Cell-surface galectin-3 confers resistance to TRAIL by impeding trafficking of death receptors in metastatic colon adenocarcinoma cells

Cell Death and Differentiation

Volumn 19, Issue 3, 2012, Pages 523-533

  Mazurek, N ^a   Byrd, J C ^a   Sun, Y ^a   Hafley, M ^a   Ramirez, K ^a   Burks, J ^a   Bresalier, R S ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

apoptosis; colon cancer; galectin 3; TRAIL

Indexed keywords

CASPASE 8; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; DEATH RECEPTOR; GALECTIN 3; LECTIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; WNT PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL STIMULATION; CELL SURFACE; CELL SURVIVAL; COLON ADENOCARCINOMA; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; APOPTOSIS; CASPASE 8; CELL LINE, TUMOR; COLONIC NEOPLASMS; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEINS; DRUG RESISTANCE, NEOPLASM; GALECTIN 3; GENE SILENCING; GLYCOSYLATION; HUMANS; MAP KINASE KINASE 4; NEOPLASM PROTEINS; PROTEIN TRANSPORT; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84857048734     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.123     Document Type: Article

References (40)

1. Ashkenazi A, Herbst RS. To kill a tumor cell: The potential of proapoptotic receptor agonists. J Clin Invest 2008; 118: 1979-1990. (Pubitemid 351872316)
2. Wiezorek J, Holland P, Graves J. Death receptor agonists as a targeted therapy for cancer. Clin Cancer Res 2010; 16: 1701-1708.
3. Abdulghani J, El-Deiry WS. TRAIL receptor signaling and therapeutics. Expert Opin Ther Targets 2010; 14: 1091-1108.
4. Wagner KW, Punnoose EA, Januario T, Lawrence DA, Pitti RM, Lancaster K et al. Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat Med 2007; 13: 1070-1077. (Pubitemid 47517508)
5. Zhang Y, Yoshida T, Zhang B. TRAIL induces endocytosis of its death receptors in MDA-MB-231 breast cancer cells. Cancer Biol Ther 2009; 8: 917-922.
6. Akazawa Y, Mott JL, Bronk SF, Werneburg NW, Kahraman A, Guicciardi ME et al. Death receptor 5 internalization is required for lysosomal permeabilization by TRAIL in malignant liver cell lines. Gastroenterology 2009; 136: 2365-2376.
7. Kohlhaas SL, Craxton A, Sun XM, Pinkowski MJ, Cohen GM. Receptor-mediated endocytosis is not required for tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis. J Biol Chem 2007; 282: 12831-12841. (Pubitemid 47100635)
8. Austin CD, Lawrence DA, Peden AA, Varfolomeev EE, Totpal K, De Maziere AM et al. Death-receptor activation halts clathrin-dependent endocytosis. Proc Natl Acad Sci USA 2006; 103: 10283-10288. (Pubitemid 44051158)
9. Suliman A, Lam A, Datta R, Srivastava RK. Intracellular mechanisms of TRAIL: Apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 2001; 20: 2122-2133. (Pubitemid 32424006)
10. Ehrhardt H, Fulda S, Schmid I, Hiscott J, Debatin KM, Jeremias I. TRAIL induced survival and proliferation in cancer cells resistant towards TRAIL-induced apoptosis mediated by NF-kappaB. Oncogene 2003; 22: 3842-3852. (Pubitemid 36819657)
11. Falschlehner C, Emmerich CH, Gerlach B, Walczak H. TRAIL signalling: Decisions between life and death. Int J Biochem Cell Biol 2007; 39: 1462-1475. (Pubitemid 47031030)
12. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 1999; 5: 157-163. (Pubitemid 29068521)
13. Jin Z, McDonald ER, Dicker DT, El-Deiry WS. Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 2004; 279: 35829-35839. (Pubitemid 39100590)
14. Kuang AA, Diehl GE, Zhang J, Winoto A. FADD is required for DR4-And DR5-mediated apoptosis: Lack of trail-induced apoptosis in FADD-deficient mouse embryonic fibroblasts. J Biol Chem 2000; 275: 25065-25068.
15. Zhang L, Zhu H, Teraishi F, Davis JJ, Guo W, Fan Z et al. Accelerated degradation of caspase-8 protein correlates with TRAIL resistance in a DLD1 human colon cancer cell line. Neoplasia 2005; 7: 594-602. (Pubitemid 40967760)
16. Larribere L, Khaled M, Tartare-Deckert S, Busca R, Luciano F, Bille K et al. PI3 K mediates protection against TRAIL-induced apoptosis in primary human melanocytes. Cell Death Differ 2004; 11: 1084-1091. (Pubitemid 39341634)
