HMG-I(Y) recognizes base-unpairing regions of matrix attachment sequences and its increased expression is directly linked to metastatic breast cancer phenotype

Cancer Research

Volumn 59, Issue 22, 1999, Pages 5695-5703

  Lui, Wen Man ^a   Guerra Vladusic, Fabiana K ^a   Kurakata, Shinichi ^b   Lupu, Ruth ^a   Kohwi Shigematsu, Terumi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DAIICHI SANKYO CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; GELATINASE B; HIGH MOBILITY GROUP PROTEIN; NEU DIFFERENTIATION FACTOR;

ARTICLE; BASE PAIRING; BINDING AFFINITY; BREAST CANCER; BREAST CARCINOMA; CANCER INVASION; CONTROLLED STUDY; DNA TRANSFECTION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; METASTASIS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANTISENSE ELEMENTS (GENETICS); BLOTTING, SOUTHERN; BLOTTING, WESTERN; BREAST NEOPLASMS; DNA-BINDING PROTEINS; ESTROGENS; FEMALE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HIGH MOBILITY GROUP PROTEINS; HMGA1A PROTEIN; HUMANS; MATRIX METALLOPROTEINASE 9; MOLECULAR WEIGHT; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEUREGULIN-1; PHENOTYPE; RIBONUCLEOPROTEINS; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0344374435     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (88)

1. Mirkovitch, J., Mirault, M-E., and Laemmli, U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell, 9: 223-232, 1984.
2. Cockerill, P. N., and Garrard, W. T. Chromosomal loop anchorage of the κ immunoglobulin gene occurs next to the enhancer in a region containing topoisomerases II sites. Cell, 44: 273-282, 1986.
3. Gasser, S. M., and Laemmli, U. K. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell, 46: 521-530, 1986.
4. Gasser, S. M., and Laemmli, U. K. The organization of chromatin loops: characterization of a scaffold. EMBO J., 5: 511-518, 1986.
5. Cockerill, P. N., Yuen, M-H., and Garrard, W. T. The enhancer of the immunoglobulin heavy chain locus is flanked by presumptive chromosomal loop anchorage elements. J Biol. Chem., 202: 5394-5397, 1987.
6. Gasser, S. M., and Laemmli, U. K. A glimpse at chromosomal order. Trends Genet., 3: 16-22, 1987.
7. Forrester, W. C., van Genderen, C., Jenuwein, T., and Grosschedl, R. Dependence of enhancer-mediated transcription of the immunoglobulin μ gene on nuclear matrix attachment regions. Science (Washington DC), 265: 1221-1225, 1994.
8. Kirillov, A., Kistler, B., Mostsolasky, R., Cedar, H., Wirth, T., and Bergman, Y. A role for nuclear NF-κB-cell-specific demethylation of the Igk locus. Nat. Genet., 13: 435-441, 1996.
9. Jenuwein, T., Foresster, W. C., Fernandez-Herrero, L. A., Laible, G., Dull, M., and Grosschedl, R. Extension of chromatin accessibility by nuclear matrix attachment regions. Nature (Lond.), 385: 269-272, 1997.
10. Kohwi-Shigematsu, T., and Kohwi, Y. Torsional stress stabilizes extended base unpairing in suppressor sites flanking immunoglobulin heavy chain enhancer. Biochemistry, 29: 9551-9560, 1990.
11. Bode, J., Kohwi, Y., Dickinson, L. A., Joh, T., Klehr, D., Mielke, C., and Kohwi-Shigematsu, T. Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science (Washington DC), 255: 195-197, 1992.
12. Kohwi-Shigematsu, T., and Kohwi, Y. High unwinding capability of matrix attachment regions and ATC-sequence context-specific MAR-binding proteins. In: R. C. Bird (ed.), Nuclear Structure and Gene Expression, pp. 111-144. San Diego, CA: Academic Press, 1997.
