FANCD2 protects against bone marrow injury from ferroptosis

Biochemical and Biophysical Research Communications

Volumn 480, Issue 3, 2016, Pages 443-449

  Song, Xinxin ^a   Xie, Yangchun ^a   Kang, Rui ^a   Hou, Wen ^b   Sun, Xiaofang ^c   Epperly, Michael W ^b   Greenberger, Joel S ^b   Tang, Daolin ^a,c  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Bone marrow; DNA damage; FANCD2; Ferroptosis; Iron; Lipid peroxidation

Indexed keywords

EPITHELIAL MEMBRANE ANTIGEN; FANCONI ANEMIA GROUP D2 PROTEIN; FERRITIN; FERROUS ION; GLUTATHIONE; HEAT SHOCK PROTEIN; HEPCIDIN; LIPID; MALONALDEHYDE; TRANSFERRIN; TRANSFERRIN RECEPTOR; FANCD2 PROTEIN, MOUSE; IRON;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BONE MARROW DISEASE; BONE MARROW STROMA CELL; CELL DEATH; CELL PROTECTION; CELL VIABILITY; DNA DAMAGE; FERROPTOSIS; GENE EXPRESSION; INJURY; IRON METABOLISM; LIPID PEROXIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; APOPTOSIS; CELL CULTURE; CELL SURVIVAL; KNOCKOUT MOUSE; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; IRON; LIPID PEROXIDATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT;

EID: 84994319021     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2016.10.068     Document Type: Article

References (46)

