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  • Original Article
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Differential regulation of CXC ligand 1 transcription in melanoma cell lines by poly(ADP-ribose) polymerase-1

Oncogene volume 25, pages 7714–7722 (2006)Cite this article

Abstract

The continuous production of the CXC ligand 1 (CXCL1) chemokine by melanoma cells is a major effector of tumor growth. We have previously shown that the constitutive expression of this chemokine is dependent upon transcription factors nuclear factor-kappa B (NF-κB), stimulating protein-1 (SP1), high-mobility group-I/Y (HMGI/Y), CAAT displacement protein (CDP) and poly(ADP-ribose) polymerase-1 (PARP-1). In this study, we demonstrate for the first time the mechanism of transcriptional regulation of CXCL1 through PARP-1 in melanoma cells. In its inactive state, PARP-1 binds to the CXCL1 promoter in a sequence-specific manner and prevents binding of NF-κB (p65/p50) to its element. However, activation of the PARP-1 enzymatic activity enhances CXCL1 expression, owing to the loss of PARP-1 binding to the CXCL1 promoter, accompanied by enhanced binding of p65 to the promoter. The delineation of the role of NF-κB-interacting factors in the putative CXCL1 enhanceosome will provide key information in developing strategies to block constitutive expression of this and other chemokines in cancer and to develop targeted therapy.

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Abbreviations

3-AB:

3-aminobenzamide

ADP:

adenosine diphosphate

5-AIQ:

5-aminoisoquinolinone.HCl

BSA:

bovine serum albumin

ChIP:

chromatin immunoprecipitation

CXCL1:

CXC ligand 1

DMEM:

Dulbecco's modified Eagle's medium

DTT:

dithiothreitol

EDTA:

ethylenediaminetetraacetic acid

EMSA:

electrophoretic mobility shift assay

FBS:

fetal bovine serum

HMGI/Y:

high-mobility group-I/Y

HMGS:

human melanocyte growth supplement

IgG:

immunoglobulin G

IUR:

immediate upstream region

NAD+:

β-nicotinamide adenine dinucleotide

NF-κB:

nuclear factor-kappa B

NHEM:

normal human epidermal melanocyte

PAGE:

polyacrylamide gel electrophoresis

PARP-1:

poly(ADP-ribose)polymerase-1

PCR:

polymerase chain reaction

SDS:

sodium dodecyl sulfate

SFM:

serum-free media

SP1:

stimulating protein-1

ssDNA:

single-stranded DNA

WT:

wild type

References

  • Alvarez-Gonzalez R, Spring H, Muller M, Burkle A . (1999). J Biol Chem 274: 32122–32126.

  • Balentien E, Mufson BE, Shattuck RL, Derynck R, Richmond A . (1991). Oncogene 6: 1115–1124.

  • Boulares AH, Zoltoski AJ, Sherif ZA, Jolly P, Massaro D, Smulson ME . (2003). Am J Respir Cell Mol Biol 28: 322–329.

  • Burkle A . (2001). Bioessays 23: 795–806.

  • Cayuela ML, Carrillo A, Ramirez P, Parrilla P, Yelamos J . (2001). Biochem Biophys Res Commun 285: 289–294.

  • Chang WJ, Alvarez-Gonzalez R . (2001). J Biol Chem 276: 47664–47670.

  • Dhawan P, Richmond A . (2002). J Biol Chem 277: 7920–7928.

  • Ha HC . (2004). Proc Natl Acad Sci USA 101: 5087–5092.

  • Haghnegahdar H, Du J, Wang D, Strieter RM, Burdick MD, Nanney LB et al. (2000). J Leukocyte Biol 67: 53–62.

  • Haqq C, Nosrati M, Sudilovsky D, Crothers J, Khodabakhsh D, Pulliam BL et al. (2005). Proc Natl Acad Sci USA 102: 6092–6097.

  • Hassa PO, Hottiger MO . (1999). Biol Chem 380: 953–959.

  • Huang K, Tidyman WE, Le KU, Kirsten E, Kun E, Ordahl CP . (2004). Biochemistry 43: 217–223.

  • Kameoka M, Ota K, Tetsuka T, Tanaka Y, Itaya A, Okamoto T et al. (2000). Biochem J 346 (Part 3): 641–649.

  • Keane MP, Arenberg DA, Lynch III JP, Whyte RI, Iannettoni MD, Burdick MD et al. (1997). J Immunol 159: 1437–1443.

