High expression level of peptidylprolyl isomerase A is correlated with poor prognosis of liver hepatocellular carcinoma
- Authors:
- Shilong Wang
- Minghuan Li
- Ligang Xing
- Jinming Yu
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Affiliations: Department of Clinical Medicine, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, P.R. China, Department of Radiation Oncology, Shandong Cancer Hospital Affiliated to Shandong University, Jinan, Shandong 250117, P.R. China - Published online on: September 10, 2019 https://doi.org/10.3892/ol.2019.10846
- Pages: 4691-4702
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Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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|
Moore LE, Fung ET, McGuire M, Rabkin CC, Molinaro A, Wang Z, Zhang F, Wang J, Yip C, Meng XY and Pfeiffer RM: Evaluation of apolipoprotein A1 and posttranslationally modified forms of transthyretin as biomarkers for ovarian cancer detection in an independent study population. Cancer Epidemiol Biomarkers Prev. 15:1641–1646. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Ahmed I and Lobo DN: Malignant tumours of the liver. Surgery. 25:34–41. 2009. | |
|
Bruix J and Sherman M; American Association for the Study of Liver Diseases, : Management of hepatocellular carcinoma: An update. Hepatology. 53:1020–1022. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, et al: Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 359:378–390. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Haendler B and Hofer E: Characterization of the human cyclophilin gene and of related processed pseudogenes. Eur J Biochem. 190:477–482. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Holzman TF, Egan DA, Edalji R, Simmer RL, Helfrich R, Taylor A and Burres NS: Preliminary characterization of a cloned neutral isoelectric form of the human peptidyl prolyl isomerase cyclophilin. J Biol Chem. 266:2474–2479. 1991.PubMed/NCBI | |
|
Hoffmann H and Schiene-Fischer C: Functional aspects of extracellular cyclophilins. Biol Chem. 395:721–735. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ramachandran S, Venugopal A, Kutty VR, A V, G D, Chitrasree V, Mullassari A, Pratapchandran NS, Santosh KR, Pillai MR and Kartha CC: Plasma level of cyclophilin A is increased in patients with type 2 diabetes mellitus and suggests presence of vascular disease. Cardiovasc Diabetol. 13:382014. View Article : Google Scholar : PubMed/NCBI | |
|
Wei Y, Jinchuan Y, Yi L, Jun W, Zhongqun W and Cuiping W: Antiapoptotic and proapoptotic signaling of cyclophilin A in endothelial cells. Inflammation. 36:567–572. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kazui T, Inoue N, Yamada O and Komatsu S: Selective cerebral perfusion during operation for aneurysms of the aortic arch: A reassessment. Ann Thorac Surg. 53:109–114. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Nigro P, Pompilio G and Capogrossi MC: Cyclophilin A: A key player for human disease. Cell Death Dis. 4:e8882013. View Article : Google Scholar : PubMed/NCBI | |
|
Brazin KN, Mallis RJ, Fulton DB and Andreotti AH: Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc Natl Acad Sci USA. 99:1899–1904. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Kasinrerk W, Fiebiger E, Stefanová I, Baumruker T, Knapp W and Stockinger H: Human leukocyte activation antigen M6, a member of the Ig superfamily, is the species homologue of rat OX-47, mouse basigin, and chicken HT7 molecule. J Immunol. 149:847–854. 1992.PubMed/NCBI | |
|
Yurchenko V, Constant S and Bukrinsky M: Dealing with the family: CD147 interactions with cyclophilins. Immunology. 117:301–309. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Miyauchi T, Masuzawa Y and Muramatsu T: The basigin group of the immunoglobulin superfamily: Complete conservation of a segment in and around transmembrane domains of human and mouse basigin and chicken HT7 antigen. J Biochem. 110:770–774. 1991. View Article : Google Scholar : PubMed/NCBI | |
|
Kanekura T, Chen X and Kanzaki T: Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metalloproteinases by fibroblasts. Int J Cancer. 99:520–528. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Jin ZG, Lungu AO, Xie L, Wang M, Wong C and Berk BC: Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler Thromb Vasc Biol. 24:1186–1191. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Seko Y, Fujimura T, Taka H, Mineki R, Murayama K and Nagai R: Hypoxia followed by reoxygenation induces secretion of cyclophilin A from cultured rat cardiac myocytes. Biochem Biophys Res Commun. 317:162–168. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Yurchenko V, Zybarth G, O'Connor M, Dai WW, Franchin G, Hao T, Guo H, Hung HC, Toole B, Gallay P, et al: Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J Biol Chem. 277:22959–22965. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Kim SH, Lessner SM, Sakurai Y and Galis ZS: Cyclophilin A as a novel biphasic mediator of endothelial activation and dysfunction. Am J Pathol. 164:1567–1574. