Multi-Omics Approach Reveals Redox Homeostasis Reprogramming in Early-Stage Clear Cell Renal Cell Carcinoma
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Design and Tissue Specimens
2.2. Irreversible Biotinylation Procedure (IBP)
2.3. SNO-Proteome
2.4. Liquid Chromatography Triple Quadrupole Mass Spectrometry (LC-MS/MS) Analysis
2.5. Identification and Measurement of Proteins
2.6. REME
2.7. Data Processing and Analysis for Proteomics and SNO-Proteome
2.8. REME Data Processing and Analysis
3. Results
3.1. Proteomic and SNO-Proteome Landscape of ccRCC
3.2. Signature Proteins and SNO Peptides in ccRCC Tissues
3.3. Molecular Patterns of Independently Differentially Expressed SNO Proteins
3.4. REME Profiled the Redox Homeostasis Reprogramming of ccRCC
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2019. CA Cancer J. Clin. 2019, 69, 7–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernández-Pello, S.; Hofmann, F.; Tahbaz, R.; Marconi, L.; Lam, T.B.; Albiges, L.; Bensalah, K.; Canfield, S.E.; Dabestani, S.; Giles, R.H.; et al. A Systematic Review and Meta-analysis Comparing the Effectiveness and Adverse Effects of Different Systemic Treatments for Non-clear Cell Renal Cell Carcinoma. Eur. Urol. 2017, 71, 426–436. [Google Scholar] [CrossRef] [PubMed]
- Wettersten, H.I.; Aboud, O.A.; Lara, P.N., Jr.; Weiss, R.H. Metabolic reprogramming in clear cell renal cell carcinoma. Nat. Rev. Nephrol. 2017, 13, 410–419. [Google Scholar] [CrossRef]
- Linehan, W.M.; Srinivasan, R.; Schmidt, L.S. The genetic basis of kidney cancer: A metabolic disease. Nat. Rev. Urol. 2010, 7, 277–285. [Google Scholar] [CrossRef]
- Pavlova, N.N.; Thompson, C.B. The Emerging Hallmarks of Cancer Metabolism. Cell Metab. 2016, 23, 27–47. [Google Scholar] [CrossRef] [Green Version]
- DeBerardinis, R.J.; Chandel, N.S. Fundamentals of cancer metabolism. Sci. Adv. 2016, 2, e1600200. [Google Scholar] [CrossRef] [Green Version]
- Hornsveld, M.; Dansen, T.B. The Hallmarks of Cancer from a Redox Perspective. Antioxid. Redox Signal. 2016, 25, 300–325. [Google Scholar] [CrossRef] [PubMed]
- Wei, X.; Deng, W.; Dong, Z.; Luo, Y.; Hu, X.; Zhang, J.; Xie, Z.; Zheng, T.; Tan, Y.; Tang, Z.; et al. Redox Metabolism-Associated Molecular Classification of Clear Cell Renal Cell Carcinoma. Oxidative Med. Cell. Longev. 2022, 2022, 5831247. [Google Scholar] [CrossRef]
- Xia, Q.D.; Yang, X.; Lu, J.L.; Liu, C.Q.; Sun, J.X.; Li, C.; Wang, S.G. Development and Validation of a Nine-Redox-Related Long Noncoding RNA Signature in Renal Clear Cell Carcinoma. Oxidative Med. Cell. Longev. 2020, 2020, 6634247. [Google Scholar] [CrossRef]
- Network, C.G.A.R. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013, 499, 43–49. [Google Scholar] [CrossRef]
- Clark, D.J.; Dhanasekaran, S.M.; Petralia, F.; Pan, J.; Song, X.; Hu, Y.; da Veiga Leprevost, F.; Reva, B.; Lih, T.M.; Chang, H.Y.; et al. Integrated Proteogenomic Characterization of Clear Cell Renal Cell Carcinoma. Cell 2019, 179, 964–983.e931. [Google Scholar] [CrossRef] [Green Version]
