Increased expression of colonic Wnt9A through Sp1-mediated transcriptional effects involving arylsulfatase B, chondroitin 4-sulfate, and Galectin-3

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 14564-14575

  Bhattacharyya, Sumit ^a,b   Feferman, Leo ^a,b   Tobacman, Joanne K ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ENZYME ACTIVITY; MAMMALS; OLIGONUCLEOTIDES;

BINDING ASSAYS; CHROMATIN IMMUNOPRECIPITATION ASSAY; COLON CARCINOMA; CONSENSUS SEQUENCE; EPITHELIAL CELLS; OLIGONUCLEOTIDE BINDING; SPECIFIC INHIBITORS; TRANSCRIPTIONAL MECHANISMS;

CELL SIGNALING;

CARRAGEENAN; CHONDROITIN 4 SULFATE; GALECTIN 3; MESSENGER RNA; N ACETYLGALACTOSAMINE 4 SULFATASE; TRANSCRIPTION FACTOR SP1; WNT9A PROTEIN; ARYLSULFATASE B, HUMAN; CHONDROITIN SULFATE; DRUG DERIVATIVE; GALECTIN; GALECTIN 3, HUMAN; GALECTIN-3, HUMAN; LGALS3 PROTEIN, MOUSE; MITHRAMYCIN; MITHRAMYCIN A; WNT PROTEIN; WNT9A PROTEIN, HUMAN; WNT9A PROTEIN, MOUSE;

AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE REGULATION; CELL FATE; CELL PROLIFERATION; COLON MUCOSA; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; FEMALE; GENE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SULFATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WNT9A GENE; ANIMAL; ANIMAL MODEL; BIOSYNTHESIS; CANCER BIOLOGY; CELL LINE; COLON; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; INTESTINE MUCOSA; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY; SPECIFICITY PROTEIN 1 (SP1); WNT;

ANIMAL MODEL; CANCER BIOLOGY; CARRAGEENAN; CHONDROITIN SULFATE; GALECTIN; SPECIFICITY PROTEIN 1 (SP1); WNT;

ANIMALS; CARRAGEENAN; CELL LINE; CHONDROITIN SULFATES; COLON; EPITHELIAL CELLS; GALECTIN 3; GENE EXPRESSION REGULATION; HUMANS; INTESTINAL MUCOSA; MALE; MICE; MICE, MUTANT STRAINS; N-ACETYLGALACTOSAMINE-4-SULFATASE; PLICAMYCIN; PROMOTER REGIONS, GENETIC; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; WNT PROTEINS;

EID: 84903451443     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.561589     Document Type: Article

References (61)

