Enfeksiyon Hastalıklarında Ferroptozun Rolü

Abstract

Glutatyon (GSH) ve glutatyon peroksidaz 4 (Glutathione peroxidase 4; GPX4) gibi lipid onarım sistemleriyle kontrol edilen ve çoklu doymamış yağ asidi (polyunsaturated fatty acids; PUFA) biyosentezini de kapsayan, bir dizi enzimatik reaksiyon ile korele olan ölüm tipine ferroptoz adı verilir. Ferroptoz aynı zamanda, ferröz (Fe+2) demire bağımlı hücre ölüm tipi olarak tanımlanmıştır. Apoptoz, piroptoz, otofaji gibi diğer hücre ölüm yollarından farklı özellikler gösterir. Ferroptoz sırasında gözlemlenen en önemli morfolojik özellikler; mitokondride gözlenen küçülme ve membran yoğunluğudur. Biyokimyasal özellikler ise, hücre içi serbest demir miktarındaki artış ve lipid peroksidasyonudur. Ferroptoz, nörodejeneratif hastalıklar ve kanser gibi hastalıkların ortaya çıkmasında ve gelişiminde önemli rol oynaması nedeniyle çok sayıda araştırmanın odak noktası haline gelmiştir. Bu hastalıkların yanı sıra; GPX4, GSH aktivitesinde azalma ve ortamda reaktif oksijen türlerinin (ROT) birikimi gibi olaylar ile birçok enfeksiyon hastalığında da ferroptoz süreci görülebilmektedir.

Keywords

• Ferroptoz
• Demir
• Lipid peroksidasyonu
• GPX4
• Enfeksiyon

Ferroptosis in Infectious Diseases

Abstract

The type of death that is controlled by lipid repair systems such as glutathione (GSH) and glutathione peroxidase 4 (GPX4) and correlates with a series of enzymatic reactions, including polyunsaturated fatty acids (PUFA) biosynthesis, is called ferroptosis. Ferroptosis has also been defined as a ferrous (Fe+2) iron-dependent type of cell death. It shows different features from other cell death pathways such as apoptosis, pyroptosis, autophagy. The most important morphological features observed during ferroptosis; shrinkage and membrane density observed in mitochondria. Biochemical features are the increase in the amount of intracellular free iron and lipid peroxidation. Ferroptosis has become the focus of numerous studies because it plays an important role in the emergence and development of diseases such as neurodegenerative diseases and cancer. Besides these diseases; Ferroptosis process can be seen in many infectious diseases with events such as decrease in GPX4, GSH activity and accumulation of reactive oxygen species (ROS) in the environment.

Keywords

• Ferroptosis
• Iron
• Lipid peroxidation
• GPX4
• Infection

References

1. 1- Cui, J., Zhao, S., Li, Y., Zhang, D., Wang, B., Xie, J., & Wang, J. (2021). Regulated cell death: discovery, features and implications for neurodegenerative diseases. Cell Communication and Signaling, 19(1), 1-29.
2. 2- Dixon SJ. Ferroptosis: bug or feature? Immunol Rev. 2017;277:150–7
3. 3- Mou, Y., Wang, J., Wu, J., He, D., Zhang, C., Duan, C., & Li, B. (2019). Ferroptosis, a new form of cell death: opportunities and challenges in cancer. Journal of hematology & oncology, 12(1), 1-16.
4. 4- Zhao, Y., Li, Y., Zhang, R., Wang, F., Wang, T., & Jiao, Y. (2020). The role of erastin in ferroptosis and its prospects in cancer therapy. OncoTargets and therapy, 13, 5429.
5. 5- Liu, M. R., Zhu, W. T., & Pei, D. S. (2021). System Xc−: A key regulatory target of ferroptosis in cancer. Investigational New Drugs, 39(4), 1123-1131.
6. 6- Bridges, R. J., Natale, N. R., & Patel, S. A. (2012). System xc cystine/glutamate antiporter: An update on molecular pharmacology and roles within the CNS. British Journal of Pharmacology, 165(1), 20–34. https://doi.org/10.1111/j.1476-5381.2011.01480.x
7. 7- Yu, H., Guo, P., Xie, X., Wang, Y., & Chen, G. (2017). Ferroptosis, a new form of cell death, and its relationships with tumourous diseases. Journal of Cellular and Molecular Medicine, 21(4), 648–657. https://doi.org/10.1111/ jcmm.13008
8. 8- Li, J., Cao, F., Yin, H. L., Huang, Z. J., Lin, Z. T., Mao, N., ... & Wang, G. (2020). Ferroptosis: past, present and future. Cell death & disease, 11(2), 88.

