43
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

PVALB Was Identified as an Independent Prognostic Factor for HCC Closely Related to Immunity, and Its Absence Accelerates Tumor Progression by Regulating NK Cell Infiltration

, , , , , , , , & ORCID Icon show all
Pages 813-838 | Received 30 Nov 2023, Accepted 23 Apr 2024, Published online: 07 May 2024

References

  • Asafo-Agyei KO, Samant H. Hepatocellular carcinoma. In: StatPearls. StatPearls Publishing Copyright © 2023, StatPearls Publishing LLC.; 2023.
  • Piñero F, Dirchwolf M, Pessôa MG. Biomarkers in hepatocellular carcinoma: diagnosis, prognosis and treatment response assessment. Cells. 2020;9(6). doi:10.3390/cells9061370
  • Wang W, Wei C. Advances in the early diagnosis of hepatocellular carcinoma. Genes Dis. 2020;7(3):308–319. doi:10.1016/j.gendis.2020.01.014
  • Mak LY, Cruz-Ramón V, Chinchilla-López P, et al. Global epidemiology, prevention, and management of hepatocellular carcinoma. Am Soc Clin Oncol Educ Book. 2018;38:262–279. doi:10.1200/edbk_200939
  • Bruix J, Castells A, Bosch J, et al. Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology. 1996;111(4):1018–1022. doi:10.1016/s0016-5085(96)70070-7
  • Shlomai A, de Jong YP, Rice CM. Virus associated malignancies: the role of viral hepatitis in hepatocellular carcinoma. Semin Cancer Biol. 2014;26:78–88. doi:10.1016/j.semcancer.2014.01.004
  • Villalba M, Rathore MG, Lopez-Royuela N, Krzywinska E, Garaude J, Allende-Vega N. From tumor cell metabolism to tumor immune escape. Int J Biochem Cell Biol. 2013;45(1):106–113. doi:10.1016/j.biocel.2012.04.024
  • Ritzler JM, Berchtold MW. An STS in the human parvalbumin gene (PVALB). Nucleic Acids Res. 1992;20(6):1428. doi:10.1093/nar/20.6.1428-A
  • Wang W, Martindale J, Metzger JM. Parvalbumin: targeting calcium handling in cardiac diastolic dysfunction. Gen Physiol Biophys. 2009;28:F3–6.
  • Schwaller B. Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol. 2010;2(11):a004051. doi:10.1101/cshperspect.a004051
  • Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4(7):517–529. doi:10.1038/nrm1155
  • Gifford JL, Walsh MP, Vogel HJ. Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J. 2007;405(2):199–221. doi:10.1042/bj20070255
  • Grabarek Z. Structural basis for diversity of the EF-hand calcium-binding proteins. J Mol Biol. 2006;359(3):509–525. doi:10.1016/j.jmb.2006.03.066
  • Schwaller B, Tetko IV, Tandon P, et al. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol Cell Neurosci. 2004;25(4):650–663. doi:10.1016/j.mcn.2003.12.006
  • Olinger E, Schwaller B, Loffing J, Gailly P, Devuyst O. Parvalbumin: calcium and magnesium buffering in the distal nephron. Nephrol Dial Transplant. 2012;27(11):3988–3994. doi:10.1093/ndt/gfs457
  • Mendes TB, Nozima BH, Budu A, et al. PVALB diminishes [Ca2+] and alters mitochondrial features in follicular thyroid carcinoma cells through AKT/GSK3β pathway. Endocr Relat Cancer. 2016;23(9):769–782. doi:10.1530/erc-16-0181
  • Chen YT, Tu JJ, Kao J, Zhou XK, Mazumdar M. Messenger RNA expression ratios among four genes predict subtypes of renal cell carcinoma and distinguish oncocytoma from carcinoma. Clin Cancer Res. 2005;11(18):6558–6566. doi:10.1158/1078-0432.Ccr-05-0647
  • Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinf. 2008;9:559. doi:10.1186/1471-2105-9-559
  • Chandrashekar DS, Bashel B, Balasubramanya SAH, et al. UALCAN: a portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia. 2017;19(8):649–658. doi:10.1016/j.neo.2017.05.002
  • Modhukur V, Iljasenko T, Metsalu T, Lokk K, Laisk-Podar T, Vilo J. MethSurv: a web tool to perform multivariable survival analysis using DNA methylation data. Epigenomics. 2018;10(3):277–288. doi:10.2217/epi-2017-0118
