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Article

Pin1 Regulates the Dynamics of c-Myc DNA Binding To Facilitate Target Gene Regulation and Oncogenesis

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Pages 2930-2949 | Received 15 Nov 2012, Accepted 17 May 2013, Published online: 20 Mar 2023

REFERENCES

  • Meyer N, Penn LZ. 2008. Reflecting on 25 years with MYC. Nat. Rev. Cancer 8:976–990.
  • Patel JH, Loboda AP, Showe MK, Showe LC, McMahon SB. 2004. Analysis of genomic targets reveals complex functions of MYC. Nat. Rev. Cancer 4:562–568.
  • Kleine-Kohlbrecher D, Adhikary S, Eilers M. 2006. Mechanisms of transcriptional repression by Myc. Curr. Top. Microbiol. Immunol. 302:51–62.
  • Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J, Cocito A, Amati B. 2003. Genomic targets of the human c-Myc protein. Genes Dev. 17:1115–1129.
  • Flinn EM, Busch CM, Wright AP. 1998. myc boxes, which are conserved in myc family proteins, are signals for protein degradation via the proteasome. Mol. Cell. Biol. 18:5961–5969.
  • Jones TR, Cole MD. 1987. Rapid cytoplasmic turnover of c-myc mRNA: requirement of the 3′ untranslated sequences. Mol. Cell. Biol. 7:4513–4521.
  • Kelly K, Cochran BH, Stiles CD, Leder P. 1983. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell 35:603–610.
  • Sears R, Leone G, DeGregori J, Nevins JR. 1999. Ras enhances Myc protein stability. Mol. Cell 3:169–179.
  • Arnold HK, Zhang X, Daniel CJ, Tibbitts D, Escamilla-Powers J, Farrell A, Tokarz S, Morgan C, Sears RC. 2009. The Axin1 scaffold protein promotes formation of a degradation complex for c-Myc. EMBO J. 28:500–512.
  • Lutterbach B, Hann SR. 1994. Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis. Mol. Cell. Biol. 14:5510–5522.
  • Pulverer BJ, Fisher C, Vousden K, Littlewood T, Evan G, Woodgett JR. 1994. Site-specific modulation of c-Myc cotransformation by residues phosphorylated in vivo. Oncogene 9:59–70.
  • Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. 2000. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev. 14:2501–2514.
  • Bachireddy P, Bendapudi PK, Felsher DW. 2005. Getting at MYC through RAS. Clin. Cancer Res. 11:4278–4281.
  • Sears RC. 2004. The life cycle of C-myc: from synthesis to degradation. Cell Cycle 3:1133–1137.
  • Bechard M, Dalton S. 2009. Subcellular localization of glycogen synthase kinase 3beta controls embryonic stem cell self-renewal. Mol. Cell. Biol. 29:2092–2104.
  • Gregory MA, Qi Y, Hann SR. 2003. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J. Biol. Chem. 278:51606–51612.
  • Arnold HK, Sears RC. 2006. Protein phosphatase 2A regulatory subunit B56alpha associates with c-myc and negatively regulates c-myc accumulation. Mol. Cell. Biol. 26:2832–2844.
  • Yeh E, Cunningham M, Arnold H, Chasse D, Monteith T, Ivaldi G, Hahn WC, Stukenberg PT, Shenolikar S, Uchida T, Counter CM, Nevins JR, Means AR, Sears R. 2004. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat. Cell Biol. 6:308–318.
  • Amati B. 2004. Myc degradation: dancing with ubiquitin ligases. Proc. Natl. Acad. Sci. U. S. A. 101:8843–8844.
  • Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN, Clurman BE. 2004. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. U. S. A. 101:9085–9090.
  • Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, Ishida N, Okumura F, Nakayama K, Nakayama KI. 2004. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 23:2116–2125.
  • Malempati S, Tibbitts D, Cunningham M, Akkari Y, Olson S, Fan G, Sears RC. 2006. Aberrant stabilization of c-Myc protein in some lymphoblastic leukemias. Leukemia 20:1572–1581.
  • Zhang X, Farrell AS, Daniel CJ, Arnold H, Scanlan C, Laraway BJ, Janghorban M, Lum L, Chen D, Troxell M, Sears R. 2012. Mechanistic insight into Myc stabilization in breast cancer involving aberrant Axin1 expression. Proc. Natl. Acad. Sci. U. S. A. 109:2790–2795.