- Foster, M.W.; Hess, D.T.; Stamler, J.S. Protein S-nitrosylation in health and disease: A current perspective. Trends Mol. Med. 2009, 15, 391–404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hess, D.T.; Matsumoto, A.; Kim, S.O.; Marshall, H.E.; Stamler, J.S. Protein S-nitrosylation: Purview and parameters. Nat. Rev. Mol. Cell Biol. 2005, 6, 150–166. [Google Scholar] [CrossRef]
- Plenchette, S.; Romagny, S.; Laurens, V.; Bettaieb, A. S-Nitrosylation in TNF superfamily signaling pathway: Implication in cancer. Redox Biol. 2015, 6, 507–515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cai, W.B.; Zhao, Y.J.; Liu, L.; Cheng, Q.; Wang, J.; Shi, X.L.; Yao, L.; Qiao, X.H.; Zhu, Y.; Chen, C.; et al. Redox environment metabolomic evaluation (REME) of the heart after myocardial ischemia/reperfusion injury. Free Radic. Biol. Med. 2021, 173, 7–18. [Google Scholar] [CrossRef] [PubMed]
- van der Reest, J.; Lilla, S.; Zheng, L.; Zanivan, S.; Gottlieb, E. Proteome-wide analysis of cysteine oxidation reveals metabolic sensitivity to redox stress. Nat. Commun. 2018, 9, 1581. [Google Scholar] [CrossRef] [Green Version]
- Yi, W.; Zhang, Y.; Liu, B.; Zhou, Y.; Liao, D.; Qiao, X.; Gao, D.; Xie, T.; Yao, Q.; Zhang, Y.; et al. Protein S-nitrosylation regulates proteostasis and viability of hematopoietic stem cell during regeneration. Cell Rep. 2021, 34, 108922. [Google Scholar] [CrossRef]
- Mnatsakanyan, R.; Markoutsa, S.; Walbrunn, K.; Roos, A.; Verhelst, S.H.L.; Zahedi, R.P. Proteome-wide detection of S-nitrosylation targets and motifs using bioorthogonal cleavable-linker-based enrichment and switch technique. Nat. Commun. 2019, 10, 2195. [Google Scholar] [CrossRef] [Green Version]
- Jiang, Y.; Sun, A.; Zhao, Y.; Ying, W.; Sun, H.; Yang, X.; Xing, B.; Sun, W.; Ren, L.; Hu, B.; et al. Proteomics identifies new therapeutic targets of early-stage hepatocellular carcinoma. Nature 2019, 567, 257–261. [Google Scholar] [CrossRef]
- He, T.; Liu, Y.; Zhou, Y.; Li, L.; Wang, H.; Chen, S.; Gao, J.; Jiang, W.; Yu, Y.; Ge, W.; et al. Comparative Evaluation of Proteome Discoverer and FragPipe for the TMT-Based Proteome Quantification. J. Proteome Res. 2022, 21, 3007–3015. [Google Scholar] [CrossRef]
- Tyanova, S.; Temu, T.; Sinitcyn, P.; Carlson, A.; Hein, M.Y.; Geiger, T.; Mann, M.; Cox, J. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 2016, 13, 731–740. [Google Scholar] [CrossRef]
- Ge, S.; Xia, X.; Ding, C.; Zhen, B.; Zhou, Q.; Feng, J.; Yuan, J.; Chen, R.; Li, Y.; Ge, Z.; et al. A proteomic landscape of diffuse-type gastric cancer. Nat. Commun. 2018, 9, 1012. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ritchie, M.E.; Phipson, B.; Wu, D.; Hu, Y.; Law, C.W.; Shi, W.; Smyth, G.K. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015, 43, e47. [Google Scholar] [CrossRef] [PubMed]
- Hung, J.H.; Yang, T.H.; Hu, Z.; Weng, Z.; DeLisi, C. Gene set enrichment analysis: Performance evaluation and usage guidelines. Brief. Bioinform. 2012, 13, 281–291. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Consortium, G.O. The Gene Ontology resource: Enriching a GOld mine. Nucleic Acids Res. 2021, 49, D325–D334. [Google Scholar] [CrossRef]
