Overexpression of HMGB1 in melanoma predicts patient survival and suppression of HMGB1 induces cell cycle arrest and senescence in association with p21 (Waf1/Cip1) up-regulation via a p53-independent, Sp1-dependent pathway

Oncotarget

Volumn 5, Issue 15, 2014, Pages 6387-6403

  Li, Qingling ^a   Li, Jie ^a   Wen, Ting ^a   Zeng, Weiqi ^a   Peng, Cong ^a   Yan, Siyu ^a   Tan, Jieqiong ^b   Yang, Keda ^a   Liu, Shuang ^a   Guo, Aiyuan ^a   Zhang, Chong ^a   Su, Juan ^a   Jiang, Minghao ^a   Liu, Zhaoqian ^b   Zhou, Honghao ^b   Chen, Xiang ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b Central South University   (China)

Author keywords

High mobility group box 1; Melanoma; P21; P53; Sp1

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; HIGH MOBILITY GROUP B1 PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR SP1; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HMGB1 PROTEIN, HUMAN; SP1 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ADULT; ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CANCER SPECIFIC SURVIVAL; CARCINOGENICITY; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; CUTANEOUS MELANOMA; DISEASE SPECIFIC SURVIVAL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MELANOMA CELL; MOUSE; NEVUS; NONHUMAN; OVERALL SURVIVAL; PROMOTER REGION; PROTEIN EXPRESSION; SENESCENCE; SURVIVAL PREDICTION; TRANSCRIPTION REGULATION; TUMOR GROWTH; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL AGING; CELL CYCLE CHECKPOINT; GENETICS; HEK293 CELL LINE; MELANOMA; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SURVIVAL; TUMOR CELL LINE; UPREGULATION; XENOGRAFT;

ANIMALS; CELL AGING; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FEMALE; HEK293 CELLS; HETEROGRAFTS; HMGB1 PROTEIN; HUMANS; MALE; MELANOMA; MICE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; SP1 TRANSCRIPTION FACTOR; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84906220892     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2201     Document Type: Article

References (55)