13. Dickinson, L. A., Joh, T., Kohwi, Y., and Kohwi-Shigematsu, T. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell, 70: 631-645, 1992.
14. Herrscher, R. F., Kaplan, M. H., Lelsz, D. L., Das, C., Scheuermann, R., and Tucker, P. W. The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trana-activator that describes a new DNA-binding protein family. Genes Dev., 9: 3067-3082, 1995.
15. de Belle, I., Cai, S., and Kohwi-Shigematsu, T. The genomic sequences bound to special AT-rich sequence-binding protein 1 (SATB1) in vivo in Jurkat T cells are tightly associated with the nuclear matrix at the bases of the chromatin loops. J. Cell Biol., 141: 335-348, 1998.
16. Dickinson, L. A., and Kohwi-Shigematsu, T. Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-unpairing potential. Mol. Cell. Biol., 15: 456-465, 1995.
17. Will, K., Warnecke, G., Wiesmuller, L., and Deppert. W. Specific interaction of mutant p53 with regions of matrix attachment region DNA elements (MARs) with a high potential for base-unpairing. Proc. Natl. Acad. Sci. USA. 95: 13681-13686, 1998.
18. Yanagisawa, J., Ando, J., Nakayama, J., Kohwi, Y., and Kohwi-Shigematsu, T. A matrix attachment region (MAR)-binding activity due to a p114 kilodalton protein is found only in human breast carcinomas and not in normal and benign breast disease tissues. Cancer Res., 56: 457-462, 1996.
19. Johnson, K. R., Lehn, D. A., and Reeves, R. Alternative processing of mRNA encoding mammalian chromosomal high-mobility-group proteins HMG-I and HMG-Y. Mol. Cell. Biol., 9: 2114-2123, 1989.
20. Zhao, K., Kas, E., Gonzalez, E., and Laemmli, U. K. SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J., 12: 3237-3247, 1993.
21. Wunderlich, V., and Bottger, M. High-mobility-group proteins and cancer - an emerging link. J. Cancer Res. Clin. Oncol., 123: 133-140, 1997.
22. Lund, T., Holtlund, J., Fredriksen, M., and Laland, S. G. On the presence of two new high mobility group-like proteins in HeLa S3 cells. FEBS Lett., 152: 163-167, 1983.
23. Giancotti, V., Berlingieri, M. T., Di Fiore, P. P., Fusco, A., Vecchio, G., and Crane-Robinson, C. Changes in nuclear proteins on transformation of rat epithelial thyroid cells by a murine sacroma retrovirus. Cancer Res., 45: 6051-6057, 1985.
24. Giancotti, V., Pani, B., D'Andrea, P., Berlingieri, M. T., Di Fiore, P. P., Fusco, A., Vecchio, G., Philp, R., Crane-Robinson, C., Nicolas, R. H., Wright, C. A., and Goodwin, G. H. Elevated levels of a specific class of nuclear phosphoproteins in cells transformed with v-ras and v-mos oncogenes and by co-transfection with c-myc and polyoma middle T genes. EMBO J., 6: 1981-1987, 1987.
25. Giancotti, V., Buratti, E., Perissin, L., Zorzet, S., Balmain, A., Portella, G., Fusco., A., and Goodwin, G. H. Analysis of the HMGI nuclear proteins in mouse neoplastic cells induced by different procedures. Exp. Cell Res., 184: 538-545, 1989.
26. Bussemakers, M. J. G., van de Ven, W. J. M., Debruyne, F. M. J., and Schalken, J. A. Identification of high mobility group protein I(Y) as potential progression marker for prostate cancer by differential hybridization analysis. Cancer Res., 51: 606-611, 1991.
27. Ram T. G., Reeves, R., and Hosick, H. L. Elevated high mobility group-I(Y) gene expression is associated with progressive transformation of mouse mammary epithelial cells. Cancer Res., 53: 2655-2660, 1993.