  • Ryo A, Liou YC, Lu KP, Wulf G. 2003. Prolyl isomerase Pin1: a catalyst for oncogenesis and a potential therapeutic target in cancer. J. Cell Sci. 116:773–783.
  • Yeh ES, Means AR. 2007. PIN1, the cell cycle and cancer. Nat. Rev. Cancer 7:381–388.
  • Rustighi A, Tiberi L, Soldano A, Napoli M, Nuciforo P, Rosato A, Kaplan F, Capobianco A, Pece S, Di Fiore PP, Del Sal G. 2009. The prolyl-isomerase Pin1 is a Notch1 target that enhances Notch1 activation in cancer. Nat. Cell Biol. 11:133–142.
  • Takahashi K, Akiyama H, Shimazaki K, Uchida C, Akiyama-Okunuki H, Tomita M, Fukumoto M, Uchida T. 2007. Ablation of a peptidyl prolyl isomerase Pin1 from p53-null mice accelerated thymic hyperplasia by increasing the level of the intracellular form of Notch1. Oncogene 26:3835–3845.
  • Yi P, Wu RC, Sandquist J, Wong J, Tsai SY, Tsai MJ, Means AR, O'Malley BW. 2005. Peptidyl-prolyl isomerase 1 (Pin1) serves as a coactivator of steroid receptor by regulating the activity of phosphorylated steroid receptor coactivator 3 (SRC-3/AIB1). Mol. Cell. Biol. 25:9687–9699.
  • Sears R, Ohtani K, Nevins JR. 1997. Identification of positively and negatively acting elements regulating expression of the E2F2 gene in response to cell growth signals. Mol. Cell. Biol. 17:5227–5235.
  • Escamilla-Powers JR, Sears RC. 2007. A conserved pathway that controls c-Myc protein stability through opposing phosphorylation events occurs in yeast. J. Biol. Chem. 282:5432–5442.
  • Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK, Clarke ND, Wei CL, Ng HH. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106–1117.
  • Kim J, Lee JH, Iyer VR. 2008. Global identification of Myc target genes reveals its direct role in mitochondrial biogenesis and its E-box usage in vivo. PLoS One 3:e1798. doi:10.1371/journal.pone.0001798.
  • Abadie A. 2002. Bootstrap tests for distributional treatment effects in instrumental variable models. J. Am. Stat. Assoc. 97:284–292.
  • Sekhon J. 2011. Multivariate and propensity score matching software with automated balance optimization. J. Stat. Software. 42:1–52.
  • Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, Quackenbush JF, Stijleman IJ, Palazzo J, Marron JS, Nobel AB, Mardis E, Nielsen TO, Ellis MJ, Perou CM, Bernard PS. 2009. Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol. 27:1160–1167.
  • Molinari E, Gilman M, Natesan S. 1999. Proteasome-mediated degradation of transcriptional activators correlates with activation domain potency in vivo. EMBO J. 18:6439–6447.
  • Salghetti SE, Muratani M, Wijnen H, Futcher B, Tansey WP. 2000. Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc. Natl. Acad. Sci. U. S. A. 97:3118–3123.
  • Thomas D, Tyers M. 2000. Transcriptional regulation: kamikaze activators. Curr. Biol. 10:R341–R343.
  • Uchida T, Takamiya M, Takahashi M, Miyashita H, Ikeda H, Terada T, Matsuo Y, Shirouzu M, Yokoyama S, Fujimori F, Hunter T. 2003. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol. 10:15–24.
  • Gartel AL, Ye X, Goufman E, Shianov P, Hay N, Najmabadi F, Tyner AL. 2001. Myc represses the p21(WAF1/CIP1) promoter and interacts with Sp1/Sp3. Proc. Natl. Acad. Sci. U. S. A. 98:4510–4515.
  • Staller P, Peukert K, Kiermaier A, Seoane J, Lukas J, Karsunky H, Moroy T, Bartek J, Massague J, Hanel F, Eilers M. 2001. Repression of p15INK4b expression by Myc through association with Miz-1. Nat. Cell Biol. 3:392–399.
