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Article

Parvin-β Inhibits Breast Cancer Tumorigenicity and Promotes CDK9-Mediated Peroxisome Proliferator-Activated Receptor Gamma 1 Phosphorylation

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Pages 687-704 | Received 29 Aug 2006, Accepted 27 Oct 2007, Published online: 27 Mar 2023

REFERENCES

  • Adams, M., M. J. Reginato, D. Shao, M. A. Lazar, and V. K. Chatterjee. 1997. Transcriptional activation by peroxisome proliferator-activated receptor gamma is inhibited by phosphorylation at a consensus mitogen-activated protein kinase site. J. Biol. Chem. 272:5128–5132.
  • Akira, S., H. Isshiki, T. Sugita, O. Tanabe, S. Kinoshita, Y. Nishio, T. Nakajima, T. Hirano, and T. Kishimoto. 1990. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9:1897–1906.
  • Biggs, J., E. V. Murphy, and M. A. Israel. 1992. A human Id-like helix-loop-helix protein expressed during early development. Proc. Natl. Acad. Sci. USA 89:1512–1516.
  • Camp, H. S., and S. R. Tafuri. 1997. Regulation of peroxisome proliferator-activated receptor gamma activity by mitogen-activated protein kinase. J. Biol. Chem. 272:10811–10816.
  • Camp, H. S., S. R. Tafuri, and T. Leff. 1999. c-Jun N-terminal kinase phosphorylates peroxisome proliferator-activated receptor-gamma 1 and negatively regulates its transcriptional activity. Endocrinology 140:392–397.
  • Castells, A., Y. Ino, D. N. Louis, V. Ramesh, J. F. Gusella, and A. K. Rustgi. 1999. Mapping of a target region of allelic loss to a 0.5-cM interval on chromosome 22q13 in human colorectal cancer. Gastroenterology 117:831–837.
  • Castells, A., J. F. Gusella, V. Ramesh, and A. K. Rustgi. 2000. A region of deletion on chromosome 22q13 is common to human breast and colorectal cancers. Cancer Res. 60:2836–2839.
  • Castellvi-Bel, S., A. Castells, C. N. Johnstone, V. Pinol, M. Pellise, J. I. Elizalde, N. Romo, A. K. Rustgi, and J. M. Pique. 2003. Evaluation of PARVG located on 22q13 as a candidate tumor suppressor gene for colorectal and breast cancer. Cancer Genet. Cytogenet. 144:80–82.
  • Chawla, A., E. J. Schwarz, D. D. Dimaculangan, and M. A. Lazar. 1994. Peroxisome proliferator-activated receptor (PPAR) gamma: adipose-predominant expression and induction early in adipocyte differentiation. Endocrinology 135:798–800.
  • Chinetti, G., S. Lestavel, V. Bocher, A. T. Remaley, B. Neve, I. P. Torra, E. Teissier, A. Minnich, M. Jaye, N. Duverger, H. B. Brewer, J. C. Fruchart, V. Clavey, and B. Staels. 2001. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat. Med. 7:53–58.
  • Cui, Y., K. Miyoshi, E. Claudio, U. K. Siebenlist, F. J. Gonzalez, J. Flaws, K. U. Wagner, and L. Hennighausen. 2002. Loss of the peroxisome proliferation-activated receptor gamma (PPARgamma) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J. Biol. Chem. 277:17830–17835.
  • Dang, D. T., J. Pevsner, and V. W. Yang. 2000. The biology of the mammalian Kruppel-like family of transcription factors. Int. J. Biochem. Cell Biol. 32:1103–1121.
  • Delcommenne, M., C. Tan, V. Gray, L. Rue, J. Woodgett, and S. Dedhar. 1998. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Natl. Acad. Sci. USA 95:11211–11216.