1. Clevers, H. (2006) Wnt/β-catenin signaling in development and disease. Cell 127, 469-480
2. Reya, T., and Clevers, H. (2005) Wnt signaling in stem cells and cancer. Nature 434, 843-850 (Pubitemid 40558990)
3. Bhattacharyya, S., Feferman, L., Borthakur, S., and Tobacman, J. K. (2014) Common food additive carrageenan stimulates Wnt/β-catenin signaling in colonic epithelium by inhibition of nucleoredoxin reduction. Nutr. Cancer 66, 117-127
4. Funato, Y., and Miki, H. (2010) Redox regulation of Wnt signaling via nucleoredoxin. Free Radic. Res. 44, 379-388
5. Schwarz-Romond, T., Fiedler, M., Shibata, N., Butler, P. J., Kikuchi, A., Higuchi Y, Bienz M. (2007) The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat. Struct. Mol. Biol. 14, 484-492 (Pubitemid 46871810)
6. Bhattacharyya, S., Borthakur, A., Dudeja, P. K., and Tobacman, J. K. (2007) Carrageenan reduces bone morphogenetic protein-4 (BMP4) and activates Wnt/β-catenin pathway in normal human colonic epithelial cells. Dig. Dis. Sci. 52, 2766-2774 (Pubitemid 47373880)
7. Cox, A. A., Jezewski, P. A., Fang, P. K., and Payne-Ferreira, T. L. (2010) Zebrafish Wnt9a, 9b paralog comparisons suggest ancestral roles for Wnt9 in neural, oral-pharyngeal ectoderm and mesoendoderm. Gene Expr. Patterns 10, 251-258
8. An, C. H., Kim, S. S., Kang, M. R., Kim, Y. R., Kim, H. S., Yoo, N. J., and Lee, S. H. (2010) Frameshift mutations of ATBF1, WNT9A, CYLD, and PARK2 in gastric and colorectal carcinomas with high microsatellite instability. Pathology 42, 583-585
9. Kirikoshi, H., Sekihara, H., and Katoh, M. (2001) Expression of WNT14 and WNT14B mRNAs in human cancer, up-regulation of WNT14 by IFN γ and up-regulation of WNT14B by β-estradiol. Int. J. Oncol. 19, 1221-1225
10. Shu, J., Jelinek, J., Chang, H., Shen, L., Qin, T., Chung, W., Oki, Y., and Issa, J. P. (2006) Silencing of bidirectional promoters by DNA methylation in tumorigenesis. Cancer Res. 66, 5077-5084 (Pubitemid 43844929)
11. Olender, T., Safran, M., Edgar R., Stelzer, G., Nativ, N., Rosen, N., Shtrichman, R., Mazor, Y., West, M. D., Keydar, I., Rappaport, N., Belinky, F., Warshawsky, D., and Lancet, D. (2013) An overview of synergistic data tools for biological scrutiny. Isr. J. Chem. 53, 185-198
12. Zhu, G. H., Lenzi, M., and Schwartz, E. L. (2002) The Sp1 transcriptional factor contributes to the tumor necrosis factor-induced expression of the angiogenic factor thymidine phosphorylase in human colon carcinoma cells. Oncogene 21, 8477-8485 (Pubitemid 36054888)
13. Kovarik, A., Lu, P. J., Peat, N., Morris, J., and Taylor-Papadimitriou, J. (1996) Regulation of the activity of the epithelium-specific MUC1 promoter. J. Biol. Chem. 271, 18140-18147
14. Keith, W. N., Vulliamy, T., Zhao, J., Ar, C., Erzik, C., Bilsland, A., Ulku, B., Marrone, A., Mason, P. J., Bessler, M., Serakinci, N., and Dokal, I. (2004) A mutation in a functional Sp1 binding site of the telomerase RNA gene (hTERC) promoter in a patient with Paroxysmal Nocturmal Haemoglobinuria. BMC Blood Disord. 4, 3
15. Onishi, T., Yamakawa, K., Franco, O. E., Kawamura, J., Watanabe, M., Shiraishi, T., and Kitazawa, S. (2001) Mitogen-activated protein kinase pathway is involved in α6 integrin gene expression in androgen-independent prostate cancer cells: role of proximal Sp1 consensus sequence. Biochim. Biophys. Acta 1538, 218-227 (Pubitemid 32402244)