  • Liu T, Huang Y, Likhotvorik RI, Keshvara L, Hoyt DG. 2008. Protein Never in Mitosis Gene A Interacting-1 (PIN1) regulates degradation of inducible nitric oxide synthase in endothelial cells. Am. J. Physiol. Cell Physiol. 295:C819–C827.
  • Winkler KE, Swenson KI, Kornbluth S, Means AR. 2000. Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 287:1644–1647.
  • Cheng SW, Davies KP, Yung E, Beltran RJ, Yu J, Kalpana GV. 1999. c-MYC interacts with INI1/hSNF5 and requires the SWI/SNF complex for transactivation function. Nat. Genet. 22:102–105.
  • Kenneth NS, Ramsbottom BA, Gomez-Roman N, Marshall L, Cole PA, White RJ. 2007. TRRAP and GCN5 are used by c-Myc to activate RNA polymerase III transcription. Proc. Natl. Acad. Sci. U. S. A. 104:14917–14922.
  • Vervoorts J, Luscher-Firzlaff JM, Rottmann S, Lilischkis R, Walsemann G, Dohmann K, Austen M, Luscher B. 2003. Stimulation of c-MYC transcriptional activity and acetylation by recruitment of the cofactor CBP. EMBO Rep. 4:484–490.
  • Gargano B, Amente S, Majello B, Lania L. 2007. P-TEFb is a crucial co-factor for Myc transactivation. Cell Cycle 6:2031–2037.
  • Hebbes TR, Thorne AW, Crane-Robinson C. 1988. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 7:1395–1402.
  • O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C, Hardwick J, Welcker M, Meijerink JP, Pieters R, Draetta G, Sears R, Clurman BE, Look AT. 2007. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J. Exp. Med. 204:1813–1824.
  • Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN. 2003. GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 4:R28.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545–15550.
  • Miller FR. 2000. Xenograft models of premalignant breast disease. J. Mammary Gland Biol. Neoplasia 5:379–391.
  • Andrechek ER, Hardy WR, Siegel PM, Rudnicki MA, Cardiff RD, Muller WJ. 2000. Amplification of the neu/erbB-2 oncogene in a mouse model of mammary tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 97:3444–3449.
  • Selbert S, Bentley DJ, Melton DW, Rannie D, Lourenco P, Watson CJ, Clarke AR. 1998. Efficient BLG-Cre mediated gene deletion in the mammary gland. Transgenic Res. 7:387–396.
  • Wang X, Cunningham M, Zhang X, Tokarz S, Laraway B, Troxell M, Sears RC. 2011. Phosphorylation regulates c-Myc's oncogenic activity in the mammary gland. Cancer Res. 71:925–936.
  • Lin CY, Loven J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA. 2012. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151:56–67.
  • Barna M, Pusic A, Zollo O, Costa M, Kondrashov N, Rego E, Rao PH, Ruggero D. 2008. Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature 456:971–975.
  • Dang CV, Le A, Gao P. 2009. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin. Cancer Res. 15:6479–6483.
  • van Riggelen J, Yetil A, Felsher DW. 2010. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat. Rev. Cancer 10:301–309.
  • Giraud M, Yoshida H, Abramson J, Rahl PB, Young RA, Mathis D, Benoist C. 2012. Aire unleashes stalled RNA polymerase to induce ectopic gene expression in thymic epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 109:535–540.
  • Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. c-Myc regulates transcriptional pause release. Cell 141:432–445.
  • Arabi A, Rustum C, Hallberg E, Wright AP. 2003. Accumulation of c-Myc and proteasomes at the nucleoli of cells containing elevated c-Myc protein levels. J. Cell Sci. 116:1707–1717.
  • Luscher B, Vervoorts J. 2012. Regulation of gene transcription by the oncoprotein MYC. Gene 494:145–160.
  • Agrawal P, Yu K, Salomon AR, Sedivy JM. 2010. Proteomic profiling of Myc-associated proteins. Cell Cycle 9:4908–4921.
  • Frank SR, Parisi T, Taubert S, Fernandez P, Fuchs M, Chan HM, Livingston DM, Amati B. 2003. MYC recruits the TIP60 histone acetyltransferase complex to chromatin. EMBO Rep. 4:575–580.