- Wu, T.; Hu, E.; Xu, S.; Chen, M.; Guo, P.; Dai, Z.; Feng, T.; Zhou, L.; Tang, W.; Zhan, L.; et al. clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. Innov. Camb. Mass. 2021, 2, 100141. [Google Scholar] [CrossRef]
- Wang, P.; Zhang, Q.; Li, S.; Cheng, B.; Xue, H.; Wei, Z.; Shao, T.; Liu, Z.X.; Cheng, H.; Wang, Z. iCysMod: An integrative database for protein cysteine modifications in eukaryotes. Brief. Bioinform. 2021, 22, bbaa400. [Google Scholar] [CrossRef]
- Tan, C.; Li, Y.; Huang, X.; Wei, M.; Huang, Y.; Tang, Z.; Huang, H.; Zhou, W.; Wang, Y.; Hu, J. Extensive protein S-nitrosylation associated with human pancreatic ductal adenocarcinoma pathogenesis. Cell Death Dis. 2019, 10, 914. [Google Scholar] [CrossRef] [Green Version]
- Zhou, H.L.; Zhang, R.; Anand, P.; Stomberski, C.T.; Qian, Z.; Hausladen, A.; Wang, L.; Rhee, E.P.; Parikh, S.M.; Karumanchi, S.A.; et al. Metabolic reprogramming by the S-nitroso-CoA reductase system protects against kidney injury. Nature 2019, 565, 96–100. [Google Scholar] [CrossRef]
- Fujiwara, H.; Seike, K.; Brooks, M.D.; Mathew, A.V.; Kovalenko, I.; Pal, A.; Lee, H.J.; Peltier, D.; Kim, S.; Liu, C.; et al. Mitochondrial complex II in intestinal epithelial cells regulates T cell-mediated immunopathology. Nat. Immunol. 2021, 22, 1440–1451. [Google Scholar] [CrossRef]
- Ma, Y.; Qi, Y.; Wang, L.; Zheng, Z.; Zhang, Y.; Zheng, J. SIRT5-mediated SDHA desuccinylation promotes clear cell renal cell carcinoma tumorigenesis. Free Radic. Biol. Med. 2019, 134, 458–467. [Google Scholar] [CrossRef] [PubMed]
- Blottner, D.; Capitanio, D.; Trautmann, G.; Furlan, S.; Gambara, G.; Moriggi, M.; Block, K.; Barbacini, P.; Torretta, E.; Py, G.; et al. Nitrosative Redox Homeostasis and Antioxidant Response Defense in Disused Vastus lateralis Muscle in Long-Term Bedrest (Toulouse Cocktail Study). Antioxidants 2021, 10, 378. [Google Scholar] [CrossRef] [PubMed]
- Tsikas, D. Extra-platelet low-molecular-mass thiols mediate the inhibitory action of S-nitrosoalbumin on human platelet aggregation via S-transnitrosylation of the platelet surface. Amino Acids 2021, 53, 563–573. [Google Scholar] [CrossRef]
- Qiao, X.; Zhang, Y.; Ye, A.; Zhang, Y.; Xie, T.; Lv, Z.; Shi, C.; Wu, D.; Chu, B.; Wu, X.; et al. ER reductive stress caused by Ero1α S-nitrosation accelerates senescence. Free Radic. Biol. Med. 2022, 180, 165–178. [Google Scholar] [CrossRef] [PubMed]
- Hakimi, A.A.; Reznik, E.; Lee, C.H.; Creighton, C.J.; Brannon, A.R.; Luna, A.; Aksoy, B.A.; Liu, E.M.; Shen, R.; Lee, W.; et al. An Integrated Metabolic Atlas of Clear Cell Renal Cell Carcinoma. Cancer Cell 2016, 29, 104–116. [Google Scholar] [CrossRef] [Green Version]
- Qu, Y.; Feng, J.; Wu, X.; Bai, L.; Xu, W.; Zhu, L.; Liu, Y.; Xu, F.; Zhang, X.; Yang, G.; et al. A proteogenomic analysis of clear cell renal cell carcinoma in a Chinese population. Nat. Commun. 2022, 13, 2052. [Google Scholar] [CrossRef]
- Vander Heiden, M.G.; Cantley, L.C.; Thompson, C.B. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 2009, 324, 1029–1033. [Google Scholar] [CrossRef] [Green Version]