  • Deramaudt, T. B., M. Takaoka, R. Upadhyay, M. J. Bowser, J. Porter, A. Lee, B. Rhoades, C. N. Johnstone, R. Weissleder, S. R. Hingorani, U. Mahmood, and A. K. Rustgi. 2006. N-cadherin and keratinocyte growth factor receptor mediate the functional interplay between Ki-RASG12V and p53V143A in promoting pancreatic cell migration, invasion, and tissue architecture disruption. Mol. Cell. Biol. 26:4185–4200.
  • Drori, S., G. D. Girnun, L. Tou, J. D. Szwaya, E. Mueller, K. Xia, R. A. Shivdasani, and B. M. Spiegelman. 2005. Hic-5 regulates an epithelial program mediated by PPARgamma. Genes Dev. 19:362–375.
  • Grigoriadis, A., A. Mackay, J. S. Reis-Filho, D. Steele, C. Iseli, B. J. Stevenson, C. V. Jongeneel, H. Valgeirsson, K. Fenwick, M. Iravani, M. Leao, A. J. Simpson, R. L. Strausberg, P. S. Jat, A. Ashworth, A. M. Neville, and M. J. O'Hare. 2006. Establishment of the epithelial-specific transcriptome of normal and malignant human breast cells based on mpss and array expression data. Breast Cancer Res. 8:R56.
  • Guan, H. P., T. Ishizuka, P. C. Chui, M. Lehrke, and M. A. Lazar. 2005. Corepressors selectively control the transcriptional activity of PPARgamma in adipocytes. Genes Dev. 19:453–461.
  • Hannigan, G., A. A. Troussard, and S. Dedhar. 2005. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat. Rev. Cancer 5:51–63.
  • Hannigan, G. E., C. Leung-Hagesteijn, L. Fitz-Gibbon, M. G. Coppolino, G. Radeva, J. Filmus, J. C. Bell, and S. Dedhar. 1996. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379:91–96.
  • Heid, H. W., M. Schnolzer, and T. W. Keenan. 1996. Adipocyte differentiation-related protein is secreted into milk as a constituent of milk lipid globule membrane. Biochem. J. 320:1025–1030.
  • Hu, E., J. B. Kim, P. Sarraf, and B. M. Spiegelman. 1996. Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARgamma. Science 274:2100–2103.
  • Iankova, I., R. K. Petersen, J. S. Annicotte, C. Chavey, J. B. Hansen, I. Kratchmarova, D. Sarruf, M. Benkirane, K. Kristiansen, and L. Fajas. 2006. Peroxisome proliferator-activated receptor gamma recruits the positive transcription elongation factor b complex to activate transcription and promote adipogenesis. Mol. Endocrinol. 20:1494–1505.
  • Itahana, Y., J. Singh, T. Sumida, J. P. Coppe, S. Parrinello, J. L. Bennington, and P. Y. Desprez. 2003. Role of Id-2 in the maintenance of a differentiated and noninvasive phenotype in breast cancer cells. Cancer Res. 63:7098–7105.
  • Johnson, K. R., J. L. Leight, and V. M. Weaver. 2007. Demystifying the effects of a three-dimensional microenvironment in tissue morphogenesis. Methods Cell Biol. 83:547–583.
  • Johnstone, C. N., N. C. Tebbutt, H. E. Abud, S. J. White, K. L. Stenvers, N. E. Hall, S. H. Cody, R. H. Whitehead, B. Catimel, E. C. Nice, A. W. Burgess, and J. K. Heath. 2000. Characterization of mouse A33 antigen, a definitive marker for basolateral surfaces of intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279:G500–G510.
  • Johnstone, C. N., S. J. White, N. C. Tebbutt, F. J. Clay, M. Ernst, W. H. Biggs, C. S. Viars, S. Czekay, K. C. Arden, and J. K. Heath. 2002. Analysis of the regulation of the A33 antigen gene reveals intestine-specific mechanisms of gene expression. J. Biol. Chem. 277:34531–34539.