1. [1] Ashkenazi, A., Salvesen, G., Regulated cell death: signaling and mechanisms. Annu. Rev. Cell Dev. Biol. 30 (2014), 337–356.
2. [2] Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H., Vandenabeele, P., Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 15 (2014), 135–147.
3. [3] Galluzzi, L., Bravo-San Pedro, J.M., Vitale, I., Aaronson, S.A., Abrams, J.M., Adam, D., Alnemri, E.S., Altucci, L., Andrews, D., Annicchiarico-Petruzzelli, M., Baehrecke, E.H., Bazan, N.G., Bertrand, M.J., Bianchi, K., Blagosklonny, M.V., Blomgren, K., Borner, C., Bredesen, D.E., Brenner, C., Campanella, M., Candi, E., Cecconi, F., Chan, F.K., Chandel, N.S., Cheng, E.H., Chipuk, J.E., Cidlowski, J.A., Ciechanover, A., Dawson, T.M., Dawson, V.L., De Laurenzi, V., De Maria, R., Debatin, K.M., Di Daniele, N., Dixit, V.M., Dynlacht, B.D., El-Deiry, W.S., Fimia, G.M., Flavell, R.A., Fulda, S., Garrido, C., Gougeon, M.L., Green, D.R., Gronemeyer, H., Hajnoczky, G., Hardwick, J.M., Hengartner, M.O., Ichijo, H., Joseph, B., Jost, P.J., Kaufmann, T., Kepp, O., Klionsky, D.J., Knight, R.A., Kumar, S., Lemasters, J.J., Levine, B., Linkermann, A., Lipton, S.A., Lockshin, R.A., Lopez-Otin, C., Lugli, E., Madeo, F., Malorni, W., Marine, J.C., Martin, S.J., Martinou, J.C., Medema, J.P., Meier, P., Melino, S., Mizushima, N., Moll, U., Munoz-Pinedo, C., Nunez, G., Oberst, A., Panaretakis, T., Penninger, J.M., Peter, M.E., Piacentini, M., Pinton, P., Prehn, J.H., Puthalakath, H., Rabinovich, G.A., Ravichandran, K.S., Rizzuto, R., Rodrigues, C.M., Rubinsztein, D.C., Rudel, T., Shi, Y., Simon, H.U., Stockwell, B.R., Szabadkai, G., Tait, S.W., Tang, H.L., Tavernarakis, N., Tsujimoto, Y., Vanden Berghe, T., Vandenabeele, P., Villunger, A., Wagner, E.F., et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 22 (2015), 58–73.
4. [4] Wang, Y., Probin, V., Zhou, D., Cancer therapy-induced residual bone marrow injury-Mechanisms of induction and implication for therapy. Curr. Cancer Ther. Rev. 2 (2006), 271–279.
5. [5] Xie, Y., Hou, W., Song, X., Yu, Y., Huang, J., Sun, X., Kang, R., Tang, D., Ferroptosis: process and function. Cell Death Differ. 23 (2016), 369–379.
6. [6] Dixon, S.J., Lemberg, K.M., Lamprecht, M.R., Skouta, R., Zaitsev, E.M., Gleason, C.E., Patel, D.N., Bauer, A.J., Cantley, A.M., Yang, W.S., Morrison, B. 3rd, Stockwell, B.R., Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149 (2012), 1060–1072.
7. [7] Yang, W.S., SriRamaratnam, R., Welsch, M.E., Shimada, K., Skouta, R., Viswanathan, V.S., Cheah, J.H., Clemons, P.A., Shamji, A.F., Clish, C.B., Brown, L.M., Girotti, A.W., Cornish, V.W., Schreiber, S.L., Stockwell, B.R., Regulation of ferroptotic cancer cell death by GPX4. Cell 156 (2014), 317–331.
8. [8] Yu, Y., Xie, Y., Cao, L., Yang, L., Yang, M., Lotze, M.T., Zeh, H.J., Kang, R., Tang, D., The ferroptosis inducer erastin enhances sensitivity of acute myeloid leukemia cells to chemotherapeutic agents. Mol. Cell Oncol., 2, 2015, e1054549.
9. [9] Sun, X., Niu, X., Chen, R., He, W., Chen, D., Kang, R., Tang, D., Metallothionein-1G facilitates sorafenib resistance through inhibition of ferroptosis. Hepatology 64 (2016), 488–500.
10. [10] Sun, X., Ou, Z., Chen, R., Niu, X., Chen, D., Kang, R., Tang, D., Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology 63 (2016), 173–184.
11. [11] Louandre, C., Marcq, I., Bouhlal, H., Lachaier, E., Godin, C., Saidak, Z., Francois, C., Chatelain, D., Debuysscher, V., Barbare, J.C., Chauffert, B., Galmiche, A., The retinoblastoma (Rb) protein regulates ferroptosis induced by sorafenib in human hepatocellular carcinoma cells. Cancer Lett. 356 (2015), 971–977.
12. [12] Louandre, C., Ezzoukhry, Z., Godin, C., Barbare, J.C., Maziere, J.C., Chauffert, B., Galmiche, A., Iron-dependent cell death of hepatocellular carcinoma cells exposed to sorafenib. Int. J. Cancer 133 (2013), 1732–1742.
13. [13] Nakanishi, K., Taniguchi, T., Ranganathan, V., New, H.V., Moreau, L.A., Stotsky, M., Mathew, C.G., Kastan, M.B., Weaver, D.T., D'Andrea, A.D., Interaction of FANCD2 and NBS1 in the DNA damage response. Nat. Cell Biol. 4 (2002), 913–920.
