CypA: A Potential Target of Tumor Radiotherapy and/or Chemotherapy

Page: [3787 - 3802] Pages: 16

  • * (Excluding Mailing and Handling)

Abstract

Cyclophilin A (CypA) is a ubiquitous and highly conserved protein. CypA, the intracellular target protein for the immunosuppressant cyclosporine A (CsA), plays important cellular roles through peptidyl-prolyl cis-trans isomerase (PPIase). Increasing evidence shows that CypA is up-regulated in a variety of human cancers. In addition to being involved in the occurrence and development of multiple tumors, overexpression of CypA has also been shown to be strongly associated with malignant transformation. Surgery, chemotherapy and radiotherapy are the three main treatments for cancer. Chemotherapy and radiotherapy are often used as direct or adjuvant treatments for cancer. However, various side effects and resistance to both chemotherapy and radiotherapy bring great challenges to these two forms of treatment. According to recent reports, CypA can improve the chemosensitivity and/or radiosensitivity of cancers, possibly by affecting the expression of drug-resistant related proteins, cell cycle arrest and activation of the mitogen-activated protein kinase (MAPK) signaling pathways. In this review, we focus on the role of CypA in cancer, its impact on cancer chemotherapeutic and radiotherapy sensitivity, and the mechanism of action. It is suggested that CypA may be a novel potential therapeutic target for cancer chemotherapy and/or radiotherapy.

Keywords: Cancer, cyclophilin A, CD147, CsA, signal transduction, chemotherapy, radiotherapy, therapy target.

[1]
Dornan, J.; Taylor, P.; Walkinshaw, M.D. Structures of immunophilins and their ligand complexes. Curr. Top. Med. Chem., 2003, 3(12), 1392-1409.
[http://dx.doi.org/10.2174/1568026033451899] [PMID: 12871171]
[2]
Galat, A. Peptidylprolyl cis/trans isomerases (immunophilins): Biological diversity--targets--functions. Curr. Top. Med. Chem., 2003, 3(12), 1315-1347.
[http://dx.doi.org/10.2174/1568026033451862] [PMID: 12871165]
[3]
Braaten, D.; Wellington, S.; Warburton, D.; Luban, J. Assignment of cyclophilin A (PPIA) to human chromosome band 7p13by in situ hybridization. Cytogenet. Cell Genet., 1996, 74(4), 262.
[http://dx.doi.org/10.1159/000134430] [PMID: 8976380]
[4]
Willenbrink, W.; Halaschek, J.; Schuffenhauer, S.; Kunz, J.; Steinkasserer, A. Cyclophilin A, the major intracellular receptor for the immunosuppressant cyclosporin A, maps to chromosome 7p11.2-p13: four pseudogenes map to chromosomes 3, 10, 14, and 18. Genomics, 1995, 28(1), 101-104.
[http://dx.doi.org/10.1006/geno.1995.1112] [PMID: 7590732]
[5]
Ivery, M.T. Immunophilins: Switched on protein binding domains? Med. Res. Rev., 2000, 20(6), 452-484.
[http://dx.doi.org/10.1002/1098-1128(200011)20:6<452::AID-MED2>3.0.CO;2-6] [PMID: 11058892]
[6]
Bannon, J.H.; O’Donovan, D.S.; Kennelly, S.M.; Mc Gee, M.M. The peptidyl prolyl isomerase cyclophilin A localizes at the centrosome and the midbody and is required for cytokinesis. Cell Cycle, 2012, 11(7), 1340-1353.
[http://dx.doi.org/10.4161/cc.19711] [PMID: 22421161]
[7]
Jin, Z.G.; Melaragno, M.G.; Liao, D.F.; Yan, C.; Haendeler, J.; Suh, Y.A.; Lambeth, J.D.; Berk, B.C. Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ. Res., 2000, 87(9), 789-796.
[http://dx.doi.org/10.1161/01.RES.87.9.789] [PMID: 11055983]
[8]
Seko, Y.; Fujimura, T.; Taka, H.; Mineki, R.; Murayama, K.; Nagai, R. Hypoxia followed by reoxygenation induces secretion of cyclophilin A from cultured rat cardiac myocytes. Biochem. Biophys. Res. Commun., 2004, 317(1), 162-168.
[http://dx.doi.org/10.1016/j.bbrc.2004.03.021] [PMID: 15047162]
[9]
Suzuki, J.; Jin, Z.G.; Meoli, D.F.; Matoba, T.; Berk, B.C. Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells. Circ. Res., 2006, 98(6), 811-817.
[http://dx.doi.org/10.1161/01.RES.0000216405.85080.a6] [PMID: 16527992]
[10]
Kim, K.; Oh, I.K.; Yoon, K.S.; Ha, J.; Kang, I.; Choe, W. Antioxidant activity is required for the protective effects of cyclophilin A against oxidative stress. Mol. Med. Rep., 2015, 12(1), 712-718.