  • Johnstone, C. N., S. Castellvi-Bel, L. M. Chang, X. Bessa, H. Nakagawa, H. Harada, R. K. Sung, J. M. Pique, A. Castells, and A. K. Rustgi. 2004. ARHGAP8 is a novel member of the RHOGAP family related to ARHGAP1/CDC42GAP/p50RHOGAP: mutation and expression analyses in colorectal and breast cancers. Gene 336:59–71.
  • Kass, L., J. T. Erler, M. Dembo, and V. M. Weaver. 2007. Mammary epithelial cell: influence of extracellular matrix composition and organization during development and tumorigenesis. Int. J. Biochem. Cell Biol. 39:1987–1994.
  • Kleinman, H. K., and G. R. Martin. 2005. Matrigel: basement membrane matrix with biological activity. Semin. Cancer Biol. 15:378–386.
  • Korenbaum, E., T. M. Olski, and A. A. Noegel. 2001. Genomic organization and expression profile of the parvin family of focal adhesion proteins in mice and humans. Gene 279:69–79.
  • Krey, G., H. Keller, A. Mahfoudi, J. Medin, K. Ozato, C. Dreyer, and W. Wahli. 1993. Xenopus peroxisome proliferator activated receptors: genomic organization, response element recognition, heterodimer formation with retinoid X receptor and activation by fatty acids. J. Steroid Biochem. Mol. Biol. 47:65–73.
  • Legate, K. R., E. Montanez, O. Kudlacek, and R. Fassler. 2006. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7:20–31.
  • Lehmann, J. M., L. B. Moore, T. A. Smith-Oliver, W. O. Wilkison, T. M. Willson, and S. A. Kliewer. 1995. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J. Biol. Chem. 270:12953–12956.
  • Lehrke, M., and M. A. Lazar. 2005. The many faces of PPARgamma. Cell 123:993–999.
  • Li, X., B. Monks, Q. Ge, and M. J. Birnbaum. 2007. Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature 447:1012–1016.
  • Majello, B., G. Napolitano, A. Giordano, and L. Lania. 1999. Transcriptional regulation by targeted recruitment of cyclin-dependent CDK9 kinase in vivo. Oncogene 18:4598–4605.
  • Mancebo, H. S., G. Lee, J. Flygare, J. Tomassini, P. Luu, Y. Zhu, J. Peng, C. Blau, D. Hazuda, D. Price, and O. Flores. 1997. P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. 11:2633–2644.
  • Marchesan, D., M. Rutberg, L. Andersson, L. Asp, T. Larsson, J. Boren, B. R. Johansson, and S. O. Olofsson. 2003. A phospholipase D-dependent process forms lipid droplets containing caveolin, adipocyte differentiation-related protein, and vimentin in a cell-free system. J. Biol. Chem. 278:27293–27300.
  • Marshall, N. F., and D. H. Price. 1995. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J. Biol. Chem. 270:12335–12338.
  • Meggio, F., D. Shugar, and L. A. Pinna. 1990. Ribofuranosyl-benzimidazole derivatives as inhibitors of casein kinase-2 and casein kinase-1. Eur. J. Biochem. 187:89–94.
  • Mishima, W., A. Suzuki, S. Yamaji, R. Yoshimi, A. Ueda, T. Kaneko, J. Tanaka, Y. Miwa, S. Ohno, and Y. Ishigatsubo. 2004. The first CH domain of affixin activates Cdc42 and Rac1 through alphaPIX, a Cdc42/Rac1-specific guanine nucleotide exchanging factor. Genes Cells 9:193–204.
  • Miyoshi, K., B. Meyer, P. Gruss, Y. Cui, J. P. Renou, F. V. Morgan, G. H. Smith, M. Reichenstein, M. Shani, L. Hennighausen, and G. W. Robinson. 2002. Mammary epithelial cells are not able to undergo pregnancy-dependent differentiation in the absence of the helix-loop-helix inhibitor Id2. Mol. Endocrinol. 16:2892–2901.
