B7-H4 downregulation induces mitochondrial dysfunction and enhances doxorubicin sensitivity via the cAMP/CREB/PGC1-α signaling pathway in HeLa cells

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 12, 2014, Pages 2323-2338

  Kim, Hyoung Kyu ^a   Song, In Sung ^a   Lee, Sun Young ^a   Jeong, Seung Hun ^a   Lee, Sung Ryul ^a   Heo, Hye Jin ^a   Thu, Vu Thi ^a   Kim, Nari ^a   Ko, Kyung Soo ^a   Rhee, Byoung Doo ^a   Jeong, Dae Hun ^b   Kim, Young Nam ^b   Han, Jin ^a  

^a Inje University College of Medicine   (South Korea)

^b Inje University College of Medicine   (South Korea)

Author keywords

Adenocarcinoma; B7 H4; cAMP; CREB; Mitochondria; PGC1

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOXORUBICIN; MITOCHONDRIAL PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UBIQUINOL CYTOCHROME C REDUCTASE; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1; ANTINEOPLASTIC ANTIBIOTIC; PPARGC1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR; VTCN1 PROTEIN, HUMAN;

ADENOCARCINOMA; ADULT; AGED; ARTICLE; CAMP ASSAY; CANCER THERAPY; CELL DEATH; CONFOCAL MICROSCOPE; CONFOCAL MICROSCOPY; CYTOSOLIC FRACTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; DRUG SENSITIVITY; ENERGY METABOLISM; FEMALE; FLOW CYTOMETER; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INNER MEMBRANE; MEMBRANE DEPOLARIZATION; METABOLIC REGULATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL TOXICITY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; UTERINE CERVIX CANCER; APOPTOSIS; DRUG EFFECTS; GENETICS; METABOLISM; MIDDLE AGED; MITOCHONDRION; UTERINE CERVIX TUMOR;

ADENOCARCINOMA; AGED; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOWN-REGULATION; DOXORUBICIN; FEMALE; HELA CELLS; HUMANS; MIDDLE AGED; MITOCHONDRIA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UTERINE CERVICAL NEOPLASMS; V-SET DOMAIN-CONTAINING T-CELL ACTIVATION INHIBITOR 1;

EID: 84912037650     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1493-3     Document Type: Article

References (42)