[http://dx.doi.org/10.3892/mmr.2015.3392] [PMID: 25738284]
[11]
Kim, H.; Kim, W.J.; Jeon, S.T.; Koh, E.M.; Cha, H.S.; Ahn, K.S.; Lee, W.H. Cyclophilin A may contribute to the inflammatory processes in rheumatoid arthritis through induction of matrix degrading enzymes and inflammatory cytokines from macrophages. Clin. Immunol., 2005, 116(3), 217-224.
[http://dx.doi.org/10.1016/j.clim.2005.05.004] [PMID: 15993649]
[12]
Wang, L.; Wang, C.H.; Jia, J.F.; Ma, X.K.; Li, Y.; Zhu, H.B.; Tang, H.; Chen, Z.N.; Zhu, P. Contribution of cyclophilin A to the regulation of inflammatory processes in rheumatoid arthritis. J. Clin. Immunol., 2010, 30(1), 24-33.
[http://dx.doi.org/10.1007/s10875-009-9329-1] [PMID: 19789967]
[13]
Dawar, F.U.; Wu, J.; Zhao, L.; Khattak, M.N.; Mei, J.; Lin, L. Updates in understanding the role of cyclophilin A in leukocyte chemotaxis. J. Leukoc. Biol., 2017, 101(4), 823-826.
[http://dx.doi.org/10.1189/jlb.3RU1116-477R] [PMID: 28062572]
[14]
Xue, Z.; Yuan, W.; Li, J.; Zhou, H.; Xu, L.; Weng, J.; Li, X.; Zhang, X.; Wang, Z.; Yan, J. Cyclophilin A mediates the ox-LDL-induced activation and apoptosis of macrophages via autophagy. Int. J. Cardiol., 2017, 230, 142-148.
[http://dx.doi.org/10.1016/j.ijcard.2016.12.042] [PMID: 28038796]
[15]
Sherry, B.; Yarlett, N.; Strupp, A.; Cerami, A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc. Natl. Acad. Sci. USA, 1992, 89(8), 3511-3515.
[http://dx.doi.org/10.1073/pnas.89.8.3511] [PMID: 1565646]
[16]
Shimokawa, H.; Sunamura, S.; Satoh, K. RhoA/Rho-kinase in the cardiovascular system. Circ. Res., 2016, 118(2), 352-366.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306532] [PMID: 26838319]
[17]
Seizer, P.; Ungern-Sternberg, S.N.; Schönberger, T.; Borst, O.; Münzer, P.; Schmidt, E.M.; Mack, A.F.; Heinzmann, D.; Chatterjee, M.; Langer, H.; Malešević, M.; Lang, F.; Gawaz, M.; Fischer, G.; May, A.E. Extracellular cyclophilin A activates platelets via EMMPRIN (CD147) and PI3K/Akt signaling, which promotes platelet adhesion and thrombus formation in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol., 2015, 35(3), 655-663.
[http://dx.doi.org/10.1161/ATVBAHA.114.305112] [PMID: 25550208]
[18]
Satoh, K.; Nigro, P.; Matoba, T.; O’Dell, M.R.; Cui, Z.; Shi, X.; Mohan, A.; Yan, C.; Abe, J.; Illig, K.A.; Berk, B.C. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat. Med., 2009, 15(6), 649-656.
[http://dx.doi.org/10.1038/nm.1958] [PMID: 19430489]
[19]
Jin, Z.G.; Lungu, A.O.; Xie, L.; Wang, M.; Wong, C.; Berk, B.C. Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler. Thromb. Vasc. Biol., 2004, 24(7), 1186-1191.
[http://dx.doi.org/10.1161/01.ATV.0000130664.51010.28] [PMID: 15130913]
[20]
Xue, C.; Sowden, M.; Berk, B.C. Extracellular cyclophilin A, especially acetylated, causes pulmonary hypertension by stimulating endothelial apoptosis, redox stress and inflammation. Arterioscler. Thromb. Vasc. Biol., 2017, 37(6), 1138-1146.
[http://dx.doi.org/10.1161/ATVBAHA.117.309212] [PMID: 28450293]
[21]
Yang, Y.; Lu, N.; Zhou, J.; Chen, Z.N.; Zhu, P. Cyclophilin A up-regulates MMP-9 expression and adhesion of monocytes/macrophages via CD147 signalling pathway in rheumatoid arthritis. Rheumatology (Oxford), 2008, 47(9), 1299-1310.
[http://dx.doi.org/10.1093/rheumatology/ken225] [PMID: 18567920]
[22]
Yurchenko, V.; Zybarth, G.; O’Connor, M.; Dai, W.W.; Franchin, G.; Hao, T.; Guo, H.; Hung, H.C.; Toole, B.; Gallay, P.; Sherry, B.; Bukrinsky, M. Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J. Biol. Chem., 2002, 277(25), 22959-22965.
[http://dx.doi.org/10.1074/jbc.M201593200] [PMID: 11943775]
[23]
Obchoei, S.; Sawanyawisuth, K.; Wongkham, C.; Kasinrerk, W.; Yao, Q.; Chen, C.; Wongkham, S. Secreted cyclophilin A mediates G1/S phase transition of cholangiocarcinoma cells via CD147/ERK1/2 pathway. Tumour Biol., 2015, 36(2), 849-859.
