Transcriptional regulation of the protocadherin β cluster during her-2 protein-induced mammary tumorigenesis results from altered N-glycan branching

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 24941-24954

  Guo, Huabei ^a,b   Nairn, Alison ^a,b   Dela Rosa, Mitche ^a,b   Nagy, Tamas ^b   Zhao, Shaying ^a   Moremen, Kelley ^a,b   Pierce, Michael ^a,b  

^a University of Georgia ^*  (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION MOLECULES; CELL SURFACE RECEPTORS; DIFFERENTIALLY EXPRESSED GENE; GENE CLUSTERS; IN-VIVO; MAMMARY TUMORS; MICROARRAY ANALYSIS; MOUSE MODELS; N-GLYCAN; N-LINKED GLYCANS; OVER-EXPRESSION; PROMOTER METHYLATION; RECEPTOR SIGNALING; SIGNALING PATHWAYS; TRANSCRIPTIONAL REGULATION; TUMOR FORMATION; TUMORIGENESIS; UP-REGULATION; WILD TYPES;

ALKYLATION; CELL MEMBRANES; MAMMALS; RNA; TUMORS;

GENE EXPRESSION;

EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLYCAN; MICRORNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER INHIBITION; CANCER TISSUE; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE CLUSTER; GENE IDENTIFICATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTOCADHERIN BETA GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE; UPREGULATION;

ANIMALS; BREAST NEOPLASMS; CADHERINS; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, KNOCKOUT; MICRORNAS; MULTIGENE FAMILY; N-ACETYLGLUCOSAMINYLTRANSFERASES; RECEPTOR, ERBB-2; RNA, NEOPLASM; TRANSCRIPTION, GENETIC;

MUS;

EID: 84864108807     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.369355     Document Type: Article

References (59)