16. Zhao, Y., Zhang, W., Guo, Z., Ma, F., Wu, Y., Bai, Y., Gong, W., Chen, Y., Cheng, T., Zhi, F., Zhang, Y., Wang, J., and Jiang, B. (2013) Inhibition of the transcription factor Sp1 suppresses colon cancer stem cell growth and induces apoptosis in vitro and in nude mice. Oncol. Rep. 30, 1782-1792
17. Wang, F., Ma, Y. L., Zhang, P., Shen, T. Y., Shi, C. Z., Yang, Y. Z., Moyer, M. P., Zhang, H. Z., Chen, H. Q., Liang, Y., and Qin, H. L. (2013) Sp1 mediates the link between methylation of the tumour suppressor miR-149 and outcome in colorectal cancer. J. Pathol. 229, 12-24
18. Maurer, G. D., Leupold, J. H., Schewe, D. M., Biller, T., Kates, R. E., Hornung, H. M., Lau-Werner, U., Post, S., and Allgayer, H. (2007) Analysis of specific transcriptional regulators as early predictors of independent relevance in resected colorectal cancer. Clin. Cancer Res. 13, 1123-1132 (Pubitemid 46424051)
19. Chang, W. C., and Hung, J. J. (2012) Functional role of post-translational modifications of Sp1 in tumorigenesis. J. Biomed. Sci. 19, 94
20. Lin, H. M., Pestell, R. G., Raz, A., and Kim, H. R. (2002) Galectin-3 enhances cyclin D1 promoter activity through SP1 and a cAMP-responsive element in human breast epithelial cells. Oncogene 21, 8001-8010 (Pubitemid 35430611)
21. Bhattacharyya, S., and Tobacman, J. K. (2012) Hypoxia reduces arylsulfatase B activity and silencing arylsulfatase B replicates and mediates the effects of hypoxia. PLoS One 7, e33250
22. Bhattacharyya, S., Feferman, L., and Tobacman, J. K. (2013) Arylsulfatase B regulates versican expression by galectin-3 and AP-1 mediated transcriptional effects. Oncogene 10.1038/onc.2013.483
23. Iwaki, J., Minamisawa, T., Tateno, H., Kominami, J., Suzuki, K., Nishi, N., Nakamura, T., and Hirabayashi, J. (2008) Desulfated galactosaminoglycans are potential ligands for galectins: evidence from frontal affinity chromatography. Biochem. Biophys. Res. Commun. 373, 206-212
24. Yoo, B. C., Hong, S. H., Ku, J. L., Kim, Y. H., Shin, Y. K., Jang, S. G., Kim, I. J., Jeong, S. Y., and Park, J. G. (2009) Galectin-3 stabilizes heterogeneous nuclear ribonucleoprotein Q to maintain proliferation of human colon cancer cells. Cell Mol. Life Sci. 66, 350-364
25. Wang, L., Inohara, H., Pienta, K. J., and Raz, A. (1995) Galectin-3 is a nuclear matrix protein which binds RNA. Biochem. Biophys. Res. Commun. 217, 292-303 (Pubitemid 26004793)
26. Song, S., Byrd, J. C., Mazurek, N., Liu, K., Koo, J. S., and Bresalier, R. S. (2005) Galectin-3 modulates MUC2 mucin expression in human colon cancer cells at the level of transcription via AP-1 activation. Gastroenterology 129, 1581-1591 (Pubitemid 41597398)
27. Yang, B., Bhattacharyya, S., Linhardt, R., and Tobacman, J. (2012) Exposure to common food additive carrageenan leads to reduced sulfatase activity and increase in sulfated glycosaminoglycans in human epithelial cells. Biochimie 94, 1309-1316
28. Heinemeyer, T., Wingender, E., Reuter, I., Hermjakob, H., Kel, A. E., Kel, O. V., Ignatieva, E. V., Ananko, E. A., Podkolodnaya, O. A., Kolpakov, F. A., Podkolodny, N. L., and Kolchanov, N. A. (1998) Databases on transcriptional regulation: TRANSFAC, TRRD, and COMPEL. Nucleic Acids Res. 26, 362-367 (Pubitemid 28295292)
29. Feferman, L., Bhattacharyya, S., Deaton, R., Gann, P., Guzman, G., Kajdacsy-Balla, A., and Tobacman, J. K. (2013) Arylsulfatase B (N-acetylgalactosamine-4-sulfatase): potential role as a biomarker in prostate cancer. Prostate Cancer Prostatic Dis. 16, 277-284