[http://dx.doi.org/10.1007/s13277-014-2691-5] [PMID: 25296734]
[24]
Boulos, S.; Meloni, B.P.; Arthur, P.G.; Majda, B.; Bojarski, C.; Knuckey, N.W. Evidence that intracellular cyclophilin A and cyclophilin A/CD147 receptor-mediated ERK1/2 signalling can protect neurons against in vitro oxidative and ischemic injury. Neurobiol. Dis., 2007, 25(1), 54-64.
[http://dx.doi.org/10.1016/j.nbd.2006.08.012] [PMID: 17011206]
[25]
Jin, J.; Wang, S.J.; Cui, J.; Li, L.; Li, J.Y.; Liu, F.L.; Sun, X.X.; Jiang, J.L.; Cui, H.Y.; Chen, Z.N. Hypo-phosphorylated CD147 promotes migration and invasion of hepatocellular carcinoma cells and predicts a poor prognosis. Cell Oncol. (Dordr.), 2019, 42(4), 537-554.
[http://dx.doi.org/10.1007/s13402-019-00444-0] [PMID: 31016558]
[26]
Li, M.; Zhai, Q.; Bharadwaj, U.; Wang, H.; Li, F.; Fisher, W.E.; Chen, C.; Yao, Q. Cyclophilin A is overexpressed in human pancreatic cancer cells and stimulates cell proliferation through CD147. Cancer, 2006, 106(10), 2284-2294.
[http://dx.doi.org/10.1002/cncr.21862] [PMID: 16604531]
[27]
Handschumacher, R.E.; Harding, M.W.; Rice, J.; Drugge, R.J.; Speicher, D.W. Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science, 1984, 226(4674), 544-547.
[http://dx.doi.org/10.1126/science.6238408] [PMID: 6238408]
[28]
Matsuda, S.; Koyasu, S. Mechanisms of action of cyclosporine. Immunopharmacology, 2000, 47(2-3), 119-125.
[http://dx.doi.org/10.1016/S0162-3109(00)00192-2] [PMID: 10878286]
[29]
Liu, J.; Farmer, J.D., Jr; Lane, W.S.; Friedman, J.; Weissman, I.; Schreiber, S.L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell, 1991, 66(4), 807-815.
[http://dx.doi.org/10.1016/0092-8674(91)90124-H] [PMID: 1715244]
[30]
Howard, B.A.; Zheng, Z.; Campa, M.J.; Wang, M.Z.; Sharma, A.; Haura, E.; Herndon, J.E., II; Fitzgerald, M.C.; Bepler, G.; Patz, E.F., Jr Translating biomarkers into clinical practice: Prognostic implications of cyclophilin A and macrophage migratory inhibitory factor identified from protein expression profiles in non-small cell lung cancer. Lung Cancer, 2004, 46(3), 313-323.
[http://dx.doi.org/10.1016/j.lungcan.2004.05.013] [PMID: 15541816]
[31]
Qian, Z.; Zhao, X.; Jiang, M.; Jia, W.; Zhang, C.; Wang, Y.; Li, B.; Yue, W. Downregulation of cyclophilin A by siRNA diminishes non-small cell lung cancer cell growth and metastasis via the regulation of matrix metallopeptidase 9. BMC Cancer, 2012, 12, 442.
[http://dx.doi.org/10.1186/1471-2407-12-442] [PMID: 23031673]
[32]
Ren, Y.X.; Wang, S.J.; Fan, J.H.; Sun, S.J.; Li, X.; Padhiar, A.A.; Zhang, J.N. CD147 stimulates hepatoma cells escaping from immune surveillance of T cells by interaction with Cyclophilin A. Biomed. Pharmacother., 2016, 80, 289-297.
[http://dx.doi.org/10.1016/j.biopha.2016.03.036] [PMID: 27133068]
[33]
Gong, Z.; Chi, C.; Huang, X.; Chu, H.; Wang, J.; Du, F.; Jiang, L.; Chen, J.; Cyclophilin, A. Cyclophilin A is overexpressed in hepatocellular carcinoma and is associated with the cell cycle. Anticancer Res., 2017, 37(8), 4443-4447.
[http://dx.doi.org/10.21873/anticanres.11839] [PMID: 28739738]
[34]
Zheng, J.; Koblinski, J.E.; Dutson, L.V.; Feeney, Y.B.; Clevenger, C.V. Prolyl isomerase cyclophilin A regulation of Janus-activated kinase 2 and the progression of human breast cancer. Cancer Res., 2008, 68(19), 7769-7778.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0639] [PMID: 18829531]
[35]
Huang, C.; Sun, Z.; Sun, Y.; Chen, X.; Zhu, X.; Fan, C.; Liu, B.; Zhao, Y.; Zhang, W. Association of increased ligand cyclophilin A and receptor CD147 with hypoxia, angiogenesis, metastasis and prognosis of tongue squamous cell carcinoma. Histopathology, 2012, 60(5), 793-803.