17. Mazurek N, Sun YJ, Liu KF, Gilcrease MZ, Schober W, Nangia-Makker P et al. Phosphorylated galectin-3 mediates tumor necrosis factor-related apoptosis-inducing ligand signaling by regulating phosphatase and tensin homologue deleted on chromosome 10 in human breast carcinoma cells. J Biol Chem 2007; 282: 21337-21348. (Pubitemid 47099965)
18. Oka N, Nakahara S, Takenaka Y, Fukumori T, Hogan V, Kanayama HO et al. Galectin-3 inhibits tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells. Cancer Res 2005; 65: 7546-7553. (Pubitemid 41297223)
19. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T et al. Galectins: A family of animal beta-galactoside-binding lectins. Cell 1994; 76: 597-598. (Pubitemid 24070645)
20. Iurisci I, Tinari N, Natoli C, Angelucci D, Cianchetti E, Iacobelli S. Concentrations of galectin-3 in the sera of normal controls and cancer patients. Clin Cancer Res 2000; 6: 1389-1393. (Pubitemid 30226225)
21. Gong HC, Honjo Y, Nangia-Makker P, Hogan V, Mazurak N, Bresalier RS et al. The NH2 terminus of galectin-3 governs cellular compartmentalization and functions in cancer cells. Cancer Res 1999; 59: 6239-6245. (Pubitemid 30035648)
22. Dumic J, Dabelic S, Flogel M. Galectin-3: An open-ended story. Biochim Biophys Acta 2006; 1760: 616-635. (Pubitemid 44382499)
23. Garner OB, Baum LG. Galectin-glycan lattices regulate cell-surface glycoprotein organization and signalling. Biochem Soc Trans 2008; 36: 1472-1477.
24. Thiemann S, Baum LG. The road less traveled: Regulation of leukocyte migration across vascular and lymphatic endothelium by galectins. J Clin Immunol 2011; 31: 2-9.
25. Earl LA, Bi S, Baum LG. Galectin multimerization and lattice formation are regulated by linker region structure. Glycobiology 2011; 21: 6-12.
26. Nangia-Makker P, Balan V, Raz A. Regulation of tumor progression by extracellular galectin-3. Cancer Microenviron 2008; 1: 43-51.
27. Wei J, Barr J, Kong LY, Wang Y, Wu A, Sharma AK et al. Gliomaassociated cancer-initiating cells induce immunosuppression. Clin Cancer Res 2010; 16: 461-473.
28. Inohara H, Raz A. Functional evidence that cell surface galectin-3 mediates homotypic cell adhesion. Cancer Res 1995; 55: 3267-3271.
29. Chan FK, Chun HJ, Zheng L, Siegel RM, Bui KL, Lenardo MJ. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science 2000; 288: 2351-2354. (Pubitemid 30448156)
30. Clancy L, Mruk K, Archer K, Woelfel M, Mongkolsapaya J, Screaton G et al. Preligand assembly domain-mediated ligand-independent association between TRAIL receptor 4 (TR4) and TR2 regulates TRAIL-induced apoptosis. Proc Natl Acad Sci USA 2005; 102: 18099-18104. (Pubitemid 41798508)
31. Bresalier RS, Raper SE, Hujanen ES, Kim YS. A new animal model for human colon cancer metastasis. Int J Cancer 1987; 39: 625-630. (Pubitemid 17084736)
32. Garofalo M, Di Leva G, Romano G, Nuovo G, Suh SS, Ngankeu A et al. miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009; 16: 498-509.
33. Cummins JM, Kohli M, Rago C, Kinzler KW, Vogelstein B, Bunz F. X-linked inhibitor of apoptosis protein (XIAP) is a nonredundant modulator of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis in human cancer cells. Cancer Res 2004; 64: 3006-3008. (Pubitemid 38581397)
34. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002; 8: 808-815.
35. Igney FH, Krammer PH. Death and anti-death: Tumour resistance to apoptosis. Nat Rev Cancer 2002; 2: 277-288. (Pubitemid 37328781)
36. Gross A, Yin XM, Wang K, Wei MC, Jockel J, Milliman C et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 1999; 274: 1156-1163.
37. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M et al. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 2007; 129: 123-134. (Pubitemid 46507588)
38. Guo HB, Johnson H, Randolph M, Lee I, Pierce M. Knockdown of GnT-Va expression inhibits ligand-induced downregulation of the epidermal growth factor receptor and intracellular signaling by inhibiting receptor endocytosis. Glycobiology 2009; 19: 547-559.
39. Lee KH, Feig C, Tchikov V, Schickel R, Hallas C, Schü tze S et al. The role of receptor internalization in CD95 signaling. EMBO J 2006; 25: 1009-1023. (Pubitemid 43372115)
40. Schneider-Brachert W, Tchikov V, Neumeyer J, Jakob M, Winoto-Morbach S et al. Compartmentalization of TNF receptor 1 signaling: Internalized TNF receptosomes as death signaling vesicles. Immunity 2004; 21: 415-428. (Pubitemid 39208342)