28. Cmarik, J. L., Li, Y., Ogram, S. A., Min, H., Reeves, R., and Colbum, N. H. Tumor promoter induces high mobility group HMG-Y protein expression in transformation-sensitive but not -resistant cells. Oncogene, 16: 3387-3396, 1998.
29. Berlingieri, M. T., Manfioletti, G., Santoro, M., Bandiera, A., Visconti, R., Giancotti, V., and Fusco, A. Identification of HMG-I-C protein synthesis suppresses retrovirally induced neoplastic transformation of rat thyroid cells. Mol. Cell. Biol., 15: 1545-1553, 1995.
30. Chiappetta, G., Tallini, G., De Biasio, M. C., Manfioletti, G., Martinez-Tello, F. J., Pentimalli, F., de Nigris, F., Mastio, A., Botti, G., Fedele, M., Berger, N., Santoro, M., Giancotti, V., and Fusco, A. Detection of high mobility group I HMGI(Y) protein in the diagnosis of thyroid tumors: HMGI(Y) expression represents a potential diagnostic indicator of carcinoma. Cancer Res., 58: 4193-4198, 1998.
31. Tamimi, Y., van der Poel, H. G., Denyn, M-M., Umbas, R., Karthaus, H. F. M., Debruyne, F. M. J., and Schalken, J. A. Increased expression of high mobility group protein I(Y) in high grade prostatic cancer determined by in situ hybridization. Cancer Res., 53: 5512-5516, 1993.
32. Tamimi, Y., van der Poel, H. G., Karthaus, H. F. M., Debruyne, F. M., and Schalken, J. A. A retrospective study of high mobility group protein I(Y) as progression marker for prostate cancer determined by in situ hybridization. Br. J. Cancer, 74: 573-578, 1996.
33. Fedele, M., Bandiera, A., Chiappetta, G., Battista, S., Vigletto, G., Manfioletti, G., Gasamassimi, A., Santoro, M., Giancotti, V., and Fusco, A. Human colorectal carcinomas express high levels of high mobility group HMGI(Y) proteins. Cancer Res., 56: 1896-1901, 1996.
34. Williams, A. J., Powell, W. L., Collins, T., and Morion C. C. HMGI(Y) expression in human uterine leiomyomata. Am. J. Pathol., 150: 911-918, 1997.
35. Bandiera, A., Bonifacio, D., Manfioletti, G., Mantovani, F., Rustighi, A., Zanconati, F., Fusco, A., Bonito, L. D., and Giancotti, V. Expression of HMGI(Y) proteins in squamous intraepithelial and invasive lesions of the uterine cervix. Cancer Res., 58: 426-431, 1998.
36. Slamon, D. J., Clark, G. M., Wong, S. G., Levin, W. J., Ullrich, A., and McGuire, W. L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science (Washington DC), 235: 177-182, 1987.
37. Slamon, D. J., Godolphin, W., Jones, L. A., Holt, J. A., Wong, S. G., Keith, D. E., Levin, W. J., Stuart, S. G., Udove, J., and Ullrich, A. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science (Washington DC), 244: 707-712, 1989.
38. Harris, J. R., Lippman, M. E., Veronesi, U., and Willett, W. Breast cancer (3). N. Engl. J. Med., 327: 473-480, 1992.
39. Dougall, W. C., Qian, X., Peterson, N. C., Millet, M. J., Samanta, A., and Greene, M. I. The neu-oncogene: signal transduction pathways, transformation mechanisms and evolving therapies. Oncogene, 9: 2109-2123, 1994.
40. Klijn, J. G., Berns, P. M., Schmitz, P. I., and Foekens, J. A. The clinical significance of epidermal growth factor receptor (EGF-R) in human breast cancer: a review on 5232 patients. Endocr. Rev., 13: 3-17, 1992.
41. Holth, L. T., Thorlacius, A. E., and Reeves, R. Effects of epidermal growth factor and estrogen on the regulation of the HMG-I/Y gene in human mammary epithelial cell lines. DNA Cell Biol., 16: 1299-1309, 1997.