9. 9- Dai L, Cao Y, Chen Y, Parsons C, Qin Z. Targeting xCT, a cystine-glutamate transporter induces apoptosis and tumor regression for KSHV/HIV-associated lymphoma. J Hematol Oncol. 2014;7:30.
10. 10- Liu, G.Z. et al. (2021) HBx facilitates ferroptosis in acute liver failure via EZH2 mediated SLC7A11 suppression. J. Biomed. Sci. 28, 1–13
11. 11- Cheng, J. et al. (2022) Swine influenza virus triggers ferroptosis in A549 cells to enhance virus replication. Virol. J. 19, 104
12. 12- Zhao, J., Xu, B., Xiong, Q., Feng, Y., & Du, H. (2021). Erastin‑induced ferroptosis causes physiological and pathological changes in healthy tissues of mice. Molecular medicine reports, 24(4), 713. https://doi.org/10.3892/mmr.2021.12352
13. 13- Liang, C., Zhang, X., Yang, M., & Dong, X. (2019). Recent progress in ferroptosis inducers for cancer therapy. Advanced materials, 31(51), 1904197.
14. 14- M. Matsushita, S. Freigang, C. Schneider, M. Conrad, G.W. Bornkamm, M. Kopf, T cell lipid peroxidation induces ferroptosis and prevents immunity to infection, J. Exp. Med. 212 (4) (2015) 555–568.
15. 15- Muri, J., H. Thut, G.W. Bornkamm, and M. Kopf. 2019. B1 and Marginal Zone B Cells but Not Follicular B2 Cells Require Gpx4 to Prevent Lipid Peroxidation and Ferroptosis. Cell Rep. 29:2731–2744.e4. https://doi.org/10 .1016/j.celrep.2019.10.070
16. 16- Yang, W. S. & Stockwell, B. R. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem. Biol. 15, 234–245 (2008).
17. 17- Hacioglu, C., Kar, F., Davran, F., & Tuncer, C. (2023). Borax regulates iron chaperone‐and autophagy‐mediated ferroptosis pathway in glioblastoma cells. Environmental Toxicology.
18. 18- Bagayoko, S., & Meunier, E. (2022). Emerging roles of ferroptosis in infectious diseases. The FEBS Journal, 289(24), 7869-7890.
19. 19- Morris D, Guerra C, Donohue C, Oh H, Khurasany M, Venketaraman V. Unveiling the mechanisms for decreased glutathione in individuals with HIV infection. Clin Dev Immunol. 2012;2012:734125
20. 20- Yang, W. S., Kim, K. J., Gaschler, M. M., Patel, M., Shchepinov, M. S., and Stockwell, B. R. (2016). Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc. Natl. Acad. Sci. U.S.A. 113, E4966–E4975. doi: 10.1073/pnas.1603244113
21. 21- Shimada, K., Skouta, R., Kaplan, A., Yang, W. S., Hayano, M., Dixon, S. J., et al. (2016b). Global survey of cell death mechanisms reveals metabolic regulation of ferroptosis. Nat. Chem. Biol. 12, 497–503. doi: 10.1038/nchembio.2079
22. 22- Zhang, X., Guo, Y., Li, H., & Han, L. (2021). FIN56, a novel ferroptosis inducer, triggers lysosomal membrane permeabilization in a TFEB-dependent manner in glioblastoma. Journal of Cancer, 12(22), 6610.
23. 23- Gaschler MM, Andia A. A et al. FINO2 initiates ferroptosis through Gpx4 inactivation and driving lipid peroxidation. Nature chemical biology. 2018; 14(5):507–15. https://doi.org/10.1038/s41589-018-0031- 6 PMID: 29610484
24. 24- Abrams RP, Carroll WL, Woerpel KA. Five-Membered Ring Peroxide Selectively Initiates Ferroptosis in Cancer Cells. ACS Chem Biol. 2016; 11(5):1305–12. https://doi.org/10.1021/acschembio.5b00900 PMID: 26797166; PubMed Central PMCID: PMC5507670.
25. 25- Jiang L, Kon N, Li T, Wang SJ, Su T, Hibshoosh H, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature. 2015;520:57–62.
