Pan-Cancer Analysis Reveals PPRC1 as a Novel Prognostic Biomarker in Ovarian Cancer and Hepatocellular Carcinoma
Abstract
1. Introduction
2. Method
2.1. Expression Level of PPRC1
2.2. Prognostic Role of PPRC1
2.3. Correlation of PPRC1 and Tumor Immune Cells
2.4. Relationship between PPRC1 with Checkpoint Genes and Tumor-Stemness Index
2.5. Statistical Analysis
3. Results
3.1. Expression Patterns of PPRC1 in Pan-Cancer
3.2. Prognostic Role of PPRC1 in Pan-Cancer
3.3. Correlation of PPRC1 and Immune Cells
3.4. Relationship between PPRC1 Expression and Immune-Checkpoint Genes
3.5. Relationship between PPRC1 Expression and Tumor-Stemness Score
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Miller, K.D.; Ortiz, A.P.; Pinheiro, P.S.; Bandi, P.; Minihan, A.; Fuchs, H.E.; Martinez Tyson, D.; Tortolero-Luna, G.; Fedewa, S.A.; Jemal, A.M.; et al. Cancer statistics for the US Hispanic/Latino population, 2021. CA Cancer J. Clin. 2021, 71, 466–487. [Google Scholar] [CrossRef] [PubMed]
- Byrd, D.R.; Brierley, J.D.; Baker, T.P.; Sullivan, D.C.; Gress, D.M. Current and future cancer staging after neoadjuvant treatment for solid tumors. CA Cancer J. Clin. 2021, 71, 140–148. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Yu, S.; Feng, C.; Mao, D.; Li, J.; Zhu, X. In Situ Analysis of Cancer Cells Based on DNA Signal Amplification and DNA Nanodevices. Crit. Rev. Anal. Chem. 2021, 51, 8–19. [Google Scholar] [CrossRef] [PubMed]
- Urbanek-Trzeciak, M.O.; Galka-Marciniak, P.; Nawrocka, P.M.; Kowal, E.; Szwec, S.; Giefing, M.; Kozlowski, P. Pan-cancer analysis of somatic mutations in miRNA genes. EBioMedicine 2020, 61, 103051. [Google Scholar] [CrossRef]
- Liu, J.; Wang, Y.; Yin, J.; Yang, Y.; Geng, R.; Zhong, Z.; Ni, S.; Liu, W.; Du, M.; Yu, H.; et al. Pan-Cancer Analysis Revealed SRSF9 as a New Biomarker for Prognosis and Immunotherapy. J. Oncol. 2022, 2022, 3477148. [Google Scholar] [CrossRef]
- Luo, C.; Widlund, H.R.; Puigserver, P. PGC-1 Coactivators: Shepherding the Mitochondrial Biogenesis of Tumors. Trends Cancer 2016, 2, 619–631. [Google Scholar] [CrossRef][Green Version]
- Puigserver, P.; Wu, Z.; Park, C.W.; Graves, R.; Wright, M.; Spiegelman, B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92, 829–839. [Google Scholar] [CrossRef][Green Version]
- Singh, F.; Zoll, J.; Duthaler, U.; Charles, A.L.; Panajatovic, M.V.; Laverny, G.; McWilliams, T.G.; Metzger, D.; Geny, B.; Krähenbühl, S.; et al. PGC-1β modulates statin-associated myotoxicity in mice. Arch. Toxicol. 2019, 93, 487–504. [Google Scholar] [CrossRef][Green Version]
- Chambers, J.M.; Wingert, R.A. PGC-1α in Disease: Recent Renal Insights into a Versatile Metabolic Regulator. Cells 2020, 9, 2234. [Google Scholar] [CrossRef]