[http://dx.doi.org/10.1111/j.1365-2559.2011.04130.x] [PMID: 22320715]
[36]
Yang, H.; Chen, J.; Yang, J.; Qiao, S.; Zhao, S.; Yu, L. Cyclophilin A is upregulated in small cell lung cancer and activates ERK1/2 signal. Biochem. Biophys. Res. Commun., 2007, 361(3), 763-767.
[http://dx.doi.org/10.1016/j.bbrc.2007.07.085] [PMID: 17678621]
[37]
Nakano, N.; Sakashita, S.; Matsuoka, R.; Murata, Y.; Shiba-Ishii, A.; Kobayashi, N.; Sato, Y.; Noguchi, M. Cyclophilin A expression and its prognostic significance in lung adenocarcinoma. Pathol. Int., 2017, 67(11), 555-563.
[http://dx.doi.org/10.1111/pin.12593] [PMID: 29027312]
[38]
Guo, Y.; Jiang, M.; Zhao, X.; Gu, M.; Wang, Z.; Xu, S.; Yue, W. Cyclophilin A promotes non-small cell lung cancer metastasis via p38 MAPK. Thorac. Cancer, 2018, 9(1), 120-128.
[http://dx.doi.org/10.1111/1759-7714.12548] [PMID: 29110442]
[39]
Zhang, M.; Dai, C.; Zhu, H.; Chen, S.; Wu, Y.; Li, Q.; Zeng, X.; Wang, W.; Zuo, J.; Zhou, M.; Xia, Z.; Ji, G.; Saiyin, H.; Qin, L.; Yu, L. Cyclophilin A promotes human hepatocellular carcinoma cell metastasis via regulation of MMP3 and MMP9. Mol. Cell. Biochem., 2011, 357(1-2), 387-395.
[http://dx.doi.org/10.1007/s11010-011-0909-z] [PMID: 21667159]
[40]
Feng, M.X.; Li, J.P.; Wang, H.; Shen, Y.X.; Tan, L.J.; Wang, Q.; Wang, Y.Q. Clinical significance of cyclophilin a expression in esophageal squamous cell carcinoma. Genet. Test. Mol. Biomarkers, 2015, 19(4), 182-186.
[http://dx.doi.org/10.1089/gtmb.2014.0067] [PMID: 25420107]
[41]
Grigoryeva, E.S.; Cherdyntseva, N.V.; Karbyshev, M.S.; Volkomorov, V.V.; Stepanov, I.V.; Zavyalova, M.V.; Perelmuter, V.M.; Buldakov, M.A.; Afanasjev, S.G.; Tuzikov, S.A.; Bukurova, Y.A.; Lisitsyn, N.A.; Beresten, S.F. Expression of cyclophilin A in gastric adenocarcinoma patients and its inverse association with local relapses and distant metastasis. Pathol. Oncol. Res., 2014, 20(2), 467-473.
[http://dx.doi.org/10.1007/s12253-013-9718-x] [PMID: 24272759]
[42]
Feng, W.; Xin, Y.; Xiao, Y.; Li, W.; Sun, D. Cyclophilin A enhances cell proliferation and xenografted tumor growth of early gastric cancer. Dig. Dis. Sci., 2015, 60(9), 2700-2711.
[http://dx.doi.org/10.1007/s10620-015-3694-9] [PMID: 26008617]
[43]
Frei, E., III Curative cancer chemotherapy. Cancer Res., 1985, 45(12 Pt 1), 6523-6537.
[PMID: 2998603]
[44]
Szekeres, T.; Novotny, L. New targets and drugs in cancer chemotherapy. Med. Princ. Pract., 2002, 11(3), 117-125.
[http://dx.doi.org/10.1159/000063243] [PMID: 12138292]
[45]
Baskar, R.; Lee, K.A.; Yeo, R.; Yeoh, K.W. Cancer and radiation therapy: Current advances and future directions. Int. J. Med. Sci., 2012, 9(3), 193-199.
[http://dx.doi.org/10.7150/ijms.3635] [PMID: 22408567]
[46]
Arevalo-Rodriguez, M.; Wu, X.; Hanes, S.D.; Heitman, J. Prolyl isomerases in yeast. Front. Biosci., 2004, 9, 2420-2446.
[http://dx.doi.org/10.2741/1405] [PMID: 15353296]
[47]
Ke, H.; Huai, Q. Crystal structures of cyclophilin and its partners. Front. Biosci., 2004, 9, 2285-2296.
[http://dx.doi.org/10.2741/1396] [PMID: 15353287]
[48]
Campa, M.J.; Wang, M.Z.; Howard, B.; Fitzgerald, M.C.; Patz, E.F., Jr Protein expression profiling identifies macrophage migration inhibitory factor and cyclophilin a as potential molecular targets in non-small cell lung cancer. Cancer Res., 2003, 63(7), 1652-1656.