26. 26- Jennis, M.; Kung, C.-P.; Basu, S.; Budina-Kolomets, A.; Leu, J.I.-J.; Khaku, S.; Scott, J.P.; Cai, K.Q.; Campbell, M.R.; Porter, D.K.; et al. An African-specific polymorphism in the TP53 gene impairs p53 tumor suppressor function in a mouse model. Genes Dev. 2016, 30, 918–930.
27. 27- Akiyama, H., Carter, B. Z., Andreeff, M., & Ishizawa, J. (2023). Molecular Mechanisms of Ferroptosis and Updates of Ferroptosis Studies in Cancers and Leukemia. Cells, 12(8), 1128.
28. 28- Chen, Y., Li, X., Wang, S., Miao, R., & Zhong, J. (2023). Targeting Iron Metabolism and Ferroptosis as Novel Therapeutic Approaches in Cardiovascular Diseases. Nutrients, 15(3), 591.
29. 29- Yao, Y., Shi, Y., Gao, Z., Sun, Y., Yao, F., & Ma, L. (2022). Ferroptosis at the crossroads of tumor-host interactions, metastasis, and therapy response. American Journal of Physiology-Cell Physiology, 323(1), C95-C103.
30. 30- Chen, Y., Fan, Z., Hu, S., Lu, C., Xiang, Y., & Liao, S. (2022). Ferroptosis: A new strategy for cancer therapy. Frontiers in Oncology, 12, 830561.
31. 31- Ju, J., Song, Y. N., & Wang, K. (2021). Mechanism of ferroptosis: a potential target for cardiovascular diseases treatment. Aging and disease, 12(1), 261.
32. 32- Gao, W., Zhang, T., & Wu, H. (2021). Emerging pathological engagement of ferroptosis in gut diseases. Oxidative Medicine and Cellular Longevity, 2021.
33. 33- Gaschler MM, Stockwell BR (2017) Lipid peroxidation in cell death. Biochem Biophys Res Commun 482:419–425. https://doi.org/10.1016/j.bbrc.2016.10.086
34. 34- Lee, J. Y., Kim, W. K., Bae, K. H., Lee, S. C., & Lee, E. W. (2021). Lipid Metabolism and Ferroptosis. Biology, 10(3), 184. https://doi.org/10.3390/biology10030184
35. 35- Conrad, M., Kagan, V. E., Bayir, H., Pagnussat, G. C., Head, B., Traber, M. G., & Stockwell, B. R. (2018). Regulation of lipid peroxidation and ferroptosis in diverse species. Genes & development, 32(9-10), 602–619. https://doi.org/10.1101/gad.314674.118
36. 36- Hacioglu, C., & Kar, F. (2023). Capsaicin induces redox imbalance and ferroptosis through ACSL4/GPx4 signaling pathways in U87-MG and U251 glioblastoma cells. Metabolic Brain Disease, 38(2), 393-408.
37. 37- Liu S, Tang Y, Liu L, Yang L, Li P, Liu X, Yin H. Proteomic analysis reveals that ACSL4 activation during reflux esophagitis contributes to ferroptosis-mediated esophageal mucosal damage. Eur J Pharmacol. 2022;931(175175):175175. doi:10.1016/j.ejphar.2022. 175175.
38. 38- Ning K, Lu K, Chen Q, Guo Z, Du X, Riaz F, Feng L, Fu Y, Yin C, Zhang F, et al. Epigallocatechin gallate protects mice against methionine–choline-Deficient Diet-Induced nonalcoholic steatohepatitis by improving gut microbiota to attenuate hepatic injury and regulate metabolism. ACS Omega. 2020;5(33):20800–20809. doi:10.1021/acsomega.0c01689.
39. 39- Yao, T., & Li, L. (2023). The influence of microbiota on ferroptosis in intestinal diseases. Gut Microbes, 15(2), 2263210.
40. 40- Sezgin, G., Fatih, K. A. R., HACIOĞLU, C., & Sema, U. S. L. U. (2022). Obezite ACSL4 ve GPX4 Aracılı Ferroptozis ile Oksidatif Stresi İndükler. Osmangazi Tıp Dergisi, 44(2), 224-230.
41. 41- Rishi et al., 2015 G. Rishi, D.F. Wallace, V.N. Subramaniam Hepcidin: regulation of the master iron regulator Biosci. Rep., 35 (3) (2015), Article e00192
42. 42- Tang, D. (Ed.). (2019). Ferroptosis in Health and Disease (pp. 43-59). Cham, Switzerland: Springer.