- Victorino, V.J.; Barroso, W.A.; Assunção, A.K.; Cury, V.; Jeremias, I.C.; Petroni, R.; Chausse, B.; Ariga, S.K.; Herrera, A.C.; Panis, C.; et al. PGC-1β regulates HER2-overexpressing breast cancer cells proliferation by metabolic and redox pathways. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 2016, 37, 6035–6044. [Google Scholar] [CrossRef]
- Li, Y.; Kasim, V.; Yan, X.; Li, L.; Meliala, I.T.S.; Huang, C.; Li, Z.; Lei, K.; Song, G.; Zheng, X.; et al. Yin Yang 1 facilitates hepatocellular carcinoma cell lipid metabolism and tumor progression by inhibiting PGC-1β-induced fatty acid oxidation. Theranostics 2019, 9, 7599–7615. [Google Scholar] [CrossRef]
- Wang, H.; Yan, X.; Ji, L.Y.; Ji, X.T.; Wang, P.; Guo, S.W.; Li, S.Z. miR-139 Functions as An Antioncomir to Repress Glioma Progression Through Targeting IGF-1 R, AMY-1, and PGC-1β. Technol. Cancer Res. Treat. 2017, 16, 497–511. [Google Scholar] [CrossRef][Green Version]
- Mori, M.P.; Souza-Pinto, N.C. PPRC1, but not PGC-1α, levels directly correlate with expression of mitochondrial proteins in human dermal fibroblasts. Genet. Mol. Biol. 2020, 43 (Suppl. 1), e20190083. [Google Scholar] [CrossRef]
- Cribbs, A.P.; Terlecki-Zaniewicz, S.; Philpott, M.; Baardman, J.; Ahern, D.; Lindow, M.; Obad, S.; Oerum, H.; Sampey, B.; Mander, P.K.; et al. Histone H3K27me3 demethylases regulate human Th17 cell development and effector functions by impacting on metabolism. Proc. Natl. Acad. Sci. USA 2020, 117, 6056–6066. [Google Scholar] [CrossRef][Green Version]
- Tsai, H.F.; Chang, Y.C.; Li, C.H.; Chan, M.H.; Chen, C.L.; Tsai, W.C.; Hsiao, M. Type V collagen alpha 1 chain promotes the malignancy of glioblastoma through PPRC1-ESM1 axis activation and extracellular matrix remodeling. Cell Death Discov. 2021, 7, 313. [Google Scholar] [CrossRef]
- Yu, G.; Wang, L.G.; Han, Y.; He, Q.Y. clusterProfiler: An R package for comparing biological themes among gene clusters. Omics A J. Integr. Biol. 2012, 16, 284–287. [Google Scholar] [CrossRef]
- Mou, C.; Liu, B.; Wang, M.; Jiang, M.; Han, T. PGC-1-related coactivator (PRC) is an important regulator of microglia M2 polarization. J. Mol. Neurosci. MN 2015, 55, 69–75. [Google Scholar] [CrossRef]
- Ge, R.; Fang, H.F.; Chang, Y.Q.; Li, Z.; Liu, C.F. Clinicopathological features of polymorphous low-grade neuroepithelial tumor of the young. Zhonghua Bing Li Xue Za Zhi Chin. J. Pathol. 2020, 49, 1131–1135. [Google Scholar]
- Cui, G.; Wang, C.; Lin, Z.; Feng, X.; Wei, M.; Miao, Z.; Sun, Z.; Wei, F. Prognostic and immunological role of Ras-related protein Rap1b in pan-cancer. Bioengineered 2021, 12, 4828–4840. [Google Scholar] [CrossRef]
- Malta, T.M.; Sokolov, A.; Gentles, A.J.; Burzykowski, T.; Poisson, L.; Weinstein, J.N.; Kamińska, B.; Huelsken, J.; Omberg, L.; Gevaert, O.; et al. Machine Learning Identifies Stemness Features Associated with Oncogenic Dedifferentiation. Cell 2018, 173, 338–354.e315. [Google Scholar] [CrossRef][Green Version]