1. Boscher, C., Dennis, J. W., and Nabi, I. R. (2011) Glycosylation, galectins and cellular signaling. Curr. Opin. Cell Biol. 23, 383-392
2. Hakomori, S. (2002) Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. U.S.A. 99, 10231-10233
3. Zhao, Y. Y., Takahashi, M., Gu, J. G., Miyoshi, E., Matsumoto, A., Kitazume, S., and Taniguchi, N. (2008) Functional roles of N-glycans in cell signaling and cell adhesion in cancer. Cancer Sci. 99, 1304-1310 (Pubitemid 351761717)
4. Demetriou, M., Nabi, I. R., Coppolino, M., Dedhar, S., and Dennis, J. W. (1995) Reduced contact-inhibition and substratum adhesion in epithelial cells expressing GlcNAc-transferase V. J. Cell Biol. 130, 383-392
5. Granovsky, M., Fata, J., Pawling, J., Muller, W. J., Khokha, R., and Dennis, J. W. (2000) Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat. Med. 6, 306-312 (Pubitemid 30148623)
6. Guo, H. B., Lee, I., Kamar, M., Akiyama, S. K., and Pierce, M. (2002) Aberrant N-glycosylation of β1 integrin causes reduced α5β1 integrin clustering and stimulates cell migration. Cancer Res. 62, 6837-6845 (Pubitemid 35424070)
7. Handerson, T., Camp, R., Harigopal, M., Rimm, D., and Pawelek, J. (2005) β1,6-Branched oligosaccharides are increased in lymph node metastases and predict poor outcome in breast carcinoma. Clin. Cancer Res. 11, 2969-2973 (Pubitemid 40525200)
8. Yamamoto, H., Swoger, J., Greene, S., Saito, T., Hurh, J., Sweeley, C., Leestma, J., Mkrdichian, E., Cerullo, L., Nishikawa, A., Ihara, Y., Taniguchi, N., and Moskal, J. R. (2000) β1,6-N-Acetylglucosamine-bearing N-glycans in human gliomas: implications for a role in regulating invasivity. Cancer Res. 60, 134-142 (Pubitemid 30058743)
9. Guo, H. B., Johnson, H., Randolph, M., Nagy, T., Blalock, R., and Pierce, M. (2010) Specific posttranslational modification regulates early events in mammary carcinoma formation. Proc. Natl. Acad. Sci. U.S.A. 107, 21116-21121
10. Seelentag, W. K., Li, W. P., Schmitz, S. F., Metzger, U., Aeberhard, P., Heitz, P. U., and Roth, J. (1998) Prognostic value of β1,6-branched oligosaccharides in human colorectal carcinoma. Cancer Res. 58, 5559-5564 (Pubitemid 28551145)
11. Guo, H. B., Johnson, H., Randolph, M., and Pierce, M. (2009) Regulation of homotypic cell-cell adhesion by branched N-glycosylation of N-cadherin extracellular EC2 and EC3 domains. J. Biol. Chem. 284, 34986-34997
12. Pinho, S. S., Reis, C. A., Paredes, J., Magalhães, A. M., Ferreira, A. C., Figueiredo, J., Xiaogang, W., Carneiro, F., Gärtner, F., and Seruca, R. (2009) The role of N-acetylglucosaminyltransferase III and V in the post-transcriptional modifications of E-cadherin. Hum. Mol. Genet. 18, 2599-2608
13. Partridge, E. A., Le Roy, C., Di Guglielmo, G. M., Pawling, J., Cheung, P., Granovsky, M., Nabi, I. R., Wrana, J. L., and Dennis, J. W. (2004) Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306, 120-124 (Pubitemid 39451953)
14. Guo, H. B., Randolph, M., and Pierce, M. (2007) Inhibition of a specific N-glycosylation activity results in attenuation of breast carcinoma cell invasiveness-related phenotypes: inhibition of epidermal growth factor-induced dephosphorylation of focal adhesion kinase. J. Biol. Chem. 282, 22150-22162 (Pubitemid 47195758)
15. Carlsson, J., Nordgren, H., Sjöström, J., Wester, K., Villman, K., Bengtsson, N. O., Ostenstad, B., Lundqvist, H., and Blomqvist, C. (2004) HER2 expression in breast cancer primary tumours and corresponding metastases. Original data and literature review. Br. J. Cancer 90, 2344-2348 (Pubitemid 38961898)
16. Slamon, D. J., Clark, G. M., Wong, S. G., Levin, W. J., Ullrich, A., and McGuire, W. L. (1987) Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177-182 (Pubitemid 17231334)
17. Muller, W. J., Sinn, E., Pattengale, P. K., Wallace, R., and Leder, P. (1988) Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54, 105-115
18. Guy, C. T., Webster, M. A., Schaller, M., Parsons, T. J., Cardiff, R. D., and Muller, W. J. (1992) Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. U.S.A. 89, 10578-10582
19. Takeichi, M. (1995) Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627
20. Yagi, T., and Takeichi, M. (2000) Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev. 14, 1169-1180 (Pubitemid 30327498)