14. [14] Timmers, C., Taniguchi, T., Hejna, J., Reifsteck, C., Lucas, L., Bruun, D., Thayer, M., Cox, B., Olson, S., D'Andrea, A.D., Moses, R., Grompe, M., Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol. Cell 7 (2001), 241–248.
15. [15] Rajagopalan, M.S., Stone, B., Rwigema, J.C., Salimi, U., Epperly, M.W., Goff, J., Franicola, D., Dixon, T., Cao, S., Zhang, X., Buchholz, B.M., Bauer, A.J., Choi, S., Bakkenist, C., Wang, H., Greenberger, J.S., Intraesophageal manganese superoxide dismutase-plasmid liposomes ameliorates novel total-body and thoracic radiation sensitivity of NOS1-/- mice. Radiat. Res. 174 (2010), 297–312.
16. [16] Berhane, H., Epperly, M.W., Goff, J., Kalash, R., Cao, S., Franicola, D., Zhang, X., Shields, D., Houghton, F., Wang, H., Wipf, P., Parmar, K., Greenberger, J.S., Radiologic differences between bone marrow stromal and hematopoietic progenitor cell lines from Fanconi Anemia (Fancd2(-/-)) mice. Radiat. Res. 181 (2014), 76–89.
17. [17] Tang, D., Kang, R., Livesey, K.M., Cheh, C.W., Farkas, A., Loughran, P., Hoppe, G., Bianchi, M.E., Tracey, K.J., Zeh, H.J. 3rd, Lotze, M.T., Endogenous HMGB1 regulates autophagy. J. Cell Biol. 190 (2010), 881–892.
18. [18] Wang, X., Andreassen, P.R., D'Andrea, A.D., Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell Biol. 24 (2004), 5850–5862.
19. [19] Podhorecka, M., Skladanowski, A., Bozko, P., H2AX phosphorylation: its role in DNA damage response and Cancer therapy. J. Nucleic Acids, 2010, 2010.
20. [20] Gao, M., Monian, P., Pan, Q., Zhang, W., Xiang, J., Jiang, X., Ferroptosis is an autophagic cell death process. Cell Res. 26 (2016), 1021–1032.
21. [21] Hou, W., Xie, Y., Song, X., Sun, X., Lotze, M.T., Zeh, H.J. 3rd, Kang, R., Tang, D., Autophagy promotes ferroptosis by degradation of ferritin. Autophagy 12 (2016), 1425–1428.
22. [22] Torii, S., Shintoku, R., Kubota, C., Yaegashi, M., Torii, R., Sasaki, M., Suzuki, T., Mori, M., Yoshimoto, Y., Takeuchi, T., Yamada, K., An essential role for functional lysosomes in ferroptosis of cancer cells. Biochem. J. 473 (2016), 769–777.
23. [23] Pasquier, B., Autophagy inhibitors. Cell Mol. Life Sci. 73 (2016), 985–1001.
24. [24] Klionsky, D.J., Abdelmohsen, K., Abe, A., Abedin, M.J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C.M., Adams, P.D., Adeli, K., Adhihetty, P.J., Adler, S.G., Agam, G., Agarwal, R., Aghi, M.K., Agnello, M., Agostinis, P., Aguilar, P.V., Aguirre-Ghiso, J., Airoldi, E.M., Ait-Si-Ali, S., Akematsu, T., Akporiaye, E.T., Al-Rubeai, M., Albaiceta, G.M., Albanese, C., Albani, D., Albert, M.L., Aldudo, J., Algul, H., Alirezaei, M., Alloza, I., Almasan, A., Almonte-Beceril, M., Alnemri, E.S., Alonso, C., Altan-Bonnet, N., Altieri, D.C., Alvarez, S., Alvarez-Erviti, L., Alves, S., Amadoro, G., Amano, A., Amantini, C., Ambrosio, S., Amelio, I., Amer, A.O., Amessou, M., Amon, A., An, Z., Anania, F.A., Andersen, S.U., Andley, U.P., Andreadi, C.K., Andrieu-Abadie, N., Anel, A., Ann, D.K., Anoopkumar-Dukie, S., Antonioli, M., Aoki, H., Apostolova, N., Aquila, S., Aquilano, K., Araki, K., Arama, E., Aranda, A., Araya, J., Arcaro, A., Arias, E., Arimoto, H., Ariosa, A.R., Armstrong, J.L., Arnould, T., Arsov, I., Asanuma, K., Askanas, V., Asselin, E., Atarashi, R., Atherton, S.S., Atkin, J.D., Attardi, L.D., Auberger, P., Auburger, G., Aurelian, L., Autelli, R., Avagliano, L., Avantaggiati, M.L., Avrahami, L., Awale, S., Azad, N., Bachetti, T., Backer, J.M., Bae, D.H., Bae, J.S., Bae, O.N., Bae, S.H., Baehrecke, E.H., Baek, S.H., Baghdiguian, S., Bagniewska-Zadworna, A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12 (2016), 1–222.
25. [25] Jiang, L., Kon, N., Li, T., Wang, S.J., Su, T., Hibshoosh, H., Baer, R., Gu, W., Ferroptosis as a p53-mediated activity during tumour suppression. Nature 520 (2015), 57–62.
26. [26] Yang, W.S., Kim, K.J., Gaschler, M.M., Patel, M., Shchepinov, M.S., Stockwell, B.R., Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E4966–E4975.
27. [27] Yuan, H., Li, X., Zhang, X., Kang, R., Tang, D., Identification of ACSL4 as a biomarker and contributor of ferroptosis. Biochem. Biophys. Res. Commun. 478 (2016), 1338–1343.