[PMID: 12670919]
[49]
Howard, B.A.; Furumai, R.; Campa, M.J.; Rabbani, Z.N.; Vujaskovic, Z.; Wang, X.F.; Patz, E.F., Jr Stable RNA interference-mediated suppression of cyclophilin A diminishes non-small-cell lung tumor growth in vivo. Cancer Res., 2005, 65(19), 8853-8860.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-1219] [PMID: 16204056]
[50]
Wang, J.; Li, F.; Tan, J.; Peng, X.; Sun, L.; Wang, P.; Jia, S.; Yu, Q.; Huo, H.; Zhao, H. Melittin inhibits the invasion of MCF-7 cells by downregulating CD147 and MMP-9 expression. Oncol. Lett., 2017, 13(2), 599-604.
[http://dx.doi.org/10.3892/ol.2016.5516] [PMID: 28356935]
[51]
Volker, S.E.; Hedrick, S.E.; Feeney, Y.B.; Clevenger, C.V. Cyclophilin A function in mammary epithelium impacts Jak2/Stat5 signaling, morphogenesis, differentiation, and tumorigenesis in the mammary gland. Cancer Res., 2018, 78(14), 3877-3887.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2892] [PMID: 29959151]
[52]
Chen, J.; He, Q.Y.; Yuen, A.P.; Chiu, J.F. Proteomics of buccal squamous cell carcinoma: The involvement of multiple pathways in tumorigenesis. Proteomics, 2004, 4(8), 2465-2475.
[http://dx.doi.org/10.1002/pmic.200300762] [PMID: 15274141]
[53]
Qi, Y.J.; He, Q.Y.; Ma, Y.F.; Du, Y.W.; Liu, G.C.; Li, Y.J.; Tsao, G.S.; Ngai, S.M.; Chiu, J.F. Proteomic identification of malignant transformation-related proteins in esophageal squamous cell carcinoma. J. Cell. Biochem., 2008, 104(5), 1625-1635.
[http://dx.doi.org/10.1002/jcb.21727] [PMID: 18320592]
[54]
Huang, C.F.; Sun, Z.J.; Zhao, Y.F.; Chen, X.M.; Jia, J.; Zhang, W.F. Increased expression of peroxiredoxin 6 and cyclophilin A in squamous cell carcinoma of the tongue. Oral Dis., 2011, 17(3), 328-334.
[http://dx.doi.org/10.1111/j.1601-0825.2010.01730.x] [PMID: 20796224]
[55]
Takahashi, M.; Suzuki, S.; Ishikawa, K. Cyclophilin A-EMMPRIN interaction induces invasion of head and neck squamous cell carcinoma. Oncol. Rep., 2012, 27(1), 198-203.
[http://dx.doi.org/10.3892/or.2011.1474] [PMID: 21956400]
[56]
Li, Y.; Guo, H.; Dong, D.; Wu, H.; Li, E. Expression and prognostic relevance of cyclophilin A and matrix metalloproteinase 9 in esophageal squamous cell carcinoma. Diagn. Pathol., 2013, 8, 207.
[http://dx.doi.org/10.1186/1746-1596-8-207] [PMID: 24351116]
[57]
Wang, D.; Li, Y.; Cui, P.; Zhao, Q.; Tan, B.B.; Zhang, Z.D.; Liu, Y.; Jia, N. Zerumbone induces gastric cancer cells apoptosis: Involving cyclophilin A. Biomed. Pharmacother., 2016, 83, 740-745.
[http://dx.doi.org/10.1016/j.biopha.2016.07.034] [PMID: 27479192]
[58]
Shen, J.; Person, M.D.; Zhu, J.; Abbruzzese, J.L.; Li, D. Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by two-dimensional gel electrophoresis and mass spectrometry. Cancer Res., 2004, 64(24), 9018-9026.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-3262] [PMID: 15604267]
[59]
Li, M.; Wang, H.; Li, F.; Fisher, W.E.; Chen, C.; Yao, Q. Effect of cyclophilin A on gene expression in human pancreatic cancer cells. Am. J. Surg., 2005, 190(5), 739-745.
[http://dx.doi.org/10.1016/j.amjsurg.2005.07.013] [PMID: 16226951]
[60]
Bauer, K.; Kretzschmar, A.K.; Cvijic, H.; Blumert, C.; Löffler, D.; Brocke-Heidrich, K.; Schiene-Fischer, C.; Fischer, G.; Sinz, A.; Clevenger, C.V.; Horn, F. Cyclophilins contribute to Stat3 signaling and survival of multiple myeloma cells. Oncogene, 2009, 28(31), 2784-2795.
[http://dx.doi.org/10.1038/onc.2009.142] [PMID: 19503092]
[61]
Zhu, D.; Wang, Z.; Zhao, J.J.; Calimeri, T.; Meng, J.; Hideshima, T.; Fulciniti, M.; Kang, Y.; Ficarro, S.B.; Tai, Y.T.; Hunter, Z.; McMilin, D.; Tong, H.; Mitsiades, C.S.; Wu, C.J.; Treon, S.P.; Dorfman, D.M.; Pinkus, G.; Munshi, N.C.; Tassone, P.; Marto, J.A.; Anderson, K.C.; Carrasco, R.D. The Cyclophilin A-CD147 complex promotes the proliferation and homing of multiple myeloma cells. Nat. Med., 2015, 21(6), 572-580.