43. 43- Chen, X., Yu, C., Kang, R., & Tang, D. (2020). Iron Metabolism in Ferroptosis. Frontiers in cell and developmental biology, 8, 590226. https://doi.org/10.3389/fcell.2020.590226
44. 44- Sun, K., Li, C., Liao, S., Yao, X., Ouyang, Y., Liu, Y., Wang, Z., Li, Z., & Yao, F. (2022). Ferritinophagy, a form of autophagic ferroptosis: New insights into cancer treatment. Frontiers in pharmacology, 13, 1043344. https://doi.org/10.3389/fphar.2022.1043344
45. 45- Hao, S., Liang, B., Huang, Q., Dong, S., Wu, Z., He, W., & Shi, M. (2018). Metabolic networks in ferroptosis. Oncology Letters, 15(4), 5405-5411.
46. 46- N. Geng, B.J. Shi, S.L. Li, Z.Y. Zhong, Y.C. Li, W.L. Xua, H. Zhou, J.H. Cai, Knockdown of ferroportin accelerates erastin-induced ferroptosis in neuroblastoma cells, Eur. Rev. Med Pharm. Sci. 22 (12) (2018) 3826–3836.
47. 47- Hou, W., Xie, Y., Song, X., Sun, X., Lotze, M. T., Zeh III, H. J., ... & Tang, D. (2016). Autophagy promotes ferroptosis by degradation of ferritin. Autophagy, 12(8), 1425-1428.
48. 48- Park, E., & Chung, S. W. (2019). ROS-mediated autophagy increases intracellular iron levels and ferroptosis by ferritin and transferrin receptor regulation. Cell Death & Disease, 10(11), 822.
49. 49- Hacioglu, C., & Tuncer, C. (2023). Boric acid Increases Susceptibility to Chemotherapy by Targeting the Ferritinophagy Signaling Pathway in TMZ Resistant Glioblastoma Cells. Biological Trace Element Research, 1-14.
50. 50- Haschka, D., Hoffmann, A., & Weiss, G. (2021, July). Iron in immune cell function and host defense. In Seminars in Cell & Developmental Biology (Vol. 115, pp. 27-36). Academic Press.
51. 51- E.E. Johnson, A. Sandgren, B.J. Cherayil, M. Murray, M. Wessling-Resnick, Role of ferroportin in macrophage-mediated immunity, Infect. Immun. 78 (12) (2010) 5099–5106.
52. 52- D. Lim, K.S. Kim, J.H. Jeong, O. Marques, H.J. Kim, M. Song, T.H. Lee, J.I. Kim, H. S. Choi, J.J. Min, D. Bumann, M.U. Muckenthaler, H.E. Choy, The hepcidinferroportin axis controls the iron content of Salmonella-containing vacuoles in macrophages, Nat. Commun. 9 (1) (2018) 2091.
53. 53- Stockwell BR, Friedmann Angeli JP, Bayir H, Bush AI, Conrad M, et al. 2017. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell 171(2): 273–85
54. 54- Fillebeen C, Pantopoulos K. Iron inhibits replication of infectious hepatitis C virus in permissive Huh7.5.1 cells. J Hepatol. 2010;53:995–9.
55. 55- Zhang, Q. et al. (2022) Exosomes derived from hepatitis B virusinfected hepatocytes promote liver fibrosis via miR-222/TFRC axis. Cell Biol. Toxicol. Published online January 3, 2022. https://doi.org/10.1007/s10565-021-09684-z
56. 56- Wang H, Li Z, Niu J, Xu Y, Ma L, Lu A, et al. Antiviral effects of ferric ammonium citrate. Cell Discov. 2018;4:14.
57. 57- Capelletti, M. M., Manceau, H., Puy, H., & Peoc'h, K. (2020). Ferroptosis in Liver Diseases: An Overview. International journal of molecular sciences, 21(14), 4908. https://doi.org/10.3390/ijms21144908
58. 58- Latunde-Dada G. O. (2017). Ferroptosis: Role of lipid peroxidation, iron and ferritinophagy. Biochimica et biophysica acta. General subjects, 1861(8), 1893–1900. https://doi.org/10.1016/j.bbagen.2017.05.019
59. 59- Degterev A., Linkermann A. Generation of small molecules to interfere with regulated necrosis. Cellular and Molecular Life Sciences. 2016;73:2251–2267. doi: 10.1007/s00018-016-2198-x.