28. [28] Yuan, H., Li, X., Zhang, X., Kang, R., Tang, D., CISD1 inhibits ferroptosis by protection against mitochondrial lipid peroxidation. Biochem. Biophys. Res. Commun. 478 (2016), 838–844.
29. [29] Hayano, M., Yang, W.S., Corn, C.K., Pagano, N.C., Stockwell, B.R., Loss of cysteinyl-tRNA synthetase (CARS) induces the transsulfuration pathway and inhibits ferroptosis induced by cystine deprivation. Cell Death Differ. 23 (2016), 270–278.
30. [30] 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 (2008), 234–245.
31. [31] Bogdan, A.R., Miyazawa, M., Hashimoto, K., Tsuji, Y., Regulators of iron homeostasis: new players in metabolism, cell death, and disease. Trends Biochem. Sci. 41 (2016), 274–286.
32. [32] Sun, X., Ou, Z., Xie, M., Kang, R., Fan, Y., Niu, X., Wang, H., Cao, L., Tang, D., HSPB1 as a novel regulator of ferroptotic cancer cell death. Oncogene 34 (2015), 5617–5625.
33. [33] Bridges, R.J., Natale, N.R., Patel, S.A., System xc(-) cystine/glutamate antiporter: an update on molecular pharmacology and roles within the CNS. Br. J. Pharmacol. 165 (2012), 20–34.
34. [34] Sertorio, M., Amarachintha, S., Wilson, A., Pang, Q.S., Fancd2 deficiency impairs autophagy via deregulating the ampk/foxo3a/akt pathway. Blood, 122, 2013.
35. [35] Park, E., Kim, H., Kim, J.M., Primack, B., Vidal-Cardenas, S., Xu, Y., Price, B.D., Mills, A.A., D'Andrea, A.D., FANCD2 activates transcription of TAp63 and suppresses tumorigenesis. Mol. Cell 50 (2013), 908–918.
36. [36] Matt, S., Hofmann, T.G., The DNA damage-induced cell death response: a roadmap to kill cancer cells. Cell Mol. Life Sci. 73 (2016), 2829–2850.
37. [37] Longerich, S., Li, J., Xiong, Y., Sung, P., Kupfer, G.M., Stress and DNA repair biology of the Fanconi anemia pathway. Blood 124 (2014), 2812–2819.
38. [38] Kratz, K., Schopf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., Cannavo, E., Sartori, A.A., Hengartner, M.O., Jiricny, J., Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142 (2010), 77–88.
39. [39] Zhang, Q.S., Marquez-Loza, L., Eaton, L., Duncan, A.W., Goldman, D.C., Anur, P., Watanabe-Smith, K., Rathbun, R.K., Fleming, W.H., Bagby, G.C., Grompe, M., Fancd2(-/-) mice have hematopoietic defects that can be partially corrected by resveratrol. Blood 116 (2010), 5140–5148.
40. [40] Shinde, A., Berhane, H., Rhieu, B.H., Kalash, R., Xu, K., Goff, J., Epperly, M.W., Franicola, D., Zhang, X., Dixon, T., Shields, D., Wang, H., Wipf, P., Parmar, K., Guinan, E., Kagan, V., Tyurin, V., Ferris, R.L., Li, S., Greenberger, J.S., Intraoral mitochondrial-targeted GS-nitroxide, JP4-039, radioprotects normal tissue in tumor-bearing radiosensitive Fancd2(-/-) (C57BL/6) mice. Radiat. Res. 185 (2016), 134–150.
41. [41] Berhane, H., Shinde, A., Kalash, R., Xu, K., Epperly, M.W., Goff, J., Franicola, D., Zhang, X., Dixon, T., Shields, D., Wang, H., Wipf, P., Li, S., Gao, X., Greenberger, J.S., Amelioration of radiation-induced oral cavity mucositis and distant bone marrow suppression in fanconi anemia Fancd2-/- (FVB/N) mice by intraoral GS-nitroxide JP4-039. Radiat. Res. 182 (2014), 35–49.
42. [42] Greenberger, J.S., Berhane, H., Shinde, A., Rhieu, B.H., Bernard, M., Wipf, P., Skoda, E.M., Epperly, M.W., Can radiosensitivity associated with defects in DNA repair be overcome by mitochondrial-targeted antioxidant radioprotectors. Front. Oncol., 4, 2014, 24.
43. [43] Bernard, M.E., Kim, H., Berhane, H., Epperly, M.W., Franicola, D., Zhang, X., Houghton, F., Shields, D., Wang, H., Bakkenist, C.J., Frantz, M.C., Forbeck, E.M., Goff, J.P., Wipf, P., Greenberger, J.S., GS-nitroxide (JP4-039)-mediated radioprotection of human Fanconi anemia cell lines. Radiat. Res. 176 (2011), 603–612.
44. [44] Dixon, S.J., Stockwell, B.R., The role of iron and reactive oxygen species in cell death. Nat. Chem. Biol. 10 (2014), 9–17.
45. [45] Chang, Y.H., Shaw, C.F., Wu, K.H., Hsieh, K.H., Su, Y.N., Lu, P.J., Treatment with deferiprone for iron overload alleviates bone marrow failure in a Fanconi anemia patient. Hemoglobin 33 (2009), 346–351.
46. [46] Winter, W.E., Bazydlo, L.A., Harris, N.S., The molecular biology of human iron metabolism. Lab. Med. 45 (2014), 92–102.