  • Li Y, Ge D, Lu C. The SMART App: an interactive web application for comprehensive DNA methylation analysis and visualization. Epigenet Chromatin. 2019;12(1):71. doi:10.1186/s13072-019-0316-3
  • Lánczky A, Győrffy B. Web-based survival analysis tool tailored for medical research (KMplot): development and implementation. J Med Internet Res. 2021;23(7):e27633. doi:10.2196/27633
  • Vasaikar SV, Straub P, Wang J, Zhang B. LinkedOmics: analyzing multi-omics data within and across 32 cancer types. Nucleic Acids Res. 2018;46(D1):D956–d963. doi:10.1093/nar/gkx1090
  • Li T, Fan J, Wang B, et al. TIMER: a web server for comprehensive analysis of tumor-infiltrating immune cells. Cancer Res. 2017;77(21):e108–e110. doi:10.1158/0008-5472.Can-17-0307
  • Ru B, Wong CN, Tong Y, et al. TISIDB: an integrated repository portal for tumor-immune system interactions. Bioinformatics. 2019;35(20):4200–4202. doi:10.1093/bioinformatics/btz210
  • Garcia DM, Baek D, Shin C, Bell GW, Grimson A, Bartel DP. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat Struct Mol Biol. 2011;18(10):1139–1146. doi:10.1038/nsmb.2115
  • Alexiou P, Maragkakis M, Papadopoulos GL, Simmosis VA, Zhang L, Hatzigeorgiou AG. The DIANA-mirExTra web server: from gene expression data to microRNA function. PLoS One. 2010;5(2):e9171. doi:10.1371/journal.pone.0009171
  • Miao YR, Liu W, Zhang Q, Guo AY. lncRNASNP2: an updated database of functional SNPs and mutations in human and mouse lncRNAs. Nucleic Acids Res. 2018;46(D1):D276–d280. doi:10.1093/nar/gkx1004
  • Warde-Farley D, Donaldson SL, Comes O, et al. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 2010;38:W214–20. doi:10.1093/nar/gkq537
  • Gao J, Aksoy BA, Dogrusoz U, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6(269):pl1. doi:10.1126/scisignal.2004088
  • Waterhouse A, Bertoni M, Bienert S, et al. Swiss-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296–w303. doi:10.1093/nar/gky427
  • Guex N, Peitsch MC, Schwede T. Automated comparative protein structure modeling with Swiss-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis. 2009;30(Suppl 1):S162–73. doi:10.1002/elps.200900140
  • Bienert S, Waterhouse A, de Beer TA, et al. The Swiss-MODEL repository-new features and functionality. Nucleic Acids Res. 2017;45(D1):D313–d319. doi:10.1093/nar/gkw1132
  • David A, Islam S, Tankhilevich E, Sternberg MJE. The alphafold database of protein structures: a biologist’s guide. J Mol Biol. 2022;434(2):167336. doi:10.1016/j.jmb.2021.167336
  • Remmert M, Biegert A, Hauser A, Söding J. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Methods. 2011;9(2):173–175. doi:10.1038/nmeth.1818
  • Davis AP, Grondin CJ, Johnson RJ, et al. Comparative Toxicogenomics Database (CTD): update 2021. Nucleic Acids Res. 2021;49(D1):D1138–d1143. doi:10.1093/nar/gkaa891
  • Liu CJ, Hu FF, Xie GY, et al. GSCA: an integrated platform for gene set cancer analysis at genomic, pharmacogenomic and immunogenomic levels. Brief Bioinform. 2023;24(1). doi:10.1093/bib/bbac558
  • Kirby ED, Kuwahara AA, Messer RL, Wyss-Coray T. Adult hippocampal neural stem and progenitor cells regulate the neurogenic niche by secreting VEGF. Proc Natl Acad Sci U S A. 2015;112(13):4128–4133. doi:10.1073/pnas.1422448112
  • Ahn HR, Baek GO, Yoon MG, et al. Hypomethylation-mediated upregulation of the WASF2 promoter region correlates with poor clinical outcomes in hepatocellular carcinoma. J Exp Clin Cancer Res. 2022;41(1):158. doi:10.1186/s13046-022-02365-7
  • Hernandez-Meza G, von Felden J, Gonzalez-Kozlova EE, et al. DNA methylation profiling of human hepatocarcinogenesis. Hepatology. 2021;74(1):183–199. doi:10.1002/hep.31659
  • Gao F, Xie K, Xiang Q, et al. The density of tumor-infiltrating lymphocytes and prognosis in resectable hepatocellular carcinoma: a two-phase study. Aging. 2021;13(7):9665–9678. doi:10.18632/aging.202710