60. 60- Dong, H. Q., Liang, S. J., Xu, Y. L., Dai, Y., Sun, N., Deng, D. H., & Cheng, P. (2022). Liproxstatin-1 induces cell cycle arrest, apoptosis, and caspase-3/GSDME-dependent secondary pyroptosis in K562 cells. International Journal of Oncology, 61(4), 1-13.
61. 61- Mishima, E.; Ito, J.; Wu, Z.; Nakamura, T.; Wahida, A.; Doll, S.; Tonnus, W.; Nepachalovich, P.; Eggenhofer, E.; Aldrovandi, M.; et al. A non-canonical vitamin K cycle is a potent ferroptosis suppressor. Nature 2022, 1–6.
62. 62- Feng, Y., Madungwe, N. B., Aliagan, A. D. I., Tombo, N., & Bopassa, J. C. (2019). Ferroptosis inhibitor, liproxstatin-1, protects the myocardium against ischemia/reperfusion injury by decreasing VDAC1 levels and rescuing GPX4 levels. Biochemical and biophysical research communications, 520(3), 606.
63. 63- Mao, H., Zhao, Y., Li, H., & Lei, L. (2020). Ferroptosis as an emerging target in inflammatory diseases. Progress in biophysics and molecular biology, 155, 20–28. https://doi.org/10.1016/j.pbiomolbio.2020.04.001
64. 64- Jia, M., D. Qin, C. Zhao, L. Chai, Z. Yu, W. Wang, L. Tong, L. Lv, Y. Wang, J. Rehwinkel, et al. 2020. Redox homeostasis maintained by GPX4 facilitates STING activation. Nat. Immunol. 21:727–735. https://doi.org/10 .1038/s41590-020-0699-0
65. 65- Spooner R, Yilmaz O. 2011. The role of reactive-oxygen-species in microbial persistence and inflammation. Int J Mol Sci. 12(1): 334-52
66. 66- Zhu H, Santo A, Jia Z, Robert Li Y. 2019. GPx4 in Bacterial Infection and Polymicrobial Sepsis: Involvement of Ferroptosis and Pyroptosis. React Oxyg Species (Apex). 7(21): 154-160.
67. 67- Gellatly, S.L.; Hancock, R.E. Pseudomonas aeruginosa: New insights into pathogenesis and host defenses. Pathog. Dis. 2013, 67, 159–173.
68. 68- Dar, H. H., Tyurina, Y. Y., Mikulska-Ruminska, K., Shrivastava, I., Ting, H. C., Tyurin, V. A., ... & Kagan, V. E. (2019). Pseudomonas aeruginosa utilizes host polyunsaturated phosphatidylethanolamines to trigger theft-ferroptosis in bronchial epithelium. The Journal of clinical investigation, 128(10), 4639-4653.
69. 69- Ousingsawat, J., Schreiber, R., Gulbins, E., Kamler, M., & Kunzelmann, K. (2021). P. aeruginosa induced lipid peroxidation causes ferroptotic cell death in airways. Cell Physiol Biochem, 55(5), 590-604.
70. 70- Britigan BE, Britigan BE & Edekert BL (1991) Pseudomonas and neutrophil products modify transferrin and lactoferrin to create conditions that favor hydroxyl radical formation. Pseudomonas and Neutrophil products modify transferrin and lactoferrin to create conditions that favor hydroxyl radical form. J Clin Invest 88, 1092–1102.
71. 71- Huang, M., Wang, Z., Yao, L., Zhang, L., Gou, X., Mo, H., ... & Zhou, X. (2023). Ferric chloride induces ferroptosis in Pseudomonas aeruginosa and heals wound infection in a mouse model. International Journal of Antimicrobial Agents, 61(5), 106794.
72. 72- Banuls, A. L., Sanou, A., Van Anh, N. T., & Godreuil, S. (2015). Mycobacterium tuberculosis: ecology and evolution of a human bacterium. Journal of medical microbiology, 64(11), 1261-1269.
73. 73- Chen, X., Kang, R., Kroemer, G., & Tang, D. (2021). Ferroptosis in infection, inflammation, and immunity. Journal of Experimental Medicine, 218(6), e20210518.
74. 74- Seyedrezazadeh, E., Ostadrahimi, A., Mahboob, S., Assadi, Y., Ghaemmagami, J., & Pourmogaddam, M. (2008). Effect of vitamin E and selenium supplementation on oxidative stress status in pulmonary tuberculosis patients. Respirology (Carlton, Vic.), 13(2), 294–298. https://doi.org/10.1111/j.1440-1843.2007.01200.x
75. 75- Qiang, L., Zhang, Y., Lei, Z., Lu, Z., Tan, S., Ge, P., ... & Wang, J. (2023). A mycobacterial effector promotes ferroptosis-dependent pathogenicity and dissemination. Nature Communications, 14(1), 1430.