  • Mongroo, P. S., C. N. Johnstone, I. Naruszewicz, C. Leung-Hagesteijn, R. K. Sung, L. Carnio, A. K. Rustgi, and G. E. Hannigan. 2004. Beta-parvin inhibits integrin-linked kinase signaling and is downregulated in breast cancer. Oncogene 23:8959–8970.
  • Moore, K. J., E. D. Rosen, M. L. Fitzgerald, F. Randow, L. P. Andersson, D. Altshuler, D. S. Milstone, R. M. Mortensen, B. M. Spiegelman, and M. W. Freeman. 2001. The role of PPAR-gamma in macrophage differentiation and cholesterol uptake. Nat. Med. 7:41–47.
  • Morgenstern, J. P., and H. Land. 1990. A series of mammalian expression vectors and characterisation of their expression of a reporter gene in stably and transiently transfected cells. Nucleic Acids Res. 18:1068.
  • Mori, S., S. I. Nishikawa, and Y. Yokota. 2000. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO J. 19:5772–5781.
  • Mueller, E., P. Sarraf, P. Tontonoz, R. M. Evans, K. J. Martin, M. Zhang, C. Fletcher, S. Singer, and B. M. Spiegelman. 1998. Terminal differentiation of human breast cancer through PPAR gamma. Mol. Cell 1:465–470.
  • Nikolopoulos, S. N., and C. E. Turner. 2000. Actopaxin, a new focal adhesion protein that binds paxillin LD motifs and actin and regulates cell adhesion. J. Cell Biol. 151:1435–1448.
  • Nikolopoulos, S. N., and C. E. Turner. 2001. Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J. Biol. Chem. 276:23499–23505.
  • O'Brien, L. E., W. Yu, K. Tang, T. S. Jou, M. M. Zegers, and K. E. Mostov. 2006. Morphological and biochemical analysis of Rac1 in three-dimensional epithelial cell cultures. Methods Enzymol. 406:676–691.
  • Olski, T. M., A. A. Noegel, and E. Korenbaum. 2001. Parvin, a 42 kDa focal adhesion protein, related to the alpha-actinin superfamily. J. Cell Sci. 114:525–538.
  • Papadaki, I., E. Mylona, I. Giannopoulou, S. Markaki, A. Keramopoulos, and L. Nakopoulou. 2005. PPARgamma expression in breast cancer: clinical value and correlation with ERbeta. Histopathology 46:37–42.
  • Paszek, M. J., N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, and V. M. Weaver. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241–254.
  • Petersen, O. W., L. Ronnov-Jessen, A. R. Howlett, and M. J. Bissell. 1992. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc. Natl. Acad. Sci. USA 89:9064–9068.
  • Rosenberger, G., I. Jantke, A. Gal, and K. Kutsche. 2003. Interaction of alphaPIX (ARHGEF6) with beta-parvin (PARVB) suggests an involvement of alphaPIX in integrin-mediated signaling. Hum. Mol. Genet. 12:155–167.
  • Sekido, R., K. Murai, J.-I. Funahashi, Y. Kamachi, A. Fujisawa-Sehara, Y.-I. Nabeshima, and H. Kondoh. 1994. The δ-crystallin enhancer-binding protein δEF1 is a repressor of E2-box-mediated gene activation. Mol. Cell. Biol. 14:5692–5700.
  • Sepulveda, J. L., and C. Wu. 2006. The parvins. Cell. Mol. Life Sci. 63:25–35.
  • Shaner, N. C., P. A. Steinbach, and R. Y. Tsien. 2005. A guide to choosing fluorescent proteins. Nat. Methods 2:905–909.
  • Simon, D. M., M. C. Arikan, S. Srisuma, S. Bhattacharya, L. W. Tsai, E. P. Ingenito, F. Gonzalez, S. D. Shapiro, and T. J. Mariani. 2006. Epithelial cell PPAR[gamma] contributes to normal lung maturation. FASEB J. 20:1507–1509.
  • Stighall, M., C. Manetopoulos, H. Axelson, and G. Landberg. 2005. High ID2 protein expression correlates with a favourable prognosis in patients with primary breast cancer and reduces cellular invasiveness of breast cancer cells. Int. J. Cancer 115:403–411.