1. Arigami T, Uenosono Y, Ishigami S, Hagihara T, Haraguchi N, Natsugoe S (2011) Clinical significance of the B7-H4 coregulatory molecule as a novel prognostic marker in gastric cancer. World J Surg 35(9):2051–2057
2. Awadallah NS, Shroyer KR, Langer DA, Torkko KC, Chen YK, Bentz JS, Papkoff J, Liu W, Nash SR, Shah RJ (2008) Detection of B7-H4 and p53 in pancreatic cancer: potential role as a cytological diagnostic adjunct. Pancreas 36(2):200–206
3. Bhalla K, Hwang BJ, Dewi RE, Ou L, Twaddel W, Fang HB, Vafai SB, Vazquez F, Puigserver P, Boros L, Girnun GD (2011) PGC1alpha promotes tumor growth by inducing gene expression programs supporting lipogenesis. Cancer Res 71(21):6888–6898
4. Brantley-Finley C, Lyle C, Du L, Goodwin M, Hall T, Szwedo D, Kaushal G, Chambers T (2003) The JNK, ERK and p53 pathways play distinct roles in apoptosis mediated by the antitumor agents vinblastine, doxorubicin, and etoposide. Biochem Pharmacol 66(3):459–469
5. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria. J Biol Chem 278(38):36027–36031
6. Chen Y, Guo G, Guo S, Shimoda S, Shroyer KR, Tang Y, Wu Y (2011) Intracellular B7-H4 suppresses bile duct epithelial cell apoptosis in human primary biliary cirrhosis. Inflammation 34(6):688–697
7. Cheng L, Jiang J, Gao R, Wei S, Nan F, Li S, Kong B (2009) B7-H4 expression promotes tumorigenesis in ovarian cancer. Int J Gynecol Cancer 19(9):1481–1486
8. Fernandez-Marcos PJ, Auwerx J (2011) Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr 93(4):884S–890S
9. Galazka K, Oplawski M, Windorbska W, Skret-Magierlo J, Koper K, Basta P, Mach P, Dutch-Wicherek M, Mazur A, Wicherek L (2012) The immunohistochemical analysis of antigens such as RCAS1 and B7H4 in the cervical cancer nest and within the fibroblasts and macrophages infiltrating the cancer microenvironment. Am J Reprod Immunol 68(1):85–93
10. Galluzzi L, Larochette N, Zamzami N, Kroemer G (2006) Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 25(34):4812–4830
11. George SE, Bungay PJ, Naylor LH (1997) Evaluation of a CRE-directed luciferase reporter gene assay as an alternative to measuring cAMP accumulation. J Biomol Screen 2(4):235–240
12. Han B, Izumi H, Yasuniwa Y, Akiyama M, Yamaguchi T, Fujimoto N, Matsumoto T, Wu B, Tanimoto A, Sasaguri Y, Kohno K (2011) Human mitochondrial transcription factor A functions in both nuclei and mitochondria and regulates cancer cell growth. Biochem Biophys Res Commun 408(1):45–51
13. He C, Qiao H, Jiang H, Sun X (2011) The inhibitory role of B7-H4 in antitumor immunity: association with cancer progression and survival. Clin Dev Immunol 2011:695834
14. Hu R, Kim B, Chen C, Hebbar V, Kong ANT (2003) The roles of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cells. Carcinogenesis 24(8):1361–1367
15. Hutchinson DS, Chernogubova E, Dallner OS, Cannon B, Bengtsson T (2005) β-Adrenoceptors, but not α-adrenoceptors, stimulate AMP-activated protein kinase in brown adipocytes independently of uncoupling protein-1. Diabetologia 48(11):2386–2395
16. Jeong S, Song I, Kim H, Lee S, Song S, Suh H, Yoon Y, Yoo Y, Kim N, Rhee B, Ko K, Han J (2012) An analogue of resveratrol HS-1793 exhibits anticancer activity against MCF-7 cells via inhibition of mitochondrial biogenesis gene expression. Mol Cell 34(4):357–365
17. Kang S, Kim N, Joo H, Youm JB, Park W, Warda M, Kim H, Cuong D, Kim T, Kim E, Han J (2005) Changes of cytosolic Ca2+ under metabolic inhibition in isolated rat ventricular myocytes. Korean J Physiol Pharmacol 9(5):291–298
18. Kim H, Thu VT, Heo HJ, Kim N, Han J (2011) Cardiac proteomic responses to ischemia-reperfusion injury and ischemic preconditioning. Expert Rev Proteomics 8(2):241–261
19. Krambeck AE, Thompson RH, Dong H, Lohse CM, Park ES, Kuntz SM, Leibovich BC, Blute ML, Cheville JC, Kwon ED (2006) B7-H4 expression in renal cell carcinoma and tumor vasculature: associations with cancer progression and survival. Proc Natl Acad Sci U S A 103(27):10391–10396
20. Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, Brumlik M, Cheng P, Curiel T, Myers L, Lackner A, Alvarez X, Ochoa A, Chen L, Zou W (2006) B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 203(4):871–881
21. Kurita T, Izumi H, Kagami S, Kawagoe T, Toki N, Matsuura Y, Hachisuga T, Kohno K (2012) Mitochondrial transcription factor A regulates BCL2L1 gene expression and is a prognostic factor in serous ovarian cancer. Cancer Sci 103(2):239–444