42. van de Vijver, M. J., Peterse, J. L., Mooi, W. J., Wisman, P., Lomans, J., Dalesio, O., and Nusse, R. Neu-protein overexpression in breast cancer. Association with comedo-type ductal carcinoma in situ and limited prognostic value in stage II breast cancer. N. Engl. J. Med., 319: 1239-1245, 1988.
43. Lacroix, H., Iglehart, J. D., Skinner, M. A., and Kraus, M. H. Overexpression of erbB-2 or EGF receptor proteins present in early stage mammary carcinoma is detected simultaneously in matched primary tumors and regional metastases. Oncogene, 4: 145-151, 1989.
44. de Potter, C. R., Beghin, C., Makar, A. P., Vandekerckhove, D., and Roels, H. J. The neu-oncogene protein as a predictive factor for haematogenous metastases in breast cancer patients. Int. J. Cancer, 45: 55-58, 1990.
45. Paik, S., Hazan, R., Fisher, E. R., Sass, R. E., Fisher, B., Redmond, C., Schlessinger, J., Lippman, M. E., and King, C. R. Pathologic findings from the National Surgical Adjuvant Breast and Bowel Project: prognostic significance of erbB-2 protein overexpression in primary breast cancer. 3. Clin. Oncol., 8: 103-112, 1990.
46. Allred, D. C., Clark, G. M., Molina, R., Tandon, A. K., Schnitt, S. J., Gilchrist, K. W., Osborne, C. K., Tormey, D. C., and McGuire, W. L. Overexpression of HER-2/neu and its relationship with other prognostic factors change during the progression of in situ to invasive breast cancer. Hum. Pathol., 23: 974-979, 1992.
47. Gusterson, B. A., Gelber, R. D., Goldhirsch, A., Price, K. N., Säve-Söderborgh, J., Anbazhagan, R., Styles, J., Rudenstam, C. M., Golouh, R., and Reed, R. Prognostic importance of c-erbB-2 expression in breast cancer. International (Ludwig) Breast Cancer Study Group. J. Clin. Oncol., 10: 1049-1056, 1992.
48. Toikkanen, S., Helin, H., Isola, J., and Joensuu, H. Prognostic significance of HER-2 oncoprotein expression in breast cancer: a 30-year follow-up. J. Clin. Oncol., 10: 1044-1048, 1992.
49. erbB-2. Science (Washington DC), 249: 1552-1555, 1990.
50. Staebler, A., Sommers, C., Mueller, S. C., Byers, S., Thompson, E. W., and Lupu, R. Modulation of breast cancer progression and differentiation by the gp30/heregulin. Breast Cancer Res. Treat., 31: 175-182, 1994.
51. erbB-2. Science (Washington DC), 256: 1206-1210, 1992.
52. Peles, E., Bacus, S. S., Koski, R. A., Lu, H. S., Wen, D., Ogden, S. G., Levy, R. B., and Yarden, Y. Isolation of the Neu/HER-2 stimulatory ligand: a 44 kDa glycoprotein that induces differentiation of mammary tumor cells. Cell, 69: 205-216, 1992.
53. Tang, C., Perez, C., Grunt, T., Waibel, C., Cho, C., and Lupu, R. Involvement of heregulin-β2 in the acquisition of the hormone-independent phenotype of breast cancer cells. Cancer Res., 56: 3350-3358, 1996.
54. Azzam, H. S., Arand, G., Lippman, M. E., and Thompson, E. W. Association of MMP-2 activation potential with metastatic progression in human breast cancer cell lines independent of MMP-2 production. J. Natl. Cancer. Inst., 85: 1758-1764, 1993.
55. r 92,000 type IV collagenase is increased in plasma of patients with colon cancer and breast cancer. Cancer Res., 53: 140-146, 1993.
56. Hua, J., and Muschel, R. J. Inhibition of matrix metalloproteinase 9 expression by a ribozyme blocks metastasis in a rat sarcoma model system. Cancer Res., 56: 5279-5284, 1996.