1. Lotze MT and Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol. 2005; 5:331-42.
2. Ellerman JE, Brown CK, de Vera M, Zeh HJ, Billiar T, Rubartelli A and Lotze MT. Masquerader: high mobility group box-1 and cancer. Clin Cancer Res. 2007; 13: 2836-48.
3. Stros M. HMGB proteins: interactions with DNA and chromatin. Biochim Biophys Acta. 2010; 1799:101-13.
4. Ogawa Y, Aizawa S, Shirakawa H and Yoshida M. Stimulation of transcription accompanying relaxation of chromatin structure in cells overexpressing high mobility group 1 protein. J Biol Chem. 1995; 270:9272-80.
5. Stros M, Polanska E, Struncova S and Pospisilova S. HMGB1 and HMGB2 proteins up-regulate cellular expression of human topoisomerase IIalpha. Nucleic Acids Res. 2009; 37:2070-86.
6. Taguchi A, Blood DC, Del TG, Canet A, Lee DC, Qu W, Tanji N, Lu Y, Lalla E, Fu C, Hofmann MA, Kislinger T, Ingram M, Lu A, Tanaka H and Hori O. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 2000; 405:354-60.
7. Kang R, Tang D, Schapiro NE, Loux T, Livesey KM, Billiar TR, Wang H, Van Houten B, Lotze MT and Zeh HJ. The HMGB1/RAGE inflammatory pathway promotes pancreatic tumor growth by regulating mitochondrial bioenergetics. Oncogene. 2014; 33:567-77.
8. Curtin JF, Liu N, Candolfi M, Xiong W, Assi H, Yagiz K, Edwards MR, Michelsen KS, Kroeger KM, Liu C, Muhammad AK, Clark MC, Arditi M, Comin-Anduix B, Ribas A and Lowenstein PR. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med. 2009; 6:e10.
9. Mittal D, Saccheri F, Venereau E, Pusterla T, Bianchi ME and Rescigno M. TLR4-mediated skin carcinogenesis is dependent on immune and radioresistant cells. Embo J. 2010; 29:2242-52.
10. Brezniceanu ML, Volp K, Bosser S, Solbach C, Lichter P, Joos S and Zornig M. HMGB1 inhibits cell death in yeast and mammalian cells and is abundantly expressed in human breast carcinoma. Faseb J. 2003; 17:1295-7.
11. Volp K, Brezniceanu ML, Bosser S, Brabletz T, Kirchner T, Gottel D, Joos S and Zornig M. Increased expression of high mobility group box 1 (HMGB1) is associated with an elevated level of the antiapoptotic c-IAP2 protein in human colon carcinomas. Gut. 2006; 55:234-42.
12. Livesey KM, Kang R, Vernon P, Buchser W, Loughran P, Watkins SC, Zhang L, Manfredi JJ, Zeh HR, Li L, Lotze MT and Tang D. p53/HMGB1 complexes regulate autophagy and apoptosis. Cancer Res. 2012; 72:1996-2005.
13. Poser I, Golob M, Buettner R and Bosserhoff AK. Upregulation of HMG1 leads to melanoma inhibitory activity expression in malignant melanoma cells and contributes to their malignancy phenotype. Mol Cell Biol. 2003; 23:2991-8.
14. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R and Beach D. p21 is a universal inhibitor of cyclin kinases. Nature. 1993; 366:701-4.
15. Harper JW, Adami GR, Wei N, Keyomarsi K and Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993; 75:805-16.
16. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW and Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993; 75:817-25.
17. Harper JW, Adami GR, Wei N, Keyomarsi K and Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993; 75:805-16.
18. Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai LH, Zhang P, Dobrowolski S, Bai C, Connell-Crowley L, Swindell E and Et A. Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell. 1995; 6:387-400.
19. Warfel NA and El-Deiry WS. p21WAF1 and tumourigenesis: 20 years after. Curr Opin Oncol. 2013; 25:52-8.
20. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y and Wang XF. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci U S A. 1995; 92:5545-9.
21. Nakano K, Mizuno T, Sowa Y, Orita T, Yoshino T, Okuyama Y, Fujita T, Ohtani-Fujita N, Matsukawa Y, Tokino T, Yamagishi H, Oka T, Nomura H and Sakai T. Butyrate activates the WAF1/Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line. J Biol Chem. 1997; 272:22199-206.
22. Huang L, Sowa Y, Sakai T and Pardee AB. Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites. Oncogene. 2000; 19:5712-9.
23. De Siervi A, Marinissen M, Diggs J, Wang XF, Pages G and Senderowicz A. Transcriptional activation of p21(waf1/ cip1) by alkylphospholipids: role of the mitogen-activated protein kinase pathway in the transactivation of the human p21(waf1/cip1) promoter by Sp1. Cancer Res. 2004; 64:743-50.
24. Berg JM. Sp1 and the subfamily of zinc finger proteins with guanine-rich binding sites. Proc Natl Acad Sci U S A. 1992; 89:11109-10.
25. Lania L, Majello B and De Luca P. Transcriptional regulation by the Sp family proteins. Int J Biochem Cell Biol. 1997; 29:1313-23.
26. Biggs JR, Kudlow JE and Kraft AS. The role of the transcription factor Sp1 in regulating the expression of the WAF1/CIP1 gene in U937 leukemic cells. J Biol Chem. 1996; 271:901-6.
27. Billon N, Carlisi D, Datto MB, van Grunsven LA, Watt A, Wang XF and Rudkin BB. Cooperation of Sp1 and p300 in the induction of the CDK inhibitor p21WAF1/CIP1 during NGF-mediated neuronal differentiation. Oncogene. 1999; 18:2872-82.
28. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, Eggermont AM, Flaherty KT, Gimotty PA, Kirkwood JM, McMasters KM and Mihm MJ. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol. 2009; 27:6199-206.
29. Piris A, Mihm MJ and Duncan LM. AJCC melanoma staging update: impact on dermatopathology practice and patient management. J Cutan Pathol. 2011; 38:394-400.