76. 76- Amaral, E.P. et al. (2019) A major role for ferroptosis in Mycobacterium tuberculosis-induced cell death and tissue necrosis. J. Exp. Med. 216, 556–570
77. 77- Safe IP, Amaral EP, Araujo-Pereira M, Lacerda MVG, Printes VS, Souza AB, Beraldi-Magalh~aes F, Monteiro WM, Sampaio VS, Barreto-Duarte B et al. (2021) Adjunct N-acetylcysteine treatment in hospitalized patients with HIV-associated tuberculosis dampens the oxidative stress in peripheral blood: results from the RIPENACTB Study trial. Front Immunol 3791, 602589.
78. 78- Safe IP, Lacerda MVG, Printes VS, Praia Marins AF, Rebelo Rabelo AL, Costa AA, Tavares MA, Jesus JS, Souza AB, Beraldi-Magalh~aes F et al. (2020) Safety and efficacy of N-acetylcysteine in hospitalized patients with HIV-associated tuberculosis: an openlabel, randomized, phase II trial (RIPENACTB Study). PLoS One 15, e0235381.
79. 79- Baker-Austin, C., Trinanes, J., Gonzalez-Escalona, N. & Martinez-Urtaza, J. Non-Choler vibrios: the microbial barometer of climate change. Trends Microbiol. 25, 76–84 (2017).
80. 80- Brumfield, K. D., Usmani, M., Chen, K. M., Gangwar, M., Jutla, A. S., Huq, A., & Colwell, R. R. (2021). Environmental parameters associated with incidence and transmission of pathogenic Vibrio spp. Environmental microbiology, 23(12), 7314-7340.
81. 81- Moravec AR, Siv AW, Hobby CR, Lindsay EN, Norbash LV, Shults DJ, Symes SJK, Giles DK. 2017. Exogenous polyunsaturated fatty acids impact membrane remodeling and affect virulence phenotypes among pathogenic Vibrio species. Appl Environ Microbiol 83: e01415-17.
82. 82- Pui, C. F., Wong, W. C., Chai, L. C., Tunung, R., Jeyaletchumi, P., Hidayah, N., ... & Son, R. (2011). Salmonella: A foodborne pathogen. International Food Research Journal, 18(2).
83. 83- Agbor TA, Demma Z, Mrsny RJ, Castillo A, Boll EJ, McCormick BA. 2014. The oxido-reductase enzyme glutathione peroxidase 4 (GPX4) governs Salmonella Typhimurium-induced neutrophil transepithelial migration. Cell Microbiol 16: 1339–1353.
84. 84- Schauser K, Olsen JE, Larsson LI. 2005. Salmonella typhimurium infection in the porcine intestine: evidence for caspase-3-dependent and -independent programmed cell death. Histochem Cell Biol 123: 43–50.
85. 85- Lim D, Kim KS, Jeong JH, Marques O, Kim HJ, Song M. et al. The hepcidin-ferroportin axis controls the iron content of Salmonella-containing vacuoles in macrophages. Nat Commun. 2018;91:2091. [PMC free article]
86. 86- Preshaw PM, Bissett SM. Periodontitis: Oral Complication of Diabetes. Endocrinol Metab Clin N Am. 2013;42(4):849–67.
87. 87- Chen, K., Ma, S., Deng, J., Jiang, X., Ma, F., & Li, Z. (2022). Ferroptosis: A New Development Trend in Periodontitis. Cells, 11(21), 3349. https://doi.org/10.3390/cells11213349
88. 88- Yao, C., Lan, D., Li, X., Wang, Y., Qi, S., & Liu, Y. (2023). Porphyromonas gingivalis is a risk factor for the development of nonalcoholic fatty liver disease via ferroptosis. Microbes and Infection, 25(1-2), 105040.
89. 89- Campbell NA, Reece JB. Biology. San Francisco: Pearson Education Inc; 2002
90. 90- Pilarczyk-Zurek M, Strus M, Adamski P, Heczko PB. The dual role of Escherichia coli in the course of ulcerative colitis. BMC Gastroenterol. 2016;16(1):128. doi:10. 1186/s12876-016-0540-2.