57. Thompson, E. W., Katz, D., Shima, T. B., Wakeling, A. E., Lippman, M. E., and Dickson, R. B. ICI 164,384, a pure antagonist of estrogen-stimulated MCF-7 cell proliferation and invasiveness. Cancer Res., 49: 6929-6934, 1989.
58. Dickinson, L. A., Dickinson, C. D., and Kohwi-Shigematsu, T. An atypical homeodomain in SATB1 promotes specific recognition of the key structural element in a matrix attachment region. J. Biol. Chem., 272: 11463-11470, 1997.
59. Lupu, R., Dickson, R. B., and Lippman, M. E. The role of erbB-2 and its ligands in growth control of malignant breast epithelium. J. Steroid Biochem. Mol. Biol., 43: 229-236, 1992.
60. Lupu, R., Cardillo, M., Cho, C., Harris, L., Hijazi, M., Perez, C., Rosenberg, K., Yang, D., and Tang, C. The significance of heregulin in breast cancer tumor progression and drug resistance. Breast Cancer Res. Treat., 38: 57-66, 1996.
61. Johnson, K. R., Disney, J. E., Wyatt, C. R., and Reeves, R. Expression of mRNAs encoding mammalian chromosomal proteins HMG-I and HMG-Y during cellular proliferation. Exp. Cell Res., 187: 69-76, 1990.
62. Russnak, R. H., Candido, E. P. M., and Astell, C. R. Interaction of the mouse chromosomal protein HMG-I with the 3′ ends of genes in vitro. J. Biol. Chem., 263: 6392-6399, 1988.
63. Pratt, S. E., and Pollak, M. N. Estrogen and antiestrogen modulation of MCF-7 human breast cancer cell proliferation is associated with specific alterations in accumulation of insulin-like growth factor-binding proteins in conditioned media. Cancer Res., 53: 5193-5198, 1993.
64. Cardillo, M., Tang, C. K., and Lupu, R. Heregulin induces a metastatic phenotype to breast cancer cells in vivo. Proc. Am. Assoc. Cancer Res., 36: 262, 1995.
65. Tamaki, K., Tanzawa, K., Kurihara, S., Oikawa, T., Monma, S., Shimada, K., and Sugimura, Y. Synthesis and structure-activity relationships of gelatinase inhibitors derived from matlystatins. Chem. Pharm. Bull. (Tokyo), 43: 1883-1893, 1995.
66. Reeves, R., and Nissen, M. S. The A-T-DNA-binding domain of mammalian high mobility group 1 chromosomal proteins. J. Biol. Chem., 265: 8573-8582, 1990.
67. Wegner, M., and Grummt, F. Netropsin, distamycin and berenil interact differentially with a high-affinity binding site for the high mobility group protein HMG-I. Biochem. Biophys. Res. Commun., 166: 1110-1117, 1990.
68. Maher, J. F., and Nathans, D. Multivalent DNA-binding properties of the HMG-I proteins. Proc. Natl. Acad. Sci. USA, 93: 6716-6720, 1996.
69. Vu, T. H., and Werb, Z. Gelatinase B: structure, regulation, and function. In: W. C. Parks and R. P. Mecham (eds.), Matrix Metalloproteinases, pp. 115-148. San Diego, CA: Academic Press, 1998.
70. Martin, D. C., Rüther, U., Sanchez-Sweatman, O. H., Orr, F. W., and Khokha, R. Inhibition of SV40 T antigen-induced hepatocellular carcinoma in TIMP-1 transgenic mice. Oncogene, 13: 569-576, 1996.
71. Wilson, C. L., Heppner, K. J., Labosky, P. A., Hogan, B. L., and Matrisian, L. M. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc. Natl. Acad. Sci. USA., 94: 1402-1407, 1997.
72. Ogram, S. A., and Reeves, R. Differential regulation of a multipromoter gene. J. Biol. Chem., 270: 14235-14242, 1995.