- Ju, H.Q.; Lin, J.F.; Tian, T.; Xie, D.; Xu, R.H. NADPH homeostasis in cancer: Functions, mechanisms and therapeutic implications. Signal Transduct. Target. Ther. 2020, 5, 231. [Google Scholar] [CrossRef]
- Xu, D.; Li, X.; Shao, F.; Lv, G.; Lv, H.; Lee, J.H.; Qian, X.; Wang, Z.; Xia, Y.; Du, L.; et al. The protein kinase activity of fructokinase A specifies the antioxidant responses of tumor cells by phosphorylating p62. Sci. Adv. 2019, 5, eaav4570. [Google Scholar] [CrossRef] [Green Version]
- Ying, W. NAD+/NADH and NADP+/NADPH in cellular functions and cell death: Regulation and biological consequences. Antioxid. Redox Signal. 2008, 10, 179–206. [Google Scholar] [CrossRef]
- Cao, X.; Wu, L.; Zhang, J.; Dolg, M. Density Functional Studies of Coenzyme NADPH and Its Oxidized Form NADP(+): Structures, UV-Vis Spectra, and the Oxidation Mechanism of NADPH. J. Comput. Chem. 2020, 41, 305–316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, J.; Yang, H.; Song, B.L. Mechanisms and regulation of cholesterol homeostasis. Nat. Rev. Mol. Cell Biol. 2020, 21, 225–245. [Google Scholar] [CrossRef] [PubMed]
- Xiao, W.; Wang, R.S.; Handy, D.E.; Loscalzo, J. NAD(H) and NADP(H) Redox Couples and Cellular Energy Metabolism. Antioxid. Redox Signal. 2018, 28, 251–272. [Google Scholar] [CrossRef] [PubMed]
- Fan, J.; Ye, J.; Kamphorst, J.J.; Shlomi, T.; Thompson, C.B.; Rabinowitz, J.D. Quantitative flux analysis reveals folate-dependent NADPH production. Nature 2014, 510, 298–302. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, L.; Shah, S.; Fan, J.; Park, J.O.; Wellen, K.E.; Rabinowitz, J.D. Malic enzyme tracers reveal hypoxia-induced switch in adipocyte NADPH pathway usage. Nat. Chem. Biol. 2016, 12, 345–352. [Google Scholar] [CrossRef] [Green Version]
- Jiang, P.; Du, W.; Wu, M. Regulation of the pentose phosphate pathway in cancer. Protein Cell 2014, 5, 592–602. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anastasiou, D.; Poulogiannis, G.; Asara, J.M.; Boxer, M.B.; Jiang, J.K.; Shen, M.; Bellinger, G.; Sasaki, A.T.; Locasale, J.W.; Auld, D.S.; et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011, 334, 1278–1283. [Google Scholar] [CrossRef] [Green Version]
- Yi, W.; Clark, P.M.; Mason, D.E.; Keenan, M.C.; Hill, C.; Goddard, W.A., 3rd; Peters, E.C.; Driggers, E.M.; Hsieh-Wilson, L.C. Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science 2012, 337, 975–980. [Google Scholar] [CrossRef] [Green Version]
- Langbein, S.; Frederiks, W.M.; zur Hausen, A.; Popa, J.; Lehmann, J.; Weiss, C.; Alken, P.; Coy, J.F. Metastasis is promoted by a bioenergetic switch: New targets for progressive renal cell cancer. Int. J. Cancer 2008, 122, 2422–2428. [Google Scholar] [CrossRef]
- Lucarelli, G.; Galleggiante, V.; Rutigliano, M.; Sanguedolce, F.; Cagiano, S.; Bufo, P.; Lastilla, G.; Maiorano, E.; Ribatti, D.; Giglio, A.; et al. Metabolomic profile of glycolysis and the pentose phosphate pathway identifies the central role of glucose-6-phosphate dehydrogenase in clear cell-renal cell carcinoma. Oncotarget 2015, 6, 13371–13386. [Google Scholar] [CrossRef]