91. 91- Keshavarzian A, Banan A, Farhadi A, Komanduri S, Mutlu E, Zhang Y, Fields JZ. Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease. Gut. 2003;52(5):720–728. doi:10.1136/gut.52.5.720
92. 92- Bauckman K., Mysorekar I. Ferritinophagy drives uropathogenic Escherichia coli persistence in bladder epithelial cells. Autophagy. 2016;12:850–863. doi: 10.1080/15548627.2016.1160176.
93. 93- Lanjouw, E., Ouburg, S., De Vries, H. J., Stary, A., Radcliffe, K., & Unemo, M. (2016). 2015 European guideline on the management of Chlamydia trachomatis infections. International journal of STD & AIDS, 27(5), 333-348.
94. 94- Chen, W. et al. (2021) P131 Chlamydia trachomatis induces ferroptosis to promote its own dissemination by inhibiting SLC7A11/GPx4 signaling. Sex. Transm. Infect. 97, A1–A186
95. 95- Azenabor AA & Mahony JB (2000) Generation of reactive oxygen species and formation of membrane lipid peroxides in cells infected with Chlamydia trachomatis. Int J Infect Dis 4, 46–50.
96. 96- Coffin, J. M. Molecular biology of HIV. In The Evolution of HIV, ed. K. A. Crandall, 1999; 3-40.
97. 97- Higueras V, Raya A, Rodrigo J, Serra M A, Rom aJ& Romero FJ (1994) Interferon decreases serum lipid peroxidation products of hepatitis C patients. Free Radic Biol Med 16, 131–133
98. 98- Xu, X., Lin, D., Tu, S., Gao, S., Shao, A., & Sheng, J. (2021). Is Ferroptosis a Future Direction in Exploring Cryptococcal Meningitis?. Frontiers in immunology, 12, 598601. https://doi.org/10.3389/fimmu.2021.598601
99. 99- Jarvis JN, Meintjes G, Bicanic T, Buffa V, Hogan L, Mo S, et al.. Cerebrospinal fluid cytokine profiles predict risk of early mortality and immune reconstitution inflammatory syndrome in HIV-associated cryptococcal meningitis. PLoS Pathog (2015) 11(4):e1004754. 10.1371/journal.ppat.1004754
100. 100- Okara, B. C., & Al-Turjman, F. (2021). Smart Technologies for COVID-19: The Strategic Approaches in Combating the Virus. Artificial Intelligence and Machine Learning for COVID-19, 1-23.
101. 101- Muhoberac BB. What Can Cellular Redox, Iron, and Reactive Oxygen Species Suggest About the Mechanisms and Potential Therapy of COVID-19? Front Cell Infect Microbiol (2020) 10:569709. 10.3389/fcimb.2020.569709
102. 102- Singh Y, Gupta G, Kazmi I, Al-Abbasi FA, Negi P, Chellappan DK, et al.. SARS CoV-2 aggravates cellular metabolism mediated complications in COVID-19 infection. Dermatol Ther (2020) 33(6):e13871. 10.1111/dth.13871
103. 103- Edeas M, Saleh J, Peyssonnaux C. Iron: Innocent bystander or vicious culprit in COVID-19 pathogenesis? Int J Infect Dis (2020) 97:303–5. 10.1016/j.ijid.2020.05.110
104. 104- Duan L, Bahl J, Smith G.J.D, Wang J, Vijaykrishna D, Zhang L.J, Zhang J.X, Li K.S, Fan X.H, Cheung C.L, Huang K, Poon L.M.M, Shortridge K.F, Webster R.G, Peiris J.S.M, Chen H, Guan Y. The develepmont and genetic diversity of H5N1 Ġnfluenza virüs in China, 1996 – 2009. Virology 2008 October 25; 380(2): 243-254. doi:10.1016/j.virol.2008.07.038.
105. 105- Dou, J., Liu, X., Yang, L., Huang, D., & Tan, X. (2022). Ferroptosis interaction with inflammatory microenvironments: Mechanism, biology, and treatment. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 155, 113711. https://doi.org/10.1016/j.biopha.2022.113711
106. 106- Plosa, E. J., Esbenshade, J. C., Fuller, M. P., & Weitkamp, J. H. (2012). Cytomegalovirus infection. Pediatrics in Review, 33(4), 156-163.
107. 107- Sun Y., Bao Q., Xuan B., Xu W., Pan D., Li Q., Qian Z. Human Cytomegalovirus Protein pUL38 Prevents Premature Cell Death by Binding to Ubiquitin-specific Protease 24 and Regulating Iron Metabolism. J. Virol. 2018;92:e00191-18. doi: 10.1128/JVI.00191-18.