21. Morishita, H., and Yagi, T. (2007) Protocadherin family: diversity, structure, and function. Curr. Opin. Cell Biol. 19, 584-592 (Pubitemid 350016857)
22. Wu, Q., and Maniatis, T. (1999) A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790 (Pubitemid 29278051)
23. Wu, Q., Zhang, T., Cheng, J. F., Kim, Y., Grimwood, J., Schmutz, J., Dickson, M., Noonan, J. P., Zhang, M. Q., Myers, R. M., and Maniatis, T. (2001) ComparativeDNAsequence analysis of mouse and human protocadherin gene clusters. Genome Res. 11, 389-404 (Pubitemid 32243849)
24. Wu, Q., and Maniatis, T. (2000) Large exons encoding multiple ectodomains are a characteristic feature of protocadherin genes. Proc. Natl. Acad. Sci. U.S.A. 97, 3124-3129 (Pubitemid 30183266)
25. Yu, J. S., Koujak, S., Nagase, S., Li, C. M., Su, T., Wang, X., Keniry, M., Memeo, L., Rojtman, A., Mansukhani, M., Hibshoosh, H., Tycko, B., and Parsons, R. (2008) PCDH8, the human homolog of PAPC, is a candidate tumor suppressor of breast cancer. Oncogene 27, 4657-4665
26. Novak, P., Jensen, T., Oshiro, M. M., Watts, G. S., Kim, C. J., and Futscher, B. W. (2008) Agglomerative epigenetic aberrations are a common event in human breast cancer. Cancer Res. 68, 8616-8625
27. Dallosso, A. R., Hancock, A. L., Szemes, M., Moorwood, K., Chilukamarri, L., Tsai, H. H., Sarkar, A., Barasch, J., Vuononvirta, R., Jones, C., Pritchard- Jones, K., Royer-Pokora, B., Lee, S. B., Owen, C., Malik, S., Feng, Y., Frank, M., Ward, A., Brown, K. W., and Malik, K. (2009) Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms' tumor. PLoS Genet. 5, e1000745
28. Yu, J., Cheng, Y. Y., Tao, Q., Cheung, K. F., Lam, C. N., Geng, H., Tian, L. W., Wong, Y. P., Tong, J. H., Ying, J. M., Jin, H., To, K. F., Chan, F. K., and Sung, J. J. (2009) Methylation of protocadherin 10, a novel tumor suppressor, is associated with poor prognosis in patients with gastric cancer. Gastroenterology 136, 640-651.e1
29. Nairn, A. V., Kinoshita-Toyoda, A., Toyoda, H., Xie, J., Harris, K., Dalton, S., Kulik, M., Pierce, J. M., Toida, T., Moremen, K. W., and Linhardt, R. J. (2007) Glycomics of proteoglycan biosynthesis in murine embryonic stem cell differentiation. J. Proteome Res. 6, 4374-4387 (Pubitemid 350158513)
30. Sharbati-Tehrani, S., Kutz-Lohroff, B., Bergbauer, R., Scholven, J., and Einspanier, R. (2008) miR-Q: a novel quantitative RT-PCR approach for the expression profiling of small RNA molecules such as miRNAs in a complex sample. BMC Mol. Biol. 9, 34
31. Gürlevik, E., Woller, N., Schache, P., Malek, N. P., Wirth, T. C., Zender, L., Manns, M. P., Kubicka, S., and Kühnel, F. (2009) p53-dependent antiviral RNA-interference facilitates tumor-selective viral replication. Nucleic Acids Res. 37, e84
32. Ginestier, C., Hur, M. H., Charafe-Jauffret, E., Monville, F., Dutcher, J., Brown, M., Jacquemier, J., Viens, P., Kleer, C. G., Liu, S., Schott, A., Hayes, D., Birnbaum, D., Wicha, M. S., and Dontu, G. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1, 555-567 (Pubitemid 350056407)
33. Fiegl, H., Millinger, S., Goebel, G., Müller-Holzner, E., Marth, C., Laird, P. W., and Widschwendter, M. (2006) Breast cancer DNA methylation profiles in cancer cells and tumor stroma: association with HER-2/neu status in primary breast cancer. Cancer Res. 66, 29-33 (Pubitemid 43166004)
34. Terada, K., Okochi-Takada, E., Akashi-Tanaka, S., Miyamoto, K., Taniyama, K., Tsuda, H., Asada, K., Kaminishi, M., and Ushijima, T. (2009) Association between frequent CpG island methylation and HER2 amplification in human breast cancers. Carcinogenesis 30, 466-471
35. Hoque, M. O., Prencipe, M., Poeta, M. L., Barbano, R., Valori, V. M., Copetti, M., Gallo, A. P., Brait, M., Maiello, E., Apicella, A., Rossiello, R., Zito, F., Stefania, T., Paradiso, A., Carella, M., Dallapiccola, B., Murgo, R., Carosi, I., Bisceglia, M., Fazio, V. M., Sidransky, D., and Parrella, P. (2009) Changes in CpG islands promoter methylation patterns during ductal breast carcinoma progression. Cancer Epidemiol. Biomarkers Prev. 18, 2694-2700
36. Huang, T. H., Wu, F., Loeb, G. B., Hsu, R., Heidersbach, A., Brincat, A., Horiuchi, D., Lebbink, R. J., Mo, Y. Y., Goga, A., and McManus, M. T. (2009) Up-regulation of miR-21 by HER2/neu signaling promotes cell invasion. J. Biol. Chem. 284, 18515-18524
