Bohan E. Park M.C. Hussain N. Olivi A. Weingart J. Kleinberg L. Brem H. Interstitial chemotherapy for malignant gliomas: the Johns Hopkins experience J. Neurooncol. 83 2007 61 70
32. Le Mercier M. Kondo Y. Mathieu V. Camby I. Decaestecker C. Kiss R. Lefranc F. Decreasing Galectin-1 Expression in Human Experimental Glioblastomas Impairs the Endoplasmic Reticulum Stress (ERS) Response and Increases Temozolomide Anti-tumor Effects. 2007 2007 AACR Annual Meeting Los Angeles CA
33. Le Mercier, M., Mathieu, V., Haibe-Kains, B., Bontempi, G., Mijatovic, T., Decaestecker, C., Kiss, R., Lefranc, F., in press. ORP150, a major target of galectin-1 pro-angiogenic effects in human Hs683 glioblastoma xenografts. J. Neuropathol. Exp. Neurol.
34. Le Q.T. Shi G. Cao H. Nelson D.W. Wang Y. Chen E.Y. Zhao S. Kong C. Richardson D. O'Byrne K.J. Giaccia A.J. Koong A.C. Galectin-1: a link between tumor hypoxia and tumor immune privilege J. Clin. Oncol. 23 2005 8932 8941
35. Lee E. Nichols P. Spicer D. Groshen S. Yu M.C. Lee A.S. GRP78 as a novel predictor of responsiveness to chemotherapy in breast cancer Cancer Res. 66 2006 7849 7853
36. Lefranc F. Mijatovic T. Mathieu V. Rorive S. Decaestecker C. Debeir O. Brotchi J. Van Ham P. Salmon I. Kiss R. Characterization of gastrin-induced proangiogenic effects in vivo in orthotopic U373 experimental human glioblastomas and in vitro in human umbilical vein endothelial cells Clin. Cancer Res. 10 2004 8250 8265
37. Lefranc F. Brotchi J. Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis J. Clin. Oncol. 23 2005 2411 2422
38. Lefranc F. Sadeghi N. Camby I. Metens T. Dewitte O. Kiss R. Present and potential future issues in glioblastoma treatment Expert Rev. Anticancer Ther. 6 2006 719 732
39. +-ATPase) to combat glioblastoma cells. Neurosurgery.
40. L'Esperance S. Popa I. Bachvarova M. Plante M. Patten N. Wu L. Tetu B. Bachvarov D. Gene expression profiling of paired ovarian tumors obtained prior to and following adjuvant chemotherapy: molecular signatures of chemoresistant tumors Int. J. Oncol. 29 2006 5 24
41. Li J. Lee A.S. Stress induction of GRP78/BiP and its role in cancer Curr. Mol. Med. 6 2006 45 54
42. Liu F.T. Rabinovich G.A. Galectins as modulators of tumour progression Nat. Rev. Cancer 5 2005 29 41
43. Liu T. Laurell C. Selivanova G. Lundeberg J. Nilsson P. Wiman K.G. Hypoxia induces p53-dependent transactivation and Fas/CD95-dependent apoptosis Cell Death Differ. 14 2007 411 421
44. Mathieu V. Mijatovic T. van Damme M. Kiss R. Gastrin exerts pleiotropic effects on human melanoma cell biology Neoplasia 7 2005 930 943
45. Mathieu V. Le Mercier M. De Neve N. Sauvage S. Gras T. Roland I. Lefranc F. Kiss R. Galectin-1 knockdown increases sensitivity to temozolomide in a B16F10 mouse metastatic melanoma model J. Invest. Dermatol. 127 2007 2399 2410
46. Megalizzi V. Mathieu V. Mijatovic T. Gailly P. Debeir O. De Neve N. Van Damme M. Bontempi G. Haibe-Kains B. Decaestecker C. Kondo Y. Kiss R. Lefranc F. 4-IBP, a sigma1 receptor agonist, decreases the migration of human cancer cells, including glioblastoma cells, in vitro and sensitizes them in vitro and in vivo to cytotoxic insults of proapoptotic and proautophagic drugs Neoplasia 9 2007 358 369
47. Menendez J.A. Vellon L. Mehmi I. Teng P.K. Griggs D.W. Lupu R. A novel CYR61-triggered 'CYR61-alphavbeta3 integrin loop' regulates breast cancer cell survival and chemosensitivity through activation of ERK1/ERK2 MAPK signaling pathway Oncogene 24 2005 761 779