108. 108- Yu, H., & Robertson, E. S. (2023). Epstein–Barr Virus History and Pathogenesis. Viruses, 15(3), 714.
109. 109- Yuan, L. et al. (2022) EBV infection-induced GPX4 promotes chemoresistance and tumor progression in nasopharyngeal carcinoma. Cell Death Differ. 29, 1513–1527
110. 110- Dzogbema, K. F. X., Talaki, E., Batawui, K. B., & Dao, B. B. (2021). Review on Newcastle disease in poultry. International Journal of Biological and Chemical Sciences, 15(2), 773-789.
111. 111- Kan, X. et al. (2021) Newcastle-disease-virus-induced ferroptosis through nutrient deprivation and ferritinophagy in tumor cells. iScience 24, 102837
112. 112- Liu, H., Zhang, M., Feng, C., Cong, S., Xu, D., Sun, H., ... & Ma, S. (2021). Characterization of Coxsackievirus A6 strains isolated from children with hand, foot, and mouth disease. Frontiers in Cellular and Infection Microbiology, 11, 700191.
113. 113- Kung, Y.A. et al. (2022) Acyl-coenzyme A synthetase long-chain family member 4 is involved in viral replication organelle formation and facilitates virus replication via ferroptosis. mBio 13, e0271721
114. 114- Abu-Freha, N., Mathew Jacob, B., Elhoashla, A., Afawi, Z., Abu-Hammad, T., Elsana, F., ... & Etzion, O. (2022). Chronic hepatitis C: Diagnosis and treatment made easy. European Journal of General Practice, 28(1), 102-108.
115. 115- Ullah, H., Khan, M. I., Suleman, N. M., Ismail, N., Khan, Z., & Sayyid, G. (2015). A Review on Malarial Parasite. World Journal of Zoology, 10(4), 285-290.
116. 116- Cotter C., Sturrock H. J. W., Hsiang M. S., Liu J., Phillips A. A., Hwang J., et al. (2013). The changing epidemiology of malaria elimination: New strategies for new challenges. Lancet 382, 900–911. 10.1016/S0140-6736(13)60310-4.
117. 117- Sena-Dos-Santos C., Braga-Da-Silva C., Marques D., Azevedo Dos Santos Pinheiro J., Ribeiro-Dos-Santos A., Cavalcante G. C. (2021). Unraveling cell death pathways during malaria infection: What do we know so far? Cells 10, 479. 10.3390/cells10020479.
118. 118- Noireau F, Diosque P, Jansen M. Trypanosoma cruzi: adaptations to its vectors and its host factors. Vet Res. 2009:40(26):1–23.
119. 119- Bogacz M & Krauth-Siegel RL (2018) Tryparedoxin peroxidase-deficiency commits trypanosomes to ferroptosis-type cell death. Elife 7. https://doi.org/10. 7554/eLife.37503
120. 120- Giro, A. (2021). Review on Cryptococcus Disease. J Trop Dis, 9, 288.
121. 121- Hall CJ, Bouhafs L, Dizcfalusy U, Sandstedt K. Cryptococcus neoformans causes lipid peroxidation; therefore it is a potential inducer of atherogenesis. Mycologia (2010) 102(3):546–51. 10.3852/08-110 .
122. 122- Hedayati, M. T., Pasqualotto, A. C., Warn, P. A., Bowyer, P., & Denning, D. W. (2007). Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology, 153(6), 1677-1692.
123. 123- Yao, L., Ban, F., Peng, S., Xu, D., Li, H., Mo, H., ... & Zhou, X. (2021). Exogenous iron induces NADPH oxidases-dependent ferroptosis in the conidia of Aspergillus flavus. Journal of agricultural and food chemistry, 69(45), 13608-13617.
124. 124- Mittal, J., Ponce, M. G., Gendlina, I., & Nosanchuk, J. D. (2019). Histoplasma Capsulatum: Mechanisms for Pathogenesis. Current topics in microbiology and immunology, 422, 157–191. https://doi.org/10.1007/82_2018_114
125. 125- Horwath MC, Bell-Horwath TR, Lescano V, Krishnan K, Merino EJ, Deepe GS, Jr. Antifungal Activity of the Lipophilic Antioxidant Ferrostatin-1. Chembiochem (2017) 18(20):2069–78. 10.1002/cbic.201700105.
126. 126- Yagoda, N. et al. RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864–868 (2007).