30. Prabhu, S. V., Bhattacharyya, S., Guzman-Hartman, G., Macias, V., Kajdacsy-Balla, A., and Tobacman, J. K. (2011) Extra-lysosomal localization of arylsulfatase B in human colonic epithelium. J. Histochem. Cytochem. 59, 328-335
31. Bhattacharyya, S., and Tobacman, J. K. (2009) Arylsulfatase B regulates colonic epithelial cell migration by effects on MMP9 expression and RhoA activation. Clin. Exp. Metastasis 26, 535-545
32. Bhattacharyya, S., Kotlo, K., Shukla, S., Danziger, R. S., and Tobacman, J. K. (2008) Distinct effects of N-acetylgalactosamine-4-sulfatase and galactose-6-sulfatase expression on chondroitin sulfate. J. Biol. Chem. 283, 9523-9530
33. Bhattacharyya, S., and Tobacman, J. K. (2007) Steroid sulfatase, arylsulfatases A and B, galactose 6-sulfatase, and iduronate sulfatase in mammary cells and effects of sulfated and non-sulfated estrogens on sulfatase activity. J. Steroid Biochem. Mol. Biol. 103, 20-34 (Pubitemid 44821815)
34. Moyer, M. P., Manzano, L. A., Merriman, R. L., Stauffer, J. S., and Tanzer, L. R. (1996) NCM460, a normal human colon mucosal epithelial cell line. In Vitro Cell Dev. Biol. Anim. 32, 315-317
35. Curtain, M. M., and Donahue, L. R. (2009) A mutation in the Arsb gene: a mouse model that resembles Maroteaux-Lamy syndrome. Mouse Genome Informatics, The Jackson Laboratory, J:149960
36. Rozen, S., and Skaletsky, H. (2000) Primer3 on WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386
37. Sleiman, S. F., Langley, B. C., Basso, M., Berlin, J., Xia, L., Payappilly, J. B., Kharel, M. K., Guo, H., Marsh, J. L., Thompson, L. M., Mahishi, L., Ahuja, P., MacLellan, W. R., Geschwind, D. H., Coppola, G., Rohr, J., and Ratan, R. R. (2011) Mithramycin is a gene-selective Sp1 inhibitor that identifies a biological intersection between cancer and neurodegeneration. J. Neurosci. 31, 6858-6870
38. Blume, S. W., Snyder, R. C., Ray, R., Thomas, S., Koller, C. A., and Miller, D. M. (1991) Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J. Clin. Invest. 88, 1613-1621
39. Tobacman, J. K. (2001) Review of harmful gastrointestinal effects of carrageenan in animal experiments. Environ. Health Perspect. 109, 983-994
40. IARC Working Group on the Evaluation of the Carcinogenic Risk of Chemicals to Humans (1983) Carrageenan. IARC Monogr. Eval. Carcinog. Risk Chem. Hum. 31, 79-94
41. Watanabe, K., Reddy, B. S., Wong, C. Q., and Weisburger, J. H. (1978) Effect of dietary undegraded carrageenan on colon carcinogenesis in F344 rats treated with azoxymethane or methylnitrosourea. Cancer Res. 38, 4427-4430 (Pubitemid 9065411)
42. Kawaura, A., Shibata, M., Togei, K., and Otsuka, H. (1982) Effect of dietary degraded carrageenan on intestinal carcinogenesis in rats treated with 1,2-dimethylhydrazine dihydrochloride. Tokushima J. Exp. Med. 29, 125-129 (Pubitemid 13226927)
43. Arakawa, S., Okumura, M., Yamada, S., Ito, M., and Tejima, S. (1986) Enhancing effect of carrageenan on the induction of rat colonic tumors by 1,2-dimethylhydrazine and its relation to β-glucuronidase activities in feces and other tissues. J. Nutr. Sci. Vitaminol. 32, 481-485
44. Gold, L. S., Slone, T. H., Manley, N. B., Garfinkel, G. A., Rohrbach, L., and Ames, B. N. (1997) Carcinogenic Potency Database in The Handbook of Carcinogenic Potency and Genotoxicity Databases (Gold, L. S., and Zeiger, E., eds) pp. 116-117, CRC Press, Inc., New York
45. Encyclopædia Britannica Macropedia (2010) Algae. Volume 13, p. 236, Encyclopædia Britannica, Inc., Chicago