48. Mijatovic T. Mathieu V. Gaussin J.F. De Neve N. Ribaucour F. Van Quaquebeke E. Dumont P. Darro F. Kiss R. Cardenolide-induced lysosomal membrane permeabilization demonstrates therapeutic benefits in experimental human non-small cell lung cancers Neoplasia 8 2006 402 412
49. Mijatovic T. Op De Beeck A. Van Quaquebeke E. Dewelle J. Darro F. de Launoit Y. Kiss R. The cardenolide UNBS1450 is able to deactivate nuclear factor kappaB-mediated cytoprotective effects in human non-small cell lung cancer cells Mol. Cancer Ther. 5 2006 391 399
50. Mirimanoff R.O. Gorlia T. Mason W. Van den Bent M.J. Kortmann R.D. Fisher B. Reni M. Brandes A.A. Curschmann J. Villa S. Cairncross G. Allgeier A. Lacombe D. Stupp R. Radiotherapy and temozolomide for newly diagnosed glioblastoma: recursive partitioning analysis of the EORTC 26981/22981-NCIC CE3 phase III randomized trial J. Clin. Oncol. 24 2006 2563 2569
51. Muller M. Schleithoff E.S. Stremmel W. Melino G. Krammer P.H. Schilling T. One, two, three—p53, p63, p73 and chemosensitivity Drug Resist. Updat 9 2006 288 306
52. Nakahara S. Oka N. Raz A. On the role of galectin-3 in cancer apoptosis Apoptosis 10 2005 267 275
53. Namba T. Hoshino T. Tanaka K. Tsutsumi S. Ishihara T. Mima S. Suzuki K. Ogawa S. Mizushima T. Up-regulation of 150-kDa oxygen-regulated protein by celecoxib in human gastric carcinoma cells Mol. Pharmacol. 71 2007 860 870
54. Nogalska A. Engel W.K. McFerrin J. Kokame K. Komano H. Askanas V. Homocysteine-induced endoplasmic reticulum protein (Herp) is up-regulated in sporadic inclusion-body myositis and in endoplasmic reticulum stress-induced cultured human muscle fibers J. Neurochem. 96 2006 1491 1499
55. Nylandsted J. Gyrd-Hansen M. Danielewicz A. Fehrenbacher N. Lademann U. Hoyer-Hansen M. Weber E. Multhoff G. Rohde M. Jaattela M. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization J. Exp. Med. 200 2004 425 435
56. Oka N. Nakahara S. Takenaka Y. Fukumori T. Hogan V. Kanayama H.O. Yanagawa T. Raz A. Galectin-3 inhibits tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells Cancer Res. 65 2005 7546 7553
57. Ouyang B. Knauf J.A. Smith E.P. Zhang L. Ramsey T. Yusuff N. Batt D. Fagin J.A. Inhibitors of Raf kinase activity block growth of thyroid cancer cells with RET/PTC or BRAF mutations in vitro and in vivo Clin. Cancer Res. 12 2006 1785 1793
58. Ozawa K. Kuwabara K. Tamatani M. Takatsuji K. Tsukamoto Y. Kaneda S. Yanagi H. Stern D.M. Eguchi Y. Tsujimoto Y. Ogawa S. Tohyama M. 150-kDa oxygen-regulated protein (ORP150) suppresses hypoxia-induced apoptotic cell death J. Biol. Chem. 274 1999 6397 6404
59. Ozawa K. Tsukamoto Y. Hori O. Kitao Y. Yanagi H. Stern D.M. Ogawa S. Regulation of tumor angiogenesis by oxygen-regulated protein 150, an inducible endoplasmic reticulum chaperone Cancer Res. 61 2001 4206 4213
60. Pelham H.R. Speculations on the functions of the major heat shock and glucose-regulated proteins Cell 46 1986 959 961
61. Puchades M. Nilsson C.L. Emmett M.R. Aldape K.D. Ji Y. Lang F.F. Liu T.J. Conrad C.A. Proteomic investigation of glioblastoma cell lines treated with wild-type p53 and cytotoxic chemotherapy demonstrates an association between galectin-1 and p53 expression J. Proteome Res. 6 2007 869 875
62. Rong Y. Durden D.L. Van Meir E.G. Brat D.J. ʻPseudopalisading' necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis J. Neuropathol. Exp. Neurol. 65 2006 529 539
63. Shannon A.M. Bouchier-Hayes D.J. Condron C.M. Toomey D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies Cancer Treat. Rev. 29 2003 297 307