  • Kim MY, Mauro S, Gevry N, Lis JT, Kraus WL . (2004). Cell 119: 803–814.

  • Li A, Varney ML, Singh RK . (2001). Clin Cancer Res 7: 3298–3304.

  • Meisterernst M, Stelzer G, Roeder RG . (1997). Proc Natl Acad Sci USA 94: 2261–2265.

  • Nirodi C, Nagdas S, Gygi SP, Olson G, Aebersold R, Richmond A . (2001). J Biol Chem 276: 9366–9374.

  • Olbina G, Cieslak D, Ruzdijic S, Esler C, An Z, Wang X et al. (1996). Anticancer Res 16: 3525–3530.

  • Owen JD, Strieter R, Burdick M, Haghnegahdar H, Nanney L, Shattuck-Brandt R et al. (1997). Int J Cancer 73: 94–103.

  • Richards BL, Eisma RJ, Spiro JD, Lindquist RL, Kreutzer DL . (1997). Am J Surg 174: 507–512.

  • Schadendorf M, Algermissen W, Sticherling M, Czarnetzki BM . (1994). J Immunol 153: 3360.

  • Schadendorf D, Fichtner I, Makki A, Alijagic S, Kupper M, Mrowietz U et al. (1996). Br J Cancer 74: 194–199.

  • Shattuck RL, Wood LD, Jaffe GJ, Richmond A . (1994). Mol Cell Biol 14: 791–802.

  • Simbulan-Rosenthal CM, Haddad BR, Rosenthal DS, Weaver Z, Coleman A, Luo R et al. (1999). Proc Natl Acad Sci USA 96: 13191–13196.

  • Simbulan-Rosenthal CM, Rosenthal DS, Luo R, Samara R, Espinoza LA, Hassa PO et al. (2003). Oncogene 22: 8460–8471.

  • Smulson ME, Simbulan-Rosenthal CM, Boulares AH, Yakovlev A, Stoica B, Iyer S et al. (2000). Adv Enzyme Regul 40: 183–215.

  • Soldatenkov VA, Chasovskikh S, Potaman VN, Trofimova I, Smulson ME, Dritschilo A . (2002). J Biol Chem 277: 665–670.

  • Strieter RM, Polverini PJ, Kunkel SL, Arenberg DA, Burdick MD, Kasper J et al. (1995). J Biol Chem 270: 27348–27357.

  • Szabo E, Virag L, Bakondi E, Gyure L, Hasko G, Bai P et al. (2001). J Invest Dermatol 117: 74–80.

  • Takamori H, Oades ZG, Hoch OC, Burger M, Schraufstatter IU . (2000). Pancreas 21: 52–56.

  • Tulin A, Chinenov Y, Spradling A . (2003). Curr Top Dev Biol 56: 55–83.

  • Tulin A, Spradling A . (2003). Science 299: 560–562.

  • Wood LD, Farmer AA, Richmond A . (1995). Nucleic Acids Res 23: 4210–4219.

  • Yang J, Richmond A . (2001). Cancer Res 61: 4901–4909.

  • Zhang Z, Hildebrandt EF, Simbulan-Rosenthal CM, Anderson MG . (2002). Virology 296: 107–116.

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Acknowledgements

This work was supported by grants from the National Institute of Health (NIH-CA-56704, AR), the VA Merit Award (AR), in part by grants from the National Cancer Institute (PO1CA-74175, MES) and the US Air Force Office of Scientific Research (AF-FA9550-04-1-0395, MES).

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Authors and Affiliations

  1. Department of Veterans Affairs, Vanderbilt University School of Medicine, Nashville, TN, USA

    K I Amiri & A Richmond

  2. Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN, USA

    K I Amiri & A Richmond

  3. Department of Microbiology, Meharry Medical College, Nashville, TN, USA

    K I Amiri

  4. Department of Biochemistry and Molecular Biology, Georgetown University School of Medicine, Washington, DC, USA

    H C Ha & M E Smulson

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  1. K I Amiri
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  2. H C Ha
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Correspondence to A Richmond.

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Amiri, K., Ha, H., Smulson, M. et al. Differential regulation of CXC ligand 1 transcription in melanoma cell lines by poly(ADP-ribose) polymerase-1. Oncogene 25, 7714–7722 (2006). https://doi.org/10.1038/sj.onc.1209751

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