22. Lee BS, Kim SH, Jin T, Choi EY, Oh J, Park S, Lee SH, Chung JH, Kang SM (2013) Protective effect of survivin in doxorubicin-induced cell death in h9c2 cardiac myocytes. Korean Circ J 43(6):400–407
23. McCubrey JA, Lahair MM, Franklin RA (2006) Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8(9–10):1775–1789
24. Modica-Napolitano JS, Singh K (2002) Mitochondria as targets for detection and treatment of cancer. Expert Rev Mol Med 4(09):1–19
25. Morse M, Tran E, Sun H, Levenson R, Fang Y (2011) Ligand-directed functional selectivity at the mu opioid receptor revealed by label-free integrative pharmacology on-target. PLoS ONE 6(10):e25643
26. Nakayama Y, Yamauchi M, Minagawa N, Torigoe T, Izumi H, Kohno K, Yamaguchi K (2012) Clinical significance of mitochondrial transcription factor A expression in patients with colorectal cancer. Oncol Rep 27(5):1325–1330
27. Salceda S, Tang T, Kmet M, Munteanu A, Ghosh M, Macina R, Liu W, Pilkington G, Papkoff J (2005) The immunomodulatory protein B7-H4 is overexpressed in breast and ovarian cancers and promotes epithelial cell transformation. Exp Cell Res 306(1):128–141
28. Sauter KA, Magun EA, Iordanov MS, Magun BE (2010) ZAK is required for doxorubicin, a novel ribotoxic stressor, to induce SAPK activation and apoptosis in HaCaT cells. Cancer Biol Ther 10(3):258–266
29. Sica GL, Choi IH, Zhu G, Tamada K, Wang SD, Tamura H, Chapoval AI, Flies DB, Bajorath J, Chen L (2003) B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 18(6):849–861
30. Song H, Park G, Kim YS, Hur I, Kim H, Ryu JW, Lee HK, Cho DH, Choi IH, Lee WJ, Hur DY (2008) B7-H4 reverse signaling induces the apoptosis of EBV-transformed B cells through Fas ligand up-regulation. Cancer Lett 266(2):227–237
31. Song IS, Ha GH, Kim JM, Jeong SY, Lee HC, Kim YS, Kim YJ, Kwon TK, Kim NS (2011) Human ZNF312b oncogene is regulated by Sp1 binding to its promoter region through DNA demethylation and histone acetylation in gastric cancer. Int J Cancer 129(9):2124–2133
32. Song IS, Kim HK, Lee SR, Jeong SH, Kim N, Ko KS, Rhee BD, Han J (2013) Mitochondrial modulation decreases the bortezomib-resistance in multiple myeloma cells. Int J Cancer 133(6):1357–1367
33. Song IS, Kim SU, Oh NS, Kim J, Yu DY, Huang SM, Kim JM, Lee DS, Kim NS (2009) Peroxiredoxin I contributes to TRAIL resistance through suppression of redox-sensitive caspase activation in human hepatoma cells. Carcinogenesis 30(7):1106–1114
34. Tringler B, Zhuo S, Pilkington G, Torkko KC, Singh M, Lucia MS, Heinz DE, Papkoff J, Shroyer KR (2005) B7-h4 is highly expressed in ductal and lobular breast cancer. Clin Cancer Res 11(5):1842–1848
35. Vazquez F, Lim J-H, Chim H, Bhalla K, Girnun G, Pierce K, Clish Clary B, Granter Scott R, Widlund Hans R, Spiegelman Bruce M, Puigserver P (2013) PGC1-alpha expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 23(3):287–301
36. Ventura-Clapier R, Garnier A, Veksler V (2008) Transcriptional control of mitochondrial biogenesis: the central role of PGC-1α. Cardiovasc Res 79(2):208–217
37. Wang X, Hao J, Metzger DL, Ao Z, Chen L, Ou D, Verchere CB, Mui A, Warnock GL (2012) B7-H4 treatment of T cells inhibits ERK, JNK, p38, and AKT activation. PLoS ONE 7(1):e28232
38. Wang X, Martindale JL, Holbrook NJ (2000) Requirement for ERK activation in cisplatin-induced apoptosis. J Biol Chem 275(50):39435–39443
39. Widlansky ME, Wang J, Shenouda SM, Hagen TM, Smith AR, Kizhakekuttu TJ, Kluge MA, Weihrauch D, Gutterman DD, Vita JA (2010) Altered mitochondrial membrane potential, mass, and morphology in the mononuclear cells of humans with type 2 diabetes. Transl Res 156(1):15–25
40. Zhang L, Wu H, Lu D, Li G, Sun C, Song H, Li J, Zhai T, Huang L, Hou C, Wang W, Zhou B, Chen S, Lu B, Zhang X (2013) The costimulatory molecule B7-H4 promote tumor progression and cell proliferation through translocating into nucleus. Oncogene 32(46):5347–5358
41. Zheng X, Li XD, Wu CP, Lu BF, Jiang JT (2012) Expression of costimulatory molecule B7-H4 in human malignant tumors. Onkologie 35(11):700–705
42. Zhou Y, Tozzi F, Chen J, Fan F, Xia L, Wang J, Gao G, Zhang A, Xia X, Brasher H, Widger W, Ellis LM, Weihua Z (2012) Intracellular ATP levels are a pivotal determinant of chemoresistance in colon cancer cells. Cancer Res 72(1):304–314