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Yang H, Li M, Chai H, Yan S, Lin P, Lumsden AB, Yao Q and Chen C: Effects of cyclophilin A on cell proliferation and gene expressions in human vascular smooth muscle cells and endothelial cells. J Surg Res. 123:312–319. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Obchoei S, Sawanyawisuth K, Wongkham C, Kasinrerk W, Yao Q, Chen C and Wongkham S: Secreted cyclophilin A mediates G1/S phase transition of cholangiocarcinoma cells via CD147/ERK1/2 pathway. Tumour Biol. 36:849–859. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Bauer K, Kretzschmar AK, Cvijic H, Blumert C, Löffler D, Brocke-Heidrich K, Schiene-Fischer C, Fischer G, Sinz A, Clevenger CV and Horn F: Cyclophilins contribute to Stat3 signaling and survival of multiple myeloma cells. Oncogene. 28:2784–2795. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Lee J and Kim SS: Current implications of cyclophilins in human cancers. J Exp Clin Cancer Res. 29:972010. View Article : Google Scholar : PubMed/NCBI | |
|
Ye Y, Huang A, Huang C, Liu J, Wang B, Lin K, Chen Q, Zeng Y, Chen H, Tao X, et al: Comparative mitochondrial proteomic analysis of hepatocellular carcinoma from patients. Proteomics Clin Appl. 7:403–415. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W and Selbach M: Global quantification of mammalian gene expression control. Nature. 473:337–342. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W and Selbach M: Corrigendum: Global quantification of mammalian gene expression control. Nature. 495:126–127. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Li JJ and Biggin MD: Gene expression. Statistics requantitates the central dogma. Science. 347:1066–1067. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Morimoto S and Yahara K: Identification of stress responsive genes by studying specific relationships between mRNA and protein abundance. Heliyon. 4:e005582018. View Article : Google Scholar : PubMed/NCBI | |
|
Liu Y, Beyer A and Aebersold R: On the dependency of cellular protein levels on mRNA abundance. Cell. 165:535–550. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A and Chinnaiyan AM: ONCOMINE: A cancer microarray database and integrated data-mining platform. Neoplasia. 6:1–6. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Pan JH, Zhou H, Cooper L, Huang JL, Zhu SB, Zhao XX, Ding H, Pan YL and Rong L: LAYN is a prognostic biomarker and correlated with immune infiltrates in gastric and colon cancers. Front Immunol. 10:62019. View Article : Google Scholar : PubMed/NCBI | |
|
Mizuno H, Kitada K, Nakai K and Sarai A: PrognoScan: A new database for meta-analysis of the prognostic value of genes. BMC Med Genomics. 2:182009. View Article : Google Scholar : PubMed/NCBI | |
|
Chandrashekar DS, Bashel B, Balasubramanya SAH, Creighton CJ, Ponce-Rodriguez I, Chakravarthi BVSK and Varambally S: UALCAN: A portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia. 19:649–658. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Menyhárt O, Nagy Á and Győrffy B: Determining consistent prognostic biomarkers of overall survival and vascular invasion in hepatocellular carcinoma. R Soc Open Sci. 5:1810062018. View Article : Google Scholar : PubMed/NCBI | |
|
Li T, Fan J, Wang B, Traugh N, Chen Q, Liu JS, Li B and Liu XS: TIMER: A web server for comprehensive analysis of tumor-infiltrating immune cells. Cancer Res. 77:e108–e110. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li B, Severson E, Pignon JC, Zhao H, Li T, Novak J, Jiang P, Shen H, Aster JC, Rodig S, et al: Comprehensive analyses of tumor immunity: Implications for cancer immunotherapy. Genome Biol. 17:1742016. View Article : Google Scholar : PubMed/NCBI | |
|
Graef T, Moesta AK, Norman PJ, Abi-Rached L, Vago L, Older Aguilar AM, Gleimer M, Hammond JA, Guethlein LA, Bushnell DA, et al: KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J Exp Med. 206:2557–2572. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Vivian JP, Duncan RC, Berry R, O'Connor GM, Reid HH, Beddoe T, Gras S, Saunders PM, Olshina MA, Widjaja JM, et al: Killer cell immunoglobulin-like receptor 3DL1-mediated recognition of human leukocyte antigen B. Nature. 479:401–405. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Goodridge JP, Burian A, Lee N and Geraghty DE: HLA-F and MHC class I open conformers are ligands for NK cell Ig-like receptors. J Immunol. 191:3553–3562. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Cantoni C, Bottino C, Vitale M, Pessino A, Augugliaro R, Malaspina A, Parolini S, Moretta L, Moretta A and Biassoni R: NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J Exp Med. 189:787–796. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Eissmann P, Beauchamp L, Wooters J, Tilton JC, Long EO and Watzl C: Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood. 105:4722–4729. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Hori S, Nomura T and Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science. 299:1057–1061. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Fontenot JD, Gavin MA and Rudensky AY: Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 4:330–336. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG and Rudensky AY: Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 22:329–341. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Wherry EJ: T cell exhaustion. Nat Immunol. 12:492–499. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Fagerberg L, Hallström BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K, et al: Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics. 13:397–406. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Chevalier F, Depagne J, Hem S, Chevillard S, Bensimon J, Bertrand P and Lebeau J: Accumulation of cyclophilin A isoforms in conditioned medium of irradiated breast cancer cells. Proteomics. 12:1756–1766. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ralhan R, Masui O, Desouza LV, Matta A, Macha M and Siu KW: Identification of proteins secreted by head and neck cancer cell lines using LC-MS/MS: Strategy for discovery of candidate serological biomarkers. Proteomics. 11:2363–2376. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Tian X, Zhao C, Zhu H, She W, Zhang J, Liu J, Li L, Zheng S, Wen YM and Xie Y: Hepatitis B virus (HBV) surface antigen interacts with and promotes cyclophilin a secretion: Possible link to pathogenesis of HBV infection. J Virol. 84:3373–3381. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Igakura T, Kadomatsu K, Taguchi O, Muramatsu H, Kaname T, Miyauchi T, Yamamura K, Arimura K and Muramatsu T: Roles of basigin, a member of the immunoglobulin superfamily, in behavior as to an irritating odor, lymphocyte response, and blood-brain barrier. Biochem Biophys Res Commun. 224:33–36. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Staffler G, Szekeres A, Schütz GJ, Säemann MD, Prager E, Zeyda M, Drbal K, Zlabinger GJ, Stulnig TM and Stockinger H: Selective inhibition of T cell activation via CD147 through novel modulation of lipid rafts. J Immunol. 171:1707–1714. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Lu M, Wu J, Hao ZW, Shang YK, Xu J, Nan G, Li X, Chen ZN and Bian H: Basolateral CD147 induces hepatocyte polarity loss by E-cadherin ubiquitination and degradation in hepatocellular carcinoma progress. Hepatology. 68:317–332. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
de la Iglesia N, Konopka G, Puram SV, Chan JA, Bachoo RM, You MJ, Levy DE, Depinho RA and Bonni A: Identification of a PTEN-regulated STAT3 brain tumor suppressor pathway. Genes Dev. 22:449–462. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao S, Wu L, Kuang Y, Su J, Luo Z, Wang Y, Li J, Zhang J, Chen W, Li F, et al: Downregulation of CD147 induces malignant melanoma cell apoptosis via the regulation of IGFBP2 expression. Int J Oncol. 53:2397–2408. 2018.PubMed/NCBI | |
|
Lee J, Kim JC, Lee SE, Quinley C, Kim H, Herdman S, Corr M and Raz E: Signal transducer and activator of transcription 3 (STAT3) protein suppresses adenoma-to-carcinoma transition in Apcmin/+ mice via regulation of Snail-1 (SNAI) protein stability. J Biol Chem. 287:18182–18189. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Musteanu M, Blaas L, Mair M, Schlederer M, Bilban M, Tauber S, Esterbauer H, Mueller M, Casanova E, Kenner L, et al: Stat3 is a negative regulator of intestinal tumor progression in Apc(Min) mice. Gastroenterology. 138:1003–1011.e1-e5. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Gomez-Rodriguez J, Kraus ZJ and Schwartzberg PL: Tec family kinases Itk and Rlk/Txk in T lymphocytes: Cross-regulation of cytokine production and T-cell fates. FEBS J. 278:1980–1989. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Chongsathidkiet P, Jackson C, Koyama S, Loebel F, Cui X, Farber SH, Woroniecka K, Elsamadicy AA, Dechant CA, Kemeny HR, et al: Sequestration of T cells in bone marrow in the setting of glioblastoma and other intracranial tumors. Nat Med. 24:1459–1468. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Damsker JM, Bukrinsky MI and Constant SL: Preferential chemotaxis of activated human CD4+ T cells by extracellular cyclophilin A. J Leukoc Biol. 82:613–618. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sherry B, Yarlett N, Strupp A and Cerami A: Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc Natl Acad Sci USA. 89:3511–3515. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Xu Q, Leiva MC, Fischkoff SA, Handschumacher RE and Lyttle CR: Leukocyte chemotactic activity of cyclophilin. J Biol Chem. 267:11968–11971. 1992.PubMed/NCBI | |
|
Forsthuber A, Lipp K, Andersen L, Ebersberger S, Graña-Castro ', Ellmeier W, Petzelbauer P, Lichtenberger BM and Loewe R: CXCL5 as regulator of neutrophil function in cutaneous melanoma. J Invest Dermatol. 139:186–194. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Drewes CC, Alves AC, Hebeda CB, Copetti I, Sandri S, Uchiyama MK, Araki K, Guterres SS, Pohlmann AR and Farsky SH: Role of poly(ε-caprolactone) lipid-core nanocapsules on melanoma-neutrophil crosstalk. Int J Nanomedicine. 12:7153–7163. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Hölzel M and Tüting T: Inflammation-induced plasticity in melanoma therapy and metastasis. Trends Immunol. 37:364–374. 2016. View Article : Google Scholar : PubMed/NCBI |