30. Bogunovic D, O'Neill DW, Belitskaya-Levy I, Vacic V, Yu YL, Adams S, Darvishian F, Berman R, Shapiro R, Pavlick AC, Lonardi S, Zavadil J, Osman I and Bhardwaj N. Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci U S A. 2009; 106:20429-34.
31. Kawai H, Wiederschain D, Kitao H, Stuart J, Tsai KK and Yuan ZM. DNA damage-induced MDMX degradation is mediated by MDM2. J Biol Chem. 2003; 278:45946-53.
32. Herman AG, Hayano M, Poyurovsky MV, Shimada K, Skouta R, Prives C and Stockwell BR. Discovery of Mdm2-MdmX E3 ligase inhibitors using a cell-based ubiquitination assay. Cancer Discov. 2011; 1:312-25.
33. Phalke S, Mzoughi S, Bezzi M, Jennifer N, Mok WC, Low DH, Thike AA, Kuznetsov VA, Tan PH, Voorhoeve PM and Guccione E. p53-Independent regulation of p21Waf1/Cip1 expression and senescence by PRMT6. Nucleic Acids Res. 2012; 40:9534-42.
34. Blume SW, Snyder RC, Ray R, Thomas S, Koller CA and Miller DM. Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J Clin Invest. 1991; 88:1613-21.
35. Kardassis D, Papakosta P, Pardali K and Moustakas A. c-Jun transactivates the promoter of the human p21(WAF1/ Cip1) gene by acting as a superactivator of the ubiquitous transcription factor Sp1. J Biol Chem. 1999; 274:29572-81.
36. Gartel AL and Radhakrishnan SK. Lost in transcription: p21 repression, mechanisms, and consequences. Cancer Res. 2005; 65:3980-5.
37. Youn JH and Shin JS. Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J Immunol. 2006; 177:7889-97.
38. Tang D, Kang R, Zeh HR and Lotze MT. High-mobility group box 1 and cancer. Biochim Biophys Acta. 2010; 1799:131-40.
39. Uramoto H, Izumi H, Nagatani G, Ohmori H, Nagasue N, Ise T, Yoshida T, Yasumoto K and Kohno K. Physical interaction of tumour suppressor p53/p73 with CCAAT-binding transcription factor 2 (CTF2) and differential regulation of human high-mobility group 1 (HMG1) gene expression. Biochem J. 2003; 371:301-10.
40. Stros M, Ozaki T, Bacikova A, Kageyama H and Nakagawara A. HMGB1 and HMGB2 cell-specifically down-regulate the p53-and p73-dependent sequence-specific transactivation from the human Bax gene promoter. J Biol Chem. 2002; 277:7157-64.
41. Dintilhac A and Bernues J. HMGB1 interacts with many apparently unrelated proteins by recognizing short amino acid sequences. J Biol Chem. 2002; 277:7021-8.
42. Jiao Y, Wang HC and Fan SJ. Growth suppression and radiosensitivity increase by HMGB1 in breast cancer. Acta Pharmacol Sin. 2007; 28:1957-67.
43. Das D, Peterson RC and Scovell WM. High mobility group B proteins facilitate strong estrogen receptor binding to classical and half-site estrogen response elements and relax binding selectivity. Mol Endocrinol. 2004; 18:2616-32.
44. Miyazaki M, Sakaguchi M, Akiyama I, Sakaguchi Y, Nagamori S and Huh NH. Involvement of interferon regulatory factor 1 and S100C/A11 in growth inhibition by transforming growth factor beta 1 in human hepatocellular carcinoma cells. Cancer Res. 2004; 64:4155-61.
45. Cheng J, Yu DV, Zhou JH and Shapiro DJ. Tamoxifen induction of CCAAT enhancer-binding protein alpha is required for tamoxifen-induced apoptosis. J Biol Chem. 2007; 282:30535-43.
46. Jungert K, Buck A, von Wichert G, Adler G, Konig A, Buchholz M, Gress TM and Ellenrieder V. Sp1 is required for transforming growth factor-beta-induced mesenchymal transition and migration in pancreatic cancer cells. Cancer Res. 2007; 67:1563-70.
47. Kou XX, Hao T, Meng Z, Zhou YH, Gan YH. Acetylated Sp1 inhibits PTEN expression through binding to PTEN core promoter and recruitment of HDAC1 and promotes cancer cell migration and invasion. Carcinogenesis. 2013; 34:58-67.
48. Kern SE, Pietenpol JA, Thiagalingam S, Seymour A, Kinzler KW and Vogelstein B. Oncogenic forms of p53 inhibit p53-regulated gene expression. Science. 1992; 256:827-30.
49. Zhu WG, Hileman T, Ke Y, Wang P, Lu S, Duan W, Dai Z, Tong T, Villalona-Calero MA, Plass C and Otterson GA. 5-aza-2'-deoxycytidine activates the p53/p21Waf1/Cip1 pathway to inhibit cell proliferation. J Biol Chem. 2004; 279:15161-6.
50. Koutsodontis G, Tentes I, Papakosta P, Moustakas A and Kardassis D. Sp1 plays a critical role in the transcriptional activation of the human cyclin-dependent kinase inhibitor p21(WAF1/Cip1) gene by the p53 tumor suppressor protein. J Biol Chem. 2001; 276:29116-25.
51. Chen X, Lin J, Kanekura T, Su J, Lin W, Xie H, Wu Y, Li J, Chen M and Chang J. A small interfering CD147-targeting RNA inhibited the proliferation, invasiveness, and metastatic activity of malignant melanoma. Cancer Res. 2006; 66:11323-30.
52. Hayat MA. Microscopy, Immunohistochemistry, and Antigen Retrieval Methods. Springer US. 2002.
53. Zhu XD, Zhang JB, Zhuang PY, Zhu HG, Zhang W, Xiong YQ, Wu WZ, Wang L, Tang ZY and Sun HC. High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J Clin Oncol. 2008; 26:2707-16.
54. Straume O, Sviland L and Akslen LA. Loss of nuclear p16 protein expression correlates with increased tumor cell proliferation (Ki-67) and poor prognosis in patients with vertical growth phase melanoma. Clin Cancer Res. 2000; 6:1845-53.
55. Sirigu P, Piras F, Minerba L, Murtas D, Maxia C, Colombari R, Corbu A, Perra MT and Ugalde J. Prognostic prediction of the immunohistochemical expression of p16 and p53 in cutaneous melanoma: a comparison of two populations from different geographical regions. Eur J Histochem. 2006; 50:191-8.