- Ducker, G.S.; Rabinowitz, J.D. One-Carbon Metabolism in Health and Disease. Cell Metab. 2017, 25, 27–42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pikman, Y.; Puissant, A.; Alexe, G.; Furman, A.; Chen, L.M.; Frumm, S.M.; Ross, L.; Fenouille, N.; Bassil, C.F.; Lewis, C.A.; et al. Targeting MTHFD2 in acute myeloid leukemia. J. Exp. Med. 2016, 213, 1285–1306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ben-Sahra, I.; Hoxhaj, G.; Ricoult, S.J.H.; Asara, J.M.; Manning, B.D. mTORC1 induces purine synthesis through control of the mitochondrial tetrahydrofolate cycle. Science 2016, 351, 728–733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yoshino, H.; Nohata, N.; Miyamoto, K.; Yonemori, M.; Sakaguchi, T.; Sugita, S.; Itesako, T.; Kofuji, S.; Nakagawa, M.; Dahiya, R.; et al. PHGDH as a Key Enzyme for Serine Biosynthesis in HIF2α-Targeting Therapy for Renal Cell Carcinoma. Cancer Res. 2017, 77, 6321–6329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kong, W.; Wang, Z.; Chen, N.; Mei, Y.; Li, Y.; Yue, Y. SHMT2 regulates serine metabolism to promote the progression and immunosuppression of papillary renal cell carcinoma. Front. Oncol. 2022, 12, 914332. [Google Scholar] [CrossRef] [PubMed]
- Navas, L.E.; Carnero, A. NAD(+) metabolism, stemness, the immune response, and cancer. Signal Transduct. Target. Ther. 2021, 6, 2. [Google Scholar] [CrossRef]
- Wettersten, H.I.; Hakimi, A.A.; Morin, D.; Bianchi, C.; Johnstone, M.E.; Donohoe, D.R.; Trott, J.F.; Aboud, O.A.; Stirdivant, S.; Neri, B.; et al. Grade-Dependent Metabolic Reprogramming in Kidney Cancer Revealed by Combined Proteomics and Metabolomics Analysis. Cancer Res. 2015, 75, 2541–2552. [Google Scholar] [CrossRef] [Green Version]
- Abu Aboud, O.; Habib, S.L.; Trott, J.; Stewart, B.; Liang, S.; Chaudhari, A.J.; Sutcliffe, J.; Weiss, R.H. Glutamine Addiction in Kidney Cancer Suppresses Oxidative Stress and Can Be Exploited for Real-Time Imaging. Cancer Res. 2017, 77, 6746–6758. [Google Scholar] [CrossRef] [Green Version]
- Hoerner, C.R.; Chen, V.J.; Fan, A.C. The ‘Achilles Heel’ of Metabolism in Renal Cell Carcinoma: Glutaminase Inhibition as a Rational Treatment Strategy. Kidney Cancer 2019, 3, 15–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.F.; Klein Geltink, R.I.; Parker, S.J.; Sorensen, P.H. Transsulfuration, minor player or crucial for cysteine homeostasis in cancer. Trends Cell Biol. 2022, 32, 800–814. [Google Scholar] [CrossRef]
- Badgley, M.A.; Kremer, D.M.; Maurer, H.C.; DelGiorno, K.E.; Lee, H.J.; Purohit, V.; Sagalovskiy, I.R.; Ma, A.; Kapilian, J.; Firl, C.E.M.; et al. Cysteine depletion induces pancreatic tumor ferroptosis in mice. Science 2020, 368, 85–89. [Google Scholar] [CrossRef] [PubMed]