[http://dx.doi.org/10.1038/nm.3867] [PMID: 26005854]
[62]
Choi, K.J.; Piao, Y.J.; Lim, M.J.; Kim, J.H.; Ha, J.; Choe, W.; Kim, S.S. Overexpressed cyclophilin A in cancer cells renders resistance to hypoxia- and cisplatin-induced cell death. Cancer Res., 2007, 67(8), 3654-3662.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1759] [PMID: 17440077]
[63]
Sun, S.; Wang, Q.; Giang, A.; Cheng, C.; Soo, C.; Wang, C.Y.; Liau, L.M.; Chiu, R. Knockdown of CypA inhibits interleukin-8 (IL-8) and IL-8-mediated proliferation and tumor growth of glioblastoma cells through down-regulated NF-κB. J. Neurooncol., 2011, 101(1), 1-14.
[http://dx.doi.org/10.1007/s11060-010-0220-y] [PMID: 20454998]
[64]
Saw, P.E.; Zhang, A.; Nie, Y.; Zhang, L.; Xu, Y.; Xu, X. Tumor-associated fibronectin targeted liposomal nanoplatform for cyclophilin A siRNA delivery and targeted malignant glioblastoma therapy. Front. Pharmacol., 2018, 9, 1194.
[http://dx.doi.org/10.3389/fphar.2018.01194] [PMID: 30386245]
[65]
Qi, Z.Y.; Wang, F.; Yue, Y.Y.; Guo, X.W.; Guo, R.M.; Li, H.L.; Xu, Y.Y. CYPA promotes the progression and metastasis of serous ovarian cancer (SOC) in vitro and in vivo. J. Ovarian Res., 2019, 12(1), 118.
[http://dx.doi.org/10.1186/s13048-019-0593-2] [PMID: 31783885]
[66]
Yang, J.; Zhou, M.; Zhao, R.; Peng, S.; Luo, Z.; Li, X.; Cao, L.; Tang, K.; Ma, J.; Xiong, W.; Fan, S.; Schmitt, D.C.; Tan, M.; Li, X.; Li, G. Identification of candidate biomarkers for the early detection of nasopharyngeal carcinoma by quantitative proteomic analysis. J. Proteomics, 2014, 109, 162-175.
[http://dx.doi.org/10.1016/j.jprot.2014.06.025] [PMID: 24998431]
[67]
Liu, L.; Zuo, L.; Yang, J.; Xin, S.; Zhang, J.; Zhou, J.; Li, G.; Tang, J.; Lu, J. Exosomal cyclophilin A as a novel noninvasive biomarker for Epstein-Barr virus associated nasopharyngeal carcinoma. Cancer Med., 2019, 8(6), 3142-3151.
[http://dx.doi.org/10.1002/cam4.2185] [PMID: 31063269]
[68]
Obchoei, S.; Weakley, S.M.; Wongkham, S.; Wongkham, C.; Sawanyawisuth, K.; Yao, Q.; Chen, C. Cyclophilin A enhances cell proliferation and tumor growth of liver fluke-associated cholangiocarcinoma. Mol. Cancer, 2011, 10, 102.
[http://dx.doi.org/10.1186/1476-4598-10-102] [PMID: 21871105]
[69]
Li, Z.; Gou, J.; Xu, J. Down-regulation of focal adhesion signaling in response to cyclophilin A knockdown in human endometrial cancer cells, implicated by cDNA microarray analysis. Gynecol. Oncol., 2013, 131(1), 191-197.
[http://dx.doi.org/10.1016/j.ygyno.2013.07.095] [PMID: 23899654]
[70]
Usta, A.; Turan, G.; Adali, E. The expression of cyclophilin A in ovarian endometrioma: Its correlation with recurrence and vascularity. Tohoku J. Exp. Med., 2017, 243(2), 141-150.
[http://dx.doi.org/10.1620/tjem.243.141] [PMID: 29081463]
[71]
Zhang, H.; Chen, J.; Liu, F.; Gao, C.; Wang, X.; Zhao, T.; Liu, J.; Gao, S.; Zhao, X.; Ren, H.; Hao, J. CypA, a gene downstream of HIF-1α, promotes the development of PDAC. PLoS One, 2014, 9(3), e92824.
[http://dx.doi.org/10.1371/journal.pone.0092824] [PMID: 24662981]
[72]
Yu, X.; Harris, S.L.; Levine, A.J. The regulation of exosome secretion: A novel function of the p53 protein. Cancer Res., 2006, 66(9), 4795-4801.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-4579] [PMID: 16651434]
[73]
Li, Z.; Min, W.; Gou, J. Knockdown of cyclophilin A reverses paclitaxel resistance in human endometrial cancer cells via suppression of MAPK kinase pathways. Cancer Chemother. Pharmacol., 2013, 72(5), 1001-1011.