46. Serafini, E. P., Kirk, A. P., and Chambers, T. J. (1981) Rate and pattern of epithelial cell proliferation in ulcerative colitis. Gut 22, 648-652 (Pubitemid 11018268)
47. Bhattacharyya, S., Dudeja, P. K., and Tobacman, J. K. (2008) Carrageenan-induced NFκB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10. Biochim. Biophys. Acta 1780, 973-982
48. Bhattacharyya, S., Gill, R., Chen, M. L., Zhang, F., Linhardt, R. J., Dudeja, P. K., and Tobacman, J. K. (2008) Toll-like receptor 4 mediates induction of Bcl10-NFκB-IL-8 inflammatory pathway by carrageenan in human intestinal epithelial cells. J. Biol. Chem. 283, 10550-10558
49. Bhattacharyya, S., Liu, H., Zhang, Z., Jam, M., Dudeja, P. K., Michel, G., Linhardt, R. J., and Tobacman, J. K. (2010) Carrageenan-induced innate immune response is modified by enzymes that hydrolyze distinct galactosidic bonds. J. Nutr. Biochem. 21, 906-913
50. Yokoyama, K. D., and Pollock, D. D. (2012) SP Transcription factor paralogs and DNA-binding sites coevolve and adaptively converge in mammals and birds. Genome Biol. Evol. 4, 1102-1117
51. Hagen, G., Müller, S., Beato, M., and Suske, G. (1994) Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13, 3843-3851 (Pubitemid 24275030)
52. Majello, B., De Luca, P., Suske, G., and Lania, L. (1995) Differential transcriptional regulation of c-myc promoter through the same DNA binding sites targeted by Sp1-like proteins. Oncogene 10, 1841-1848
53. Yu, B., Datta, P. K., and Bagchi, S. (2003) Stability of the Sp3-DNA complex is promoter-specific: Sp3 efficiently competes with Sp1 for binding to promoters containing multiple Sp-sites. Nucleic Acids Res. 31, 5368-5376 (Pubitemid 37441905)
54. Pagliuca, A., Gallo, P., and Lania, L. (2000) differential role for Sp1/Sp3 transcription factors in the regulation of the promoter activity of multiple cyclin-dependent kinase inhibitor genes. J. Cell Biochem. 76, 360-367 (Pubitemid 30078445)
55. Encarnacao, P. C., Ramirez, V. P., and Zhang, C., and Aneskievich, B. J. (2013) Sp sites contribute to basal and inducible expression of the human TNIP1 (TNFα-inducible protein 3-interaction protein 1) promoter. Biochem. J. 452, 519-529
56. Li, L., and Davie, J. R. (2010) the role of Sp1 and Sp3 in normal and cancer cell biology. Ann. Anat. 192, 275-283
57. Hagen, G., Dennig, J., Preiss, A., Beato, M., and Suske, G. (1995) Functional analyses of the transcription factor Sp4 reveal properties distinct from Sp1 and Sp3. J. Biol. Chem. 270, 24989-24994
58. +-ATPase by neuron-specific transcription factor Sp4: implication in the tight coupling of energy production, neuronal activity and energy consumption in neurons. Eur. J. Neurosci. 39, 566-578
59. Priya, A., Johar, K., Nair, B., and Wong-Riley, M. T. (2014) Specificity protein 4 (Sp4) regulates the transcription of AMPA receptor subunit GluA2 (Gria2). Biochim. Biophys. Acta 1843, 1196-1206
60. Danielson, K. G., Pillarisetti J., Cohen, I. R., Sholehvar, B., Huebner K., Ng, L. J., Nicholls, J. M., Cheah, K. S., and Iozzo, R. V. (1995) Characterization of the complete genomic structure of the human WNT-5A gene, functional analysis of its promoter, chromosomal mapping, and expression in early human embryogenesis. J. Biol. Chem. 270, 31225-31234 (Pubitemid 26012209)
61. Kumawat, K., Menzen, M. H., Slegtenhorst, R. M., Halayko, A. J., Schmidt, M., and Gosens, R. (2014) TGF-β-activated kinase 1 (TAK1) signaling regulates TGF-β-induced WNT-5A expression in airway smooth muscle cells via Sp1 and β-catenin. PLoS One 9, e94801