  • Wang J, Liu X, Wu H, et al. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res. 2010;38(16):5366–5383. doi:10.1093/nar/gkq285
  • Huang G, Liang M, Liu H, et al. CircRNA hsa_circRNA_104348 promotes hepatocellular carcinoma progression through modulating miR-187-3p/RTKN2 axis and activating Wnt/β-catenin pathway. Cell Death Dis. 2020;11(12):1065. doi:10.1038/s41419-020-03276-1
  • Zhang Y, Zhang Z. The history and advances in cancer immunotherapy: understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell Mol Immunol. 2020;17(8):807–821. doi:10.1038/s41423-020-0488-6
  • Bai Y, Cao K, Zhang P, Ma J, Zhu J. Prognostic and Immunological Implications of FAM72A in pan-cancer and functional validations. Int J Mol Sci. 2022;24(1). doi:10.3390/ijms24010375
  • Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86. doi:10.1002/ijc.29210
  • Roayaie S, Jibara G, Tabrizian P, et al. The role of hepatic resection in the treatment of hepatocellular cancer. Hepatology. 2015;62(2):440–451. doi:10.1002/hep.27745
  • Bruix J, Takayama T, Mazzaferro V, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a Phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2015;16(13):1344–1354. doi:10.1016/s1470-2045(15)00198-9
  • Au KP, Chok KSH. Multidisciplinary approach for post-liver transplant recurrence of hepatocellular carcinoma: a proposed management algorithm. World J Gastroenterol. 2018;24(45):5081–5094. doi:10.3748/wjg.v24.i45.5081
  • Xu Z, Xie H, Zhou L, Chen X, Zheng S. The combination strategy of transarterial chemoembolization and radiofrequency ablation or microwave ablation against hepatocellular carcinoma. Anal Cell Pathol. 2019;2019:8619096. doi:10.1155/2019/8619096
  • Nordness MF, Hamel S, Godfrey CM, et al. Fatal hepatic necrosis after nivolumab as a bridge to liver transplant for HCC: are checkpoint inhibitors safe for the pretransplant patient? Am J Transplant. 2020;20(3):879–883. doi:10.1111/ajt.15617
  • Liang W, Wang D, Ling X, et al. Sirolimus-based immunosuppression in liver transplantation for hepatocellular carcinoma: a meta-analysis. Liver Transpl. 2012;18(1):62–69. doi:10.1002/lt.22441
  • Lencioni R, de Baere T, Soulen MC, Rilling WS, Geschwind JF. Lipiodol transarterial chemoembolization for hepatocellular carcinoma: a systematic review of efficacy and safety data. Hepatology. 2016;64(1):106–116. doi:10.1002/hep.28453
  • Das S, Camphausen K, Shankavaram U. Cancer-specific immune prognostic signature in solid tumors and its relation to immune checkpoint therapies. Cancers. 2020;12(9). doi:10.3390/cancers12092476
  • Li T, Yan Z, Wang W, et al. SEMA6B overexpression predicts poor prognosis and correlates with the tumor immunosuppressive microenvironment in colorectal cancer. Front Mol Biosci. 2021;8:687319. doi:10.3389/fmolb.2021.687319
  • Mossanen JC, Kohlhepp M, Wehr A, et al. CXCR6 inhibits hepatocarcinogenesis by promoting natural killer T- and CD4(+) T-cell-dependent control of senescence. Gastroenterology. 2019;156(6):1877–1889.e4. doi:10.1053/j.gastro.2019.01.247
  • Zhang Q, Lou Y, Yang J, et al. Integrated multiomic analysis reveals comprehensive tumour heterogeneity and novel immunophenotypic classification in hepatocellular carcinomas. Gut. 2019;68(11):2019–2031. doi:10.1136/gutjnl-2019-318912
  • Ally A, Balasundaram M, Carlsen R, et al. Comprehensive and integrative genomic characterization of hepatocellular carcinoma. Cell. 2017;169(7):1327–1341.e23. doi:10.1016/j.cell.2017.05.046
  • Chew V, Lai L, Pan L, et al. Delineation of an immunosuppressive gradient in hepatocellular carcinoma using high-dimensional proteomic and transcriptomic analyses. Proc Natl Acad Sci U S A. 2017;114(29):E5900–e5909. doi:10.1073/pnas.1706559114