[http://dx.doi.org/10.1007/s00280-013-2285-8] [PMID: 24036847]
[74]
Kim, H.; Oh, Y.; Kim, K.; Jeong, S.; Chon, S.; Kim, D.; Jung, M.H.; Pak, Y.K.; Ha, J.; Kang, I.; Choe, W. Cyclophilin A regulates JNK/p38-MAPK signaling through its physical interaction with ASK1. Biochem. Biophys. Res. Commun., 2015, 464(1), 112-117.
[http://dx.doi.org/10.1016/j.bbrc.2015.06.078] [PMID: 26095851]
[75]
Lin, Z.L.; Wu, H.J.; Chen, J.A.; Lin, K.C.; Hsu, J.H. Cyclophilin A as a downstream effector of PI3K/Akt signalling pathway in multiple myeloma cells. Cell Biochem. Funct., 2015, 33(8), 566-574.
[http://dx.doi.org/10.1002/cbf.3156] [PMID: 26833980]
[76]
Wang, G.; Shen, J.; Sun, J.; Jiang, Z.; Fan, J.; Wang, H.; Yu, S.; Long, Y.; Liu, Y.; Bao, H.; Zhang, K.X.; Han, K.; Zhu, M.; Zheng, Y.; Lin, Z.; Jiang, C.; Guo, M. Cyclophilin A maintains glioma-initiating cell stemness by regulating Wnt/β-catenin signaling. Clin. Cancer Res., 2017, 23(21), 6640-6649.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-0774] [PMID: 28790108]
[77]
Saleh, T.; Jankowski, W.; Sriram, G.; Rossi, P.; Shah, S.; Lee, K.B.; Cruz, L.A.; Rodriguez, A.J.; Birge, R.B.; Kalodimos, C.G. Cyclophilin A promotes cell migration via the Abl-Crk signaling pathway. Nat. Chem. Biol., 2016, 12(2), 117-123.
[http://dx.doi.org/10.1038/nchembio.1981] [PMID: 26656091]
[78]
Xie, Y.; Li, X.; Ge, J. Cyclophilin A-FoxO1 signaling pathway in endothelial cell apoptosis. Cell. Signal., 2019, 61, 57-65.
[http://dx.doi.org/10.1016/j.cellsig.2019.04.014] [PMID: 31063815]
[79]
Wang, T.; Carraway, R.E.; LaRoche, D.; FitzGerald, T.J. Disruption of ERK1/2 sensitizes radiation resistance prostate cancer cells to paclitaxel and ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys., 2014, 90, S806.
[http://dx.doi.org/10.1016/j.ijrobp.2014.05.2326]
[80]
Chen, S.; Zhang, M.; Ma, H.; Saiyin, H.; Shen, S.; Xi, J.; Wan, B.; Yu, L. Oligo-microarray analysis reveals the role of cyclophilin A in drug resistance. Cancer Chemother. Pharmacol., 2008, 61(3), 459-469.
[http://dx.doi.org/10.1007/s00280-007-0491-y] [PMID: 17520256]
[81]
Lee, J. Novel combinational treatment of cisplatin with cyclophilin A inhibitors in human heptocellular carcinomas. Arch. Pharm. Res., 2010, 33(9), 1401-1409.
[http://dx.doi.org/10.1007/s12272-010-0914-x] [PMID: 20945139]
[82]
Huang, J.C.; Zhao, P.C.; Zhang, H.Z.; Wang, H. A proteomical study on the radiosensitized target molecules of fuzheng zengxiao formula in pulmonary adenocarcinoma nude mice model. J. Tradit. Chin. Med., 2011, 31(1), 3-6.
[http://dx.doi.org/10.1016/S0254-6272(11)60001-0] [PMID: 21563497]
[83]
Jiang, X.; Zhang, Q.L.; Tian, Y.H.; Huang, J.C.; Ma, G.L. RNA interference-mediated gene silencing of cyclophilin A enhances the radiosensitivity of PAa human lung adenocarcinoma cells in vitro. Oncol. Lett., 2017, 13(3), 1619-1624.
[http://dx.doi.org/10.3892/ol.2017.5667] [PMID: 28454299]
[84]
Chevalier, F.; Depagne, J.; Hem, S.; Chevillard, S.; Bensimon, J.; Bertrand, P.; Lebeau, J. Accumulation of cyclophilin A isoforms in conditioned medium of irradiated breast cancer cells. Proteomics, 2012, 12(11), 1756-1766.
[http://dx.doi.org/10.1002/pmic.201100319] [PMID: 22623065]
[85]
Schweyer, S.; Soruri, A.; Heintze, A.; Radzun, H.J.; Fayyazi, A. The role of reactive oxygen species in cisplatin-induced apoptosis in human malignant testicular germ cell lines. Int. J. Oncol., 2004, 25(6), 1671-1676.