  • Sanchez-Arevalo Lobo VJ, Doni M, Verrecchia A, Sanulli S, Faga G, Piontini A, Bianchi M, Conacci-Sorrell M, Mazzarol G, Peg V, Losa JH, Ronchi P, Ponzoni M, Eisenman RN, Doglioni C, Amati B.14 January2013. Dual regulation of Myc by Abl. Oncogene. doi:10.1038/onc.2012.621.
  • Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6:197–208.
  • Fladvad M, Zhou K, Moshref A, Pursglove S, Safsten P, Sunnerhagen M. 2005. N and C-terminal sub-regions in the c-Myc transactivation region and their joint role in creating versatility in folding and binding. J. Mol. Biol. 346:175–189.
  • Cowling VH, Cole MD. 2006. Mechanism of transcriptional activation by the Myc oncoproteins. Semin. Cancer Biol. 16:242–252.
  • Kim MR, Choi HS, Heo TH, Hwang SW, Kang KW. 2008. Induction of vascular endothelial growth factor by peptidyl-prolyl isomerase Pin1 in breast cancer cells. Biochem. Biophys. Res. Commun. 369:547–553.
  • Mantovani F, Piazza S, Gostissa M, Strano S, Zacchi P, Mantovani R, Blandino G, Del Sal G. 2004. Pin1 links the activities of c-Abl and p300 in regulating p73 function. Mol. Cell 14:625–636.
  • Mantovani F, Tocco F, Girardini J, Smith P, Gasco M, Lu X, Crook T, Del Sal G. 2007. The prolyl isomerase Pin1 orchestrates p53 acetylation and dissociation from the apoptosis inhibitor iASPP. Nat. Struct. Mol. Biol. 14:912–920.
  • Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, Wulf G, Rottapel R, Yamaoka S, Lu KP. 2003. Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell 12:1413–1426.
  • Takahashi K, Uchida C, Shin RW, Shimazaki K, Uchida T. 2008. Prolyl isomerase, Pin1: new findings of post-translational modifications and physiological substrates in cancer, asthma and Alzheimer's disease. Cell. Mol. Life Sci. 65:359–375.
  • Lufei C, Koh TH, Uchida T, Cao X. 2007. Pin1 is required for the Ser727 phosphorylation-dependent Stat3 activity. Oncogene 26:7656–7664.
  • Reid G, Hubner MR, Metivier R, Brand H, Denger S, Manu D, Beaudouin J, Ellenberg J, Gannon F. 2003. Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11:695–707.
  • Lonard DM, Nawaz Z, Smith CL, O'Malley BW. 2000. The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol. Cell 5:939–948.
  • Salghetti SE, Caudy AA, Chenoweth JG, Tansey WP. 2001. Regulation of transcriptional activation domain function by ubiquitin. Science 293:1651–1653.
  • Zhang Q, Spears E, Boone DN, Li Z, Gregory MA, Hann SR. 2013. Domain-specific c-Myc ubiquitylation controls c-Myc transcriptional and apoptotic activity. Proc. Natl. Acad. Sci. U. S. A. 110:978–983.
  • Ayala G, Wang D, Wulf G, Frolov A, Li R, Sowadski J, Wheeler TM, Lu KP, Bao L. 2003. The prolyl isomerase Pin1 is a novel prognostic marker in human prostate cancer. Cancer Res. 63:6244–6251.
  • Lu KP. 2003. Prolyl isomerase Pin1 as a molecular target for cancer diagnostics and therapeutics. Cancer Cell 4:175–180.
  • Ryo A, Liou YC, Wulf G, Nakamura M, Lee SW, Lu KP. 2002. PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol. 22:5281–5295.
  • Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Petkova V, Lu KP. 2001. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J. 20:3459–3472.
  • Lu KP, Hanes SD, Hunter T. 1996. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380:544–547.
  • Rippmann JF, Hobbie S, Daiber C, Guilliard B, Bauer M, Birk J, Nar H, Garin-Chesa P, Rettig WJ, Schnapp A. 2000. Phosphorylation-dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis. Cell Growth Differ. 11:409–416.
  • Wulf G, Ryo A, Liou YC, Lu KP. 2003. The prolyl isomerase Pin1 in breast development and cancer. Breast Cancer Res. 5:76–82.
  • Wulf G, Garg P, Liou YC, Iglehart D, Lu KP. 2004. Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J. 23:3397–3407.

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