73. Friedmann, M., Holth, L. T., Zoghbi, H. Y., and Reeves, R. Organization, inducible-expression and chromosome localization of the human HMG-I(Y) nonhistone protein gene. Nucleic Acids Res., 21: 4259-4267, 1993.
74. Kinoshita, T., Shirasawa, H., Shino, Y., Shimizu, K., Moriya, H., and Simizu, B. Human papillomavirus type 16 E6 protein up-regulates the expression of the high mobility group protein HMG-I(Y) gene in mouse 10T1/2 cells. Virus Res., 42: 119-125, 1996.
75. Strauss, F., and Varshavsky, A. A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome. Cell, 37: 889-901, 1984.
76. Reeves, R., Elton, T. S., Nissen, M. S., Lehn, D., and Johnson, K. R. Posttranscriptional gene regulation and specific binding of the nonhistone protein HMG-I by the 3′ untranslated region of bovine interleukin 2 cDNA. Proc. Natl. Acad. Sci. USA, 84: 6531-6535, 1987.
77. Wegner, M., Helftenbein, E., Muller, F., Meinecke, M., Muller, S., and Grummt, F. Identification of an amplification promoting DNA sequence from the hypotrichous ciliate Stylonychis lemnae. Nucleic Acids Res., 17: 8783-8802, 1989.
78. Wolffe, A. P. Architectural transcription factors. Science (Washington DC), 264: 1100-1101, 1994.
79. Grosschedl, R. Higher-order nucleoprotein complexes in transcription: analogies with site-specific recombination. Curr. Opin. Cell Biol., 7: 362-370, 1995.
80. Bustin, M., and Reeves, R. High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol., 54: 35-100, 1996.
81. Bagga, R., and Emerson, B. M. An HMG-I/Y-containing repressor complex and supercoiled DNA topology are critical for long-range enhancer-dependent transcription in vitro. Genes Dev., 11: 629-639, 1997.
82. Chin, M. T., Pellacani, A., Wang, H., Lin, S. S. J., Jain, M. K., Perrella, M. A., and Lee, M-E. Enhancement of serum-response factor-dependent transcription and DNA binding by the architectural transcription factor HMG-I(Y). J. Biol. Chem., 273: 9755-9760, 1998.
83. Bonnefoy, E., Bandu, M-T., and Doly, J. Specific binding of high-mobility-group I (HMGI) protein and histone H1 to the upstream AT-rich region of the murine β interferon promoter: HMGI protein acts as a potential antirepressor of the promoter. Mol. Cell. Biol., 19: 2803-2816, 1999.
84. Chase, M. B., Haga, S. B., Hankins, W. D., Williams, D. M., Bi, Z., Strovel, J. W., Obriecht, C., and Berg, P. E. Binding of HMG-I(Y) elicits structural changes in a silencer of the human β-globin gene. Am. J. Hematol., 60: 27-35, 1999.
85. Grummt, F., Hoist, A., Muller, F., Wegner, M., Schwender, S., Luksza, H., Zastrow, G., and Klavinius, A. Mouse ARS elements and ARS-binding proteins. Cancer Cells (Cold Spring Harbor), 6: 463-466, 1988.
86. Disney, J. E., Johnson, K. R., Magnuson, N. S., Sylvester, S. R., and Reeves, R. High-mobility group protein HMG-I localizes to G/Q- and C-bands of human and mouse chromosomes. J. Cell Biol., 109: 1975-1982, 1989.
87. Amirand, C., Viari, A., Ballini, J. P., Rezaei, H., Beaujean, N., Jullien, D., Käs, E., and Debey, P. Three distinct sub-nuclear populations of HMG-I protein of different properties revealed by co-localization image analysis. J. Cell Sci., III: 3551-3561, 1998.
88. Nelson, W. G., Pienta, K. J., Barrack, E. R., and Coffey, D. S. The role of the nuclear matrix in the organization and function of DNA. Annu. Rev. Biophys. Biophys Chem., 15: 457-475, 1986.