  • Itoh S, Yoshizumi T, Yugawa K, et al. Impact of immune response on outcomes in hepatocellular carcinoma: association with vascular formation. Hepatology. 2020;72(6):1987–1999. doi:10.1002/hep.31206
  • Zhang Q, He Y, Luo N, et al. Landscape and dynamics of single immune cells in hepatocellular carcinoma. Cell. 2019;179(4):829–845.e20. doi:10.1016/j.cell.2019.10.003
  • Sun H, Huang Q, Huang M, et al. Human CD96 correlates to natural killer cell exhaustion and predicts the prognosis of human hepatocellular carcinoma. Hepatology. 2019;70(1):168–183. doi:10.1002/hep.30347
  • Zhou J, Peng H, Li K, et al. Liver-resident NK cells control antiviral activity of hepatic T Cells via the PD-1-PD-L1 Axis. Immunity. 2019;50(2):403–417.e4. doi:10.1016/j.immuni.2018.12.024
  • Ma H, Kang Z, Foo TK, Shen Z, Xia B. Disrupted BRCA1-PALB2 interaction induces tumor immunosuppression and T-lymphocyte infiltration in HCC through cGAS-STING pathway. Hepatology. 2023;77(1):33–47. doi:10.1002/hep.32335
  • Zhang PF, Gao C, Huang XY, et al. Cancer cell-derived exosomal circUHRF1 induces natural killer cell exhaustion and may cause resistance to anti-PD1 therapy in hepatocellular carcinoma. Mol Cancer. 2020;19(1):110. doi:10.1186/s12943-020-01222-5
  • Hoechst B, Voigtlaender T, Ormandy L, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 2009;50(3):799–807. doi:10.1002/hep.23054
  • Qin WH, Yang ZS, Li M, et al. High serum levels of cholesterol increase antitumor functions of nature killer cells and reduce growth of liver tumors in mice. Gastroenterology. 2020;158(6):1713–1727. doi:10.1053/j.gastro.2020.01.028
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.013
  • Voskoboinik I, Smyth MJ, Trapani JA. Perforin-mediated target-cell death and immune homeostasis. Nat Rev Immunol. 2006;6(12):940–952. doi:10.1038/nri1983
  • Guillerey C, Huntington ND, Smyth MJ. Targeting natural killer cells in cancer immunotherapy. Nat Immunol. 2016;17(9):1025–1036. doi:10.1038/ni.3518
  • Habif G, Crinier A, André P, Vivier E, Narni-Mancinelli E. Targeting natural killer cells in solid tumors. Cell Mol Immunol. 2019;16(5):415–422. doi:10.1038/s41423-019-0224-2
  • Prager I, Watzl C. Mechanisms of natural killer cell-mediated cellular cytotoxicity. J Leukoc Biol. 2019;105(6):1319–1329. doi:10.1002/jlb.Mr0718-269r
  • Prager I, Liesche C, van Ooijen H, et al. NK cells switch from granzyme B to death receptor-mediated cytotoxicity during serial killing. J Exp Med. 2019;216(9):2113–2127. doi:10.1084/jem.20181454
  • Sordo-Bahamonde C, Lorenzo-Herrero S, González S, López-Soto A. A cytofluorimetric assay to evaluate intracellular cytokine production by NK cells. Methods Enzymol. 2020;631:343–355. doi:10.1016/bs.mie.2019.05.049
  • Que ZJ, Yao JL, Zhou ZY, et al. Jinfukang inhibits lung cancer metastasis by upregulating CX3CL1 to recruit NK cells to kill CTCs. J Ethnopharmacol. 2021;275:114175. doi:10.1016/j.jep.2021.114175
  • Strand S, Hofmann WJ, Hug H, et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells--A mechanism of immune evasion? Nat Med. 1996;2(12):1361–1366. doi:10.1038/nm1296-1361
  • Liu E, Marin D, Banerjee P, et al. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020;382(6):545–553. doi:10.1056/NEJMoa1910607
  • Robin X, Turck N, Hainard A, et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinf. 2011;12:77. doi:10.1186/1471-2105-12-77
  • Liu XH, Sun M, Nie FQ, et al. Lnc RNA HOTAIR functions as a competing endogenous RNA to regulate HER2 expression by sponging miR-331-3p in gastric cancer. Mol Cancer. 2014;13:92. doi:10.1186/1476-4598-13-92
  • Wang SH, Ma F, Tang ZH, et al. Long non-coding RNA H19 regulates FOXM1 expression by competitively binding endogenous miR-342-3p in gallbladder cancer. J Exp Clin Cancer Res. 2016;35(1):160. doi:10.1186/s13046-016-0436-6