37. Fujita, S., Ito, T., Mizutani, T., Minoguchi, S., Yamamichi, N., Sakurai, K., and Iba, H. (2008) miR-21 gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J. Mol. Biol. 378, 492-504
38. Pierce, J. M. (2009) in Handbook of Glycomics (Cummings, R. D., and Pierce, J. M., eds) 1st Ed., pp. 399-429, Elsevier, London
39. Obata, S., Sago, H., Mori, N., Rochelle, J. M., Seldin, M. F., Davidson, M., St John, T., Taketani, S., and Suzuki, S. T. (1995) Protocadherin Pcdh2 shows properties similar to, but distinct from, those of classical cadherins. J. Cell Sci. 108, 3765-3773 (Pubitemid 26004029)
40. Morishita, H., Umitsu, M., Murata, Y., Shibata, N., Udaka, K., Higuchi, Y., Akutsu, H., Yamaguchi, T., Yagi, T., and Ikegami, T. (2006) Structure of the cadherin-related neuronal receptor/protocadherin-α first extracellular cadherin domain reveals diversity across cadherin families. J. Biol. Chem. 281, 33650-33663 (Pubitemid 46036744)
41. Hambsch, B., Grinevich, V., Seeburg, P. H., and Schwarz, M. K. (2005) γ-Protocadherins, presenilin-mediated release of C-terminal fragment promotes locus expression. J. Biol. Chem. 280, 15888-15897 (Pubitemid 40616711)
42. Buchanan, S. M., Schalm, S. S., and Maniatis, T. (2010) Proteolytic processing of protocadherin proteins requires endocytosis. Proc. Natl. Acad. Sci. U.S.A. 107, 17774-17779
43. Jones, P. A., and Baylin, S. B. (2007) The epigenomics of cancer. Cell 128, 683-692 (Pubitemid 46273572)
44. Widschwendter, M., and Jones, P. A. (2002) DNA methylation and breast carcinogenesis. Oncogene 21, 5462-5482 (Pubitemid 34983482)
45. Wu, L., Fan, J., and Belasco, J. G. (2006) MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. U.S.A. 103, 4034-4039
46. Eulalio, A., Huntzinger, E., and Izaurralde, E. (2008) Getting to the root of miRNA-mediated gene silencing. Cell 132, 9-14
47. Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A., Downing, J. R., Jacks, T., Horvitz, H. R., and Golub, T. R. (2005) MicroRNA expression profiles classify human cancers. Nature 435, 834-838 (Pubitemid 40839735)
48. Calin, G. A., and Croce, C. M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866 (Pubitemid 44629897)
49. Selcuklu, S. D., Donoghue, M. T., and Spillane, C. (2009) miR-21 as a key regulator of oncogenic processes. Biochem. Soc. Trans. 37, 918-925
50. Volinia, S., Calin, G. A., Liu, C. G., Ambs, S., Cimmino, A., Petrocca, F., Visone, R., Iorio, M., Roldo, C., Ferracin, M., Prueitt, R. L., Yanaihara, N., Lanza, G., Scarpa, A., Vecchione, A., Negrini, M., Harris, C. C., and Croce, C. M. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. U.S.A. 103, 2257-2261 (Pubitemid 43271657)
51. Si, M. L., Zhu, S., Wu, H., Lu, Z., Wu, F., and Mo, Y. Y. (2007) miR-21- mediated tumor growth. Oncogene 26, 2799-2803
52. Moreira, F., Kiehl, T. R., So, K., Ajeawung, N. F., Honculada, C., Gould, P., Pieper, R. O., and Kamnasaran, D. (2011) NPAS3 demonstrates features of a tumor suppressive role in driving the progression of astrocytomas. Am. J. Pathol. 179, 462-476
53. Hayashi, T., Koyama, N., Azuma, Y., and Kashimata, M. (2011) Mesenchymal miR-21 regulates branching morphogenesis in murine submandibular gland in vitro. Dev. Biol. 352, 299-307
54. Pasquale, E. B. (2010) Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat. Rev. Cancer 10, 165-180
55. Frankel, L. B., Christoffersen, N. R., Jacobsen, A., Lindow, M., Krogh, A., and Lund, A. H. (2008) Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 283, 1026-1033
56. + T cells by directly and indirectly targeting DNA methyltransferase 1. J. Immunol. 184, 6773-6781
57. Adams, B. D., Furneaux, H., and White, B. A. (2007) The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-α (ERα) and represses ERα messenger RNA and protein expression in breast cancer cell lines. Mol. Endocrinol. 21, 1132-1147 (Pubitemid 46984764)
58. Yokoe, S., Takahashi, M., Asahi, M., Lee, S. H., Li, W., Osumi, D., Miyoshi, E., and Taniguchi, N. (2007) The Asn418-linkedN-glycan of ErbB3 plays a crucial role in preventing spontaneous heterodimerization and tumor promotion. Cancer Res. 67, 1935-1942 (Pubitemid 46424209)
59. Guo, H. B., Johnson, H., Randolph, M., Lee, I., and Pierce, M. (2009) Knockdown of GnT-Va expression inhibits ligand-induced downregulation of the epidermal growth factor receptor and intracellular signaling by inhibiting receptor endocytosis. Glycobiology 19, 547-559