64. Strano S. DellʻOrso S. Di Agostino S. Fontemaggi G. Sacchi A. Blandino G. Mutant p53: an oncogenic transcription factor Oncogene 26 2007 2212 2219
65. Strik H.M. Schmidt K. Lingor P. Tonges L. Kugler W. Nitsche M. Rabinovich G.A. Bahr M. Galectin-1 expression in human glioma cells: modulation by ionizing radiation and effects on tumor cell proliferation and migration Oncol. Rep. 18 2007 483 488
66. Stupp R. Mason W.P. van den Bent M.J. Weller M. Fisher B. Taphoorn M.J. Belanger K. Brandes A.A. Marosi C. Bogdahn U. Curschmann J. Janzer R.C. Ludwin S.K. Gorlia T. Allgeier A. Lacombe D. Cairncross J.G. Eisenhauer E. Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma N. Engl.J. Med. 352 2005 987 996
67. Swanton C. Marani M. Pardo O. Warne P.H. Kelly G. Sahai E. Elustondo F. Chang J. Temple J. Ahmed A.A. Brenton J.D. Downward J. Nicke B. Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs Cancer Cell 11 2007 498 512
68. Takenaka Y. Fukumori T. Yoshii T. Oka N. Inohara H. Kim H.R. Bresalier R.S. Raz A. Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs Mol. Cell. Biol. 24 2004 4395 4406
69. Team T.R.D.C. R: A Language and Environment for Statistical Computing 2006 R Foundation for Statistical Coumputing Vienna, Austria
70. Thakker D.R. Natt F. Husken D. Maier R. Muller M. van der Putten H. Hoyer D. Cryan J.F. Neurochemical and behavioral consequences of widespread gene knockdown in the adult mouse brain by using nonviral RNA interference Proc. Natl. Acad. Sci. 101 2004 17270 17275
71. Thijssen V.L. Postel R. Brandwijk R.J. Dings R.P. Nesmelova I. Satijn S. Verhofstad N. Nakabeppu Y. Baum L.G. Bakkers J. Mayo K.H. Poirier F. Griffioen A.W. Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy Proc. Natl. Acad. Sci. 103 2006 15975 15980
72. Thijssen V.L. Poirier F. Baum L.G. Griffioen A.W. Galectins in the tumor endothelium; opportunities for combined cancer therapy Blood 110 2007 2819 2827
73. Tsutsumi S. Namba T. Tanaka K.I. Arai Y. Ishihara T. Aburaya M. Mima S. Hoshino T. Mizushima T. Celecoxib upregulates endoplasmic reticulum chaperones that inhibit celecoxib-induced apoptosis in human gastric cells Oncogene 25 2006 1018 1029
74. Ueda K. Arakawa H. Nakamura Y. Dual-specificity phosphatase 5 (DUSP5) as a direct transcriptional target of tumor suppressor p53 Oncogene 22 2003 5586 5591
75. Uhrbom L. Kastemar M. Johansson F.K. Westermark B. Holland E.C. Cell type-specific tumor suppression by Ink4a and Arf in Kras-induced mouse gliomagenesis Cancer Res. 65 2005 2065 2069
76. Valenzuela H.F. Pace K.E. Cabrera P.V. White R. Porvari K. Kaija H. Vihko P. Baum L.G. O -glycosylation regulates LNCaP prostate cancer cell susceptibility to apoptosis induced by galectin-1 Cancer Res. 67 2007 6155 6162
77. Weaver D.A. Crawford E.L. Warner K.A. Elkhairi F. Khuder S.A. Willey J.C. ABCC5, ERCC2, XPA and XRCC1 transcript abundance levels correlate with cisplatin chemoresistance in non-small cell lung cancer cell lines Mol. Cancer 4 2005 18
78. Wild-Bode C. Weller M. Rimner A. Dichgans J. Wick W. Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma Cancer Res. 61 2001 2744 2750
79. Wilson C.L. Miller C.J. Simpleaffy: a BioConductor package for Affymetrix quality control and data analysis Bioinformatics 21 2005 3683 3685
80. Zhang F. Hamanaka R.B. Bobrovnikova-Marjon E. Gordan J.D. Dai M.S. Lu H. Simon M.C. Diehl J.A. Ribosomal stress couples the unfolded protein response to p53-dependent cell cycle arrest J. Biol. Chem. 281 2006 30036 30045