- Hou, G.X.; Liu, P.; Yang, J.; Wen, S. Mining expression and prognosis of topoisomerase isoforms in non-small-cell lung cancer by using Oncomine and Kaplan-Meier plotter. PLoS ONE 2017, 12, e0174515. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Lv, Z.; Qi, L.; Hu, X.; Mo, M.; Jiang, H.; Fan, B.; Li, Y. Zic Family Member 2 (ZIC2): A Potential Diagnostic and Prognostic Biomarker for Pan-Cancer. Front. Mol. Biosci. 2021, 8, 631067. [Google Scholar] [CrossRef] [PubMed]
- Lei, X.; Lei, Y.; Li, J.K.; Du, W.X.; Li, R.G.; Yang, J.; Li, J.; Li, F.; Tan, H.B. Immune cells within the tumor microenvironment: Biological functions and roles in cancer immunotherapy. Cancer Lett. 2020, 470, 126–133. [Google Scholar] [CrossRef]
- Soularue, E.; Lepage, P.; Colombel, J.F.; Coutzac, C.; Faleck, D.; Marthey, L.; Collins, M.; Chaput, N.; Robert, C.; Carbonnel, F. Enterocolitis due to immune checkpoint inhibitors: A systematic review. Gut 2018, 67, 2056–2067. [Google Scholar] [CrossRef] [PubMed]
- Hargadon, K.M.; Johnson, C.E.; Williams, C.J. Immune checkpoint blockade therapy for cancer: An overview of FDA-approved immune checkpoint inhibitors. Int. Immunopharmacol. 2018, 62, 29–39. [Google Scholar] [CrossRef]
- Hoos, A. Development of immuno-oncology drugs—From CTLA4 to PD1 to the next generations. Nat. Rev. Drug Discov. 2016, 15, 235–247. [Google Scholar] [CrossRef]
- Lytle, N.K.; Barber, A.G.; Reya, T. Stem cell fate in cancer growth, progression and therapy resistance. Nat. Rev. Cancer 2018, 18, 669–680. [Google Scholar] [CrossRef]
- Huss, J.M.; Torra, I.P.; Staels, B.; Giguère, V.; Kelly, D.P. Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 2004, 24, 9079–9091. [Google Scholar] [CrossRef][Green Version]
- Alaynick, W.A. Nuclear receptors, mitochondria and lipid metabolism. Mitochondrion 2008, 8, 329–337. [Google Scholar] [CrossRef][Green Version]
- Kemper, M.F.; Zhao, Y.; Duckles, S.P.; Krause, D.N. Endogenous ovarian hormones affect mitochondrial efficiency in cerebral endothelium via distinct regulation of PGC-1 isoforms. J. Cereb. Blood Flow Metab. 2013, 33, 122–128. [Google Scholar] [CrossRef][Green Version]
- Anderson, N.R.; Minutolo, N.G.; Gill, S.; Klichinsky, M. Macrophage-Based Approaches for Cancer Immunotherapy. Cancer Res. 2021, 81, 1201–1208. [Google Scholar] [CrossRef]
- Wei, F.; Zhang, T.; Deng, S.C.; Wei, J.C.; Yang, P.; Wang, Q.; Chen, Z.P.; Li, W.L.; Chen, H.C.; Hu, H.; et al. PD-L1 promotes colorectal cancer stem cell expansion by activating HMGA1-dependent signaling pathways. Cancer Lett. 2019, 450, 1–13. [Google Scholar] [CrossRef]
- Santoni, M.; Massari, F.; Montironi, R.; Battelli, N. Manipulating macrophage polarization in cancer patients: From nanoparticles to human chimeric antigen receptor macrophages. Biochim. Biophys. Acta Rev. Cancer 2021, 1876, 188547. [Google Scholar] [CrossRef]