  • Thiagalingam, A., A. De Bustros, M. Borges, R. Jasti, D. Compton, L. Diamond, M. Mabry, D. W. Ball, S. B. Baylin, and B. D. Nelkin. 1996. RREB-1, a novel zinc finger protein, is involved in the differentiation response to Ras in human medullary thyroid carcinomas. Mol. Cell. Biol. 16:5335–5345.
  • Thiesen, H.-J., and C. Bach. 1990. Target detection assay (TDA): a versatile procedure to determine DNA binding sites as demonstrated on SP1 protein. Nucleic Acids Res. 18:3202–3209.
  • Tontonoz, P., E. Hu, and B. M. Spiegelman. 1995. Regulation of adipocyte gene expression and differentiation by peroxisome proliferator activated receptor gamma. Curr. Opin. Genet. Dev. 5:571–576.
  • Tu, Y., Y. Huang, Y. Zhang, Y. Hua, and C. Wu. 2001. A new focal adhesion protein that interacts with integrin-linked kinase and regulates cell adhesion and spreading. J. Cell Biol. 153:585–598.
  • Wang, X., R. C. Southard, and M. W. Kilgore. 2004. The increased expression of peroxisome proliferator-activated receptor-gamma1 in human breast cancer is mediated by selective promoter usage. Cancer Res. 64:5592–5596.
  • Weaver, V. M., A. H. Fischer, O. W. Peterson, and M. J. Bissell. 1996. The importance of the microenvironment in breast cancer progression: recapitulation of mammary tumorigenesis using a unique human mammary epithelial cell model and a three-dimensional culture assay. Biochem. Cell Biol. 74:833–851.
  • White, D. E., R. D. Cardiff, S. Dedhar, and W. J. Muller. 2001. Mammary epithelial-specific expression of the integrin-linked kinase (ILK) results in the induction of mammary gland hyperplasias and tumors in transgenic mice. Oncogene 20:7064–7072.
  • Wu, C., S. Y. Keightley, C. Leung-Hagesteijn, G. Radeva, M. Coppolino, S. Goicoechea, J. A. McDonald, and S. Dedhar. 1998. Integrin-linked protein kinase regulates fibronectin matrix assembly, E-cadherin expression, and tumorigenicity. J. Biol. Chem. 273:528–536.
  • Yamaji, S., A. Suzuki, Y. Sugiyama, Y. Koide, M. Yoshida, H. Kanamori, H. Mohri, S. Ohno, and Y. Ishigatsubo. 2001. A novel integrin-linked kinase-binding protein, affixin, is involved in the early stage of cell-substrate interaction. J. Cell Biol. 153:1251–1264.
  • Yamaji, S., A. Suzuki, H. Kanamori, W. Mishima, R. Yoshimi, H. Takasaki, M. Takabayashi, K. Fujimaki, S. Fujisawa, S. Ohno, and Y. Ishigatsubo. 2004. Affixin interacts with alpha-actinin and mediates integrin signaling for reorganization of F-actin induced by initial cell-substrate interaction. J. Cell Biol. 165:539–551.
  • Yang, Y., B. G. Goldstein, H. H. Chao, and J. P. Katz. 2005. KLF4 and KLF5 regulate proliferation, apoptosis and invasion in esophageal cancer cells. Cancer Biol. Ther. 4:1216–1221.
  • Zhang, Y., K. Chen, L. Guo, and C. Wu. 2002. Characterization of PINCH-2, a new focal adhesion protein that regulates the PINCH-1-ILK interaction, cell spreading, and migration. J. Biol. Chem. 277:38328–38338.
  • Zhang, Y., K. Chen, Y. Tu, and C. Wu. 2004. Distinct roles of two structurally closely related focal adhesion proteins, alpha-parvins and beta-parvins, in regulation of cell morphology and survival. J. Biol. Chem. 279:41695–41705.

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