- Cramer, S.L.; Saha, A.; Liu, J.; Tadi, S.; Tiziani, S.; Yan, W.; Triplett, K.; Lamb, C.; Alters, S.E.; Rowlinson, S.; et al. Systemic depletion of L-cyst(e)ine with cyst(e)inase increases reactive oxygen species and suppresses tumor growth. Nat. Med. 2017, 23, 120–127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liao, Z.; Fang, Z.; Gou, S.; Luo, Y.; Liu, Y.; He, Z.; Li, X.; Peng, Y.; Fu, Z.; Li, D.; et al. The role of diet in renal cell carcinoma incidence: An umbrella review of meta-analyses of observational studies. BMC Med. 2022, 20, 39. [Google Scholar] [CrossRef] [PubMed]
- Ngo, B.; Van Riper, J.M.; Cantley, L.C.; Yun, J. Targeting cancer vulnerabilities with high-dose vitamin C. Nat. Rev. Cancer 2019, 19, 271–282. [Google Scholar] [CrossRef]
- Buettner, G.R. The pecking order of free radicals and antioxidants: Lipid peroxidation, alpha-tocopherol, and ascorbate. Arch. Biochem. Biophys. 1993, 300, 535–543. [Google Scholar] [CrossRef]
- Padayatty, S.J.; Levine, M. Vitamin C: The known and the unknown and Goldilocks. Oral Dis. 2016, 22, 463–493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shenoy, N.; Creagan, E.; Witzig, T.; Levine, M. Ascorbic Acid in Cancer Treatment: Let the Phoenix Fly. Cancer Cell 2018, 34, 700–706. [Google Scholar] [CrossRef] [Green Version]
- Tian, W.; Wang, Y.; Xu, Y.; Guo, X.; Wang, B.; Sun, L.; Liu, L.; Cui, F.; Zhuang, Q.; Bao, X.; et al. The hypoxia-inducible factor renders cancer cells more sensitive to vitamin C-induced toxicity. J. Biol. Chem. 2014, 289, 3339–3351. [Google Scholar] [CrossRef] [Green Version]
- Oda, M.; Satta, Y.; Takenaka, O.; Takahata, N. Loss of urate oxidase activity in hominoids and its evolutionary implications. Mol. Biol. Evol. 2002, 19, 640–653. [Google Scholar] [CrossRef] [Green Version]
- Ames, B.N.; Cathcart, R.; Schwiers, E.; Hochstein, P. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc. Natl. Acad. Sci. USA 1981, 78, 6858–6862. [Google Scholar] [CrossRef]
- Crawley, W.T.; Jungels, C.G.; Stenmark, K.R.; Fini, M.A. U-shaped association of uric acid to overall-cause mortality and its impact on clinical management of hyperuricemia. Redox Biol. 2022, 51, 102271. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Xu, W.; Chen, Y.; Han, A.; Song, J.; Zhou, X.; Song, W. Renal NF-κB activation impairs uric acid homeostasis to promote tumor-associated mortality independent of wasting. Immunity 2022, 55, 1594–1608.e1596. [Google Scholar] [CrossRef] [PubMed]
- Yim, K.; Bindayi, A.; McKay, R.; Mehrazin, R.; Raheem, O.A.; Field, C.; Bloch, A.; Wake, R.; Ryan, S.; Patterson, A.; et al. Rising Serum Uric Acid Level Is Negatively Associated with Survival in Renal Cell Carcinoma. Cancers 2019, 11, 536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeon, H.G.; Choo, S.H.; Jeong, B.C.; Seo, S.I.; Jeon, S.S.; Choi, H.Y.; Lee, H.M. Uric acid levels correlate with baseline renal function and high levels are a potent risk factor for postoperative chronic kidney disease in patients with renal cell carcinoma. J. Urol. 2013, 189, 1249–1254. [Google Scholar] [CrossRef]
- Park, T.J.; Reznick, J.; Peterson, B.L.; Blass, G.; Omerbašić, D.; Bennett, N.C.; Kuich, P.; Zasada, C.; Browe, B.M.; Hamann, W.; et al. Fructose-driven glycolysis supports anoxia resistance in the naked mole-rat. Science 2017, 356, 307–311. [Google Scholar] [CrossRef] [Green Version]