- Giese, M.A.; Hind, L.E.; Huttenlocher, A. Neutrophil plasticity in the tumor microenvironment. Blood 2019, 133, 2159–2167. [Google Scholar] [CrossRef]
- Lee, Y.S.; Radford, K.J. The role of dendritic cells in cancer. Int. Rev. Cell Mol. Biol. 2019, 348, 123–178. [Google Scholar]
- Swann, J.B.; Smyth, M.J. Immune surveillance of tumors. J. Clin. Investig. 2007, 117, 1137–1146. [Google Scholar] [CrossRef][Green Version]
- Li, B.; Chan, H.L.; Chen, P. Immune Checkpoint Inhibitors: Basics and Challenges. Curr. Med. Chem. 2019, 26, 3009–3025. [Google Scholar] [CrossRef]
- Iwai, Y.; Hamanishi, J.; Chamoto, K.; Honjo, T. Cancer immunotherapies targeting the PD-1 signaling pathway. J. Biomed. Sci. 2017, 24, 26. [Google Scholar] [CrossRef][Green Version]
- Chen, D.; Menon, H.; Verma, V.; Guo, C.; Ramapriyan, R.; Barsoumian, H.; Younes, A.; Hu, Y.; Wasley, M.; Cortez, M.A.; et al. Response and outcomes after anti-CTLA4 versus anti-PD1 combined with stereotactic body radiation therapy for metastatic non-small cell lung cancer: Retrospective analysis of two single-institution prospective trials. J. Immunother. Cancer 2020, 8, e000492. [Google Scholar] [CrossRef][Green Version]
- Zeng, D.; Li, M.; Zhou, R.; Zhang, J.; Sun, H.; Shi, M.; Bin, J.; Liao, Y.; Rao, J.; Liao, W. Tumor Microenvironment Characterization in Gastric Cancer Identifies Prognostic and Immunotherapeutically Relevant Gene Signatures. Cancer Immunol. Res. 2019, 7, 737–750. [Google Scholar] [CrossRef][Green Version]
Clinicopathological Characteristics | Ovarian Cancer (Overall Survival, n = 1657) | Liver Cancer (Overall Survival, n = 364) | ||||
---|---|---|---|---|---|---|
N | HR | p-Value | N | HR | p-Value | |
Stage | ||||||
1 | 107 | 2.51 (0.75–8.34) | 0.12 | 170 | 0.74 (0.4–1.37) | 0.34 |
2 | 61 | 6.21 (1.96–19.72) | 0.0004 | 83 | 0.48 (0.21–1.07) | 0.065 |
3 | 1044 | 1.11 (0.94–1.31) | 0.22 | 83 | 2.22 (1.12–4.4) | 0.02 |
4 | 176 | 1.7 (1.1–2.62) | 0.015 | 4 | Ns | Ns |
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Ruan, X.; Cui, G.; Li, C.; Sun, Z. Pan-Cancer Analysis Reveals PPRC1 as a Novel Prognostic Biomarker in Ovarian Cancer and Hepatocellular Carcinoma. Medicina 2023, 59, 784. https://doi.org/10.3390/medicina59040784
Ruan X, Cui G, Li C, Sun Z. Pan-Cancer Analysis Reveals PPRC1 as a Novel Prognostic Biomarker in Ovarian Cancer and Hepatocellular Carcinoma. Medicina. 2023; 59(4):784. https://doi.org/10.3390/medicina59040784
Chicago/Turabian StyleRuan, Xingqiu, Guoliang Cui, Changyu Li, and Zhiguang Sun. 2023. "Pan-Cancer Analysis Reveals PPRC1 as a Novel Prognostic Biomarker in Ovarian Cancer and Hepatocellular Carcinoma" Medicina 59, no. 4: 784. https://doi.org/10.3390/medicina59040784
APA StyleRuan, X., Cui, G., Li, C., & Sun, Z. (2023). Pan-Cancer Analysis Reveals PPRC1 as a Novel Prognostic Biomarker in Ovarian Cancer and Hepatocellular Carcinoma. Medicina, 59(4), 784. https://doi.org/10.3390/medicina59040784