[http://dx.doi.org/10.3892/ijo.25.6.1671] [PMID: 15547704]
[86]
Guo, H.; Lee, C.; Shah, M.; Janga, S.R.; Edman, M.C.; Klinngam, W.; Hamm-Alvarez, S.F.; MacKay, J.A. A novel elastin-like polypeptide drug carrier for cyclosporine A improves tear flow in a mouse model of Sjögren’s syndrome. J. Control. Release, 2018, 292, 183-195.
[http://dx.doi.org/10.1016/j.jconrel.2018.10.026] [PMID: 30359668]
[87]
Yang, C.H.; Horwitz, S.B. Taxol®: The first microtubule stabilizing agent. Int. J. Mol. Sci., 2017, 18(8), 1733.
[http://dx.doi.org/10.3390/ijms18081733] [PMID: 28792473]
[88]
Kanwar, J.R.; Kamalapuram, S.K.; Kanwar, R.K. Targeting survivin in cancer: Patent review. Expert Opin. Ther. Pat., 2010, 20(12), 1723-1737.
[http://dx.doi.org/10.1517/13543776.2010.533657] [PMID: 21083520]
[89]
Fojo, T.; Menefee, M. Mechanisms of multidrug resistance: The potential role of microtubule-stabilizing agents. Ann. Oncol., 2007, 18(Suppl. 5), v3-v8.
[http://dx.doi.org/10.1093/annonc/mdm172] [PMID: 17656560]
[90]
Duan, Z.; Lamendola, D.E.; Penson, R.T.; Kronish, K.M.; Seiden, M.V. Overexpression of IL-6 but not IL-8 increases paclitaxel resistance of U-2OS human osteosarcoma cells. Cytokine, 2002, 17(5), 234-242.
[http://dx.doi.org/10.1006/cyto.2001.1008] [PMID: 12027404]
[91]
Gerk, P.M.; Vore, M. Regulation of expression of the multidrug resistance-associated protein 2 (MRP2) and its role in drug disposition. J. Pharmacol. Exp. Ther., 2002, 302(2), 407-415.
[http://dx.doi.org/10.1124/jpet.102.035014] [PMID: 12130697]
[92]
Zeng, H.; Liu, G.; Rea, P.A.; Kruh, G.D. Transport of amphipathic anions by human multidrug resistance protein 3. Cancer Res., 2000, 60(17), 4779-4784.
[PMID: 10987286]
[93]
To-Figueras, J.; Gené, M.; Gómez-Catalán, J.; Piqué, E.; Borrego, N.; Caballero, M.; Cruellas, F.; Raya, A.; Dicenta, M.; Corbella, J. Microsomal epoxide hydrolase and glutathione S-transferase polymorphisms in relation to laryngeal carcinoma risk. Cancer Lett., 2002, 187(1-2), 95-101.
[http://dx.doi.org/10.1016/S0304-3835(02)00406-8] [PMID: 12359356]
[94]
Blackburn, A.C.; Coggan, M.; Tzeng, H.F.; Lantum, H.; Polekhina, G.; Parker, M.W.; Anders, M.W.; Board, P.G. GSTZ1d: A new allele of glutathione transferase zeta and maleylacetoacetate isomerase. Pharmacogenetics, 2001, 11(8), 671-678.
[http://dx.doi.org/10.1097/00008571-200111000-00005] [PMID: 11692075]
[95]
Fojo, T.; Bates, S. Strategies for reversing drug resistance. Oncogene, 2003, 22(47), 7512-7523.
[http://dx.doi.org/10.1038/sj.onc.1206951] [PMID: 14576855]
[96]
Brazin, K.N.; Mallis, R.J.; Fulton, D.B.; Andreotti, A.H. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc. Natl. Acad. Sci. USA, 2002, 99(4), 1899-1904.
[http://dx.doi.org/10.1073/pnas.042529199] [PMID: 11830645]
[97]
Cheng, F.; Yuan, W.; Cao, M.; Chen, R.; Wu, X.; Yan, J. Cyclophilin A protects cardiomyocytes against hypoxia/reoxygenation-induced apoptosis via the AKT/Nox2 pathway. Oxid. Med. Cell. Longev., 2019, 2019, 2717986.
[http://dx.doi.org/10.1155/2019/2717986] [PMID: 31182989]
[98]
Pawlik, T.M.; Keyomarsi, K. Role of cell cycle in mediating sensitivity to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys., 2004, 59(4), 928-942.
[http://dx.doi.org/10.1016/j.ijrobp.2004.03.005] [PMID: 15234026]
[99]
Han, X.; Yoon, S.H.; Ding, Y.; Choi, T.G.; Choi, W.J.; Kim, Y.H.; Kim, Y.J.; Huh, Y.B.; Ha, J.; Kim, S.S. Cyclosporin A and sanglifehrin A enhance chemotherapeutic effect of cisplatin in C6 glioma cells. Oncol. Rep., 2010, 23(4), 1053-1062.
[http://dx.doi.org/10.3892/or_00000732] [PMID: 20204291]