- Fini, M.A.; Elias, A.; Johnson, R.J.; Wright, R.M. Contribution of uric acid to cancer risk, recurrence, and mortality. Clin. Transl. Med. 2012, 1, 16. [Google Scholar] [CrossRef] [Green Version]
- Allegrini, S.; Garcia-Gil, M.; Pesi, R.; Camici, M.; Tozzi, M.G. The Good, the Bad and the New about Uric Acid in Cancer. Cancers 2022, 14, 4959. [Google Scholar] [CrossRef]
- Yoon, C.Y.; Shim, Y.J.; Kim, E.H.; Lee, J.H.; Won, N.H.; Kim, J.H.; Park, I.S.; Yoon, D.K.; Min, B.H. Renal cell carcinoma does not express argininosuccinate synthetase and is highly sensitive to arginine deprivation via arginine deiminase. Int. J. Cancer 2007, 120, 897–905. [Google Scholar] [CrossRef]
- Gonçalves, D.A.; Jasiulionis, M.G.; Melo, F.H.M. The Role of the BH4 Cofactor in Nitric Oxide Synthase Activity and Cancer Progression: Two Sides of the Same Coin. Int. J. Mol. Sci. 2021, 22, 9546. [Google Scholar] [CrossRef]
- Maric, S.; Restin, T.; Muff, J.L.; Camargo, S.M.; Guglielmetti, L.C.; Holland-Cunz, S.G.; Crenn, P.; Vuille-Dit-Bille, R.N. Citrulline, Biomarker of Enterocyte Functional Mass and Dietary Supplement. Metabolism, Transport, and Current Evidence for Clinical Use. Nutrients 2021, 13, 2794. [Google Scholar] [CrossRef]
- Zhang, Y.; Sun, C.; Xiao, G.; Shan, H.; Tang, L.; Yi, Y.; Yu, W.; Gu, Y. S-nitrosylation of the Peroxiredoxin-2 promotes S-nitrosoglutathione-mediated lung cancer cells apoptosis via AMPK-SIRT1 pathway. Cell Death Dis. 2019, 10, 329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhong, H.; Yin, H. Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: Focusing on mitochondria. Redox Biol. 2015, 4, 193–199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, H.; Wu, L.; Yan, G.; Chen, Y.; Zhou, M.; Wu, Y.; Li, Y. Inflammation and tumor progression: Signaling pathways and targeted intervention. Signal Transduct. Target. Ther. 2021, 6, 263. [Google Scholar] [CrossRef] [PubMed]
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Zhang, W.; Qiao, X.; Xie, T.; Cai, W.; Zhang, X.; Chen, C.; Zhang, Y. Multi-Omics Approach Reveals Redox Homeostasis Reprogramming in Early-Stage Clear Cell Renal Cell Carcinoma. Antioxidants 2023, 12, 81. https://doi.org/10.3390/antiox12010081
Zhang W, Qiao X, Xie T, Cai W, Zhang X, Chen C, Zhang Y. Multi-Omics Approach Reveals Redox Homeostasis Reprogramming in Early-Stage Clear Cell Renal Cell Carcinoma. Antioxidants. 2023; 12(1):81. https://doi.org/10.3390/antiox12010081
Chicago/Turabian StyleZhang, Wei, Xinhua Qiao, Ting Xie, Wenbin Cai, Xu Zhang, Chang Chen, and Yaoguang Zhang. 2023. "Multi-Omics Approach Reveals Redox Homeostasis Reprogramming in Early-Stage Clear Cell Renal Cell Carcinoma" Antioxidants 12, no. 1: 81. https://doi.org/10.3390/antiox12010081
APA StyleZhang, W., Qiao, X., Xie, T., Cai, W., Zhang, X., Chen, C., & Zhang, Y. (2023). Multi-Omics Approach Reveals Redox Homeostasis Reprogramming in Early-Stage Clear Cell Renal Cell Carcinoma. Antioxidants, 12(1), 81. https://doi.org/10.3390/antiox12010081