CD47 deficiency confers cell and tissue radioprotection by activation of autophagy

Autophagy

Volumn 8, Issue 11, 2012, Pages 1628-1642

  Soto Pantoja, David R ^a   Miller, Thomas W ^a   Pendrak, Michael L ^a   DeGraff, William G ^a   Sullivan, Camille ^a   Ridnour, Lisa A ^a   Abu Asab, Mones ^a,b   Wink, David A ^a   Tsokos, Maria ^a   Roberts, David D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL EYE INSTITUTE   (United States)

Author keywords

ATG5; ATG7; Autophagosome; BECN1; CD47; Ionizing radiation; MAP1A 1BLC3; p62

Indexed keywords

CD47 ANTIGEN; THROMBOSPONDIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IONIZING RADIATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION PROTECTION; T LYMPHOCYTE;

EID: 84869408875     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.21562     Document Type: Article

References (53)

1. Maxhimer JB, Soto-Pantoja DR, Ridnour LA, Shih HB, Degraff WG, Tsokos M, et al. Radioprotection in normal tissue and delayed tumor growth by blockade of CD47 signaling. Sci Transl Med 2009; 1:ra7; PMID:20161613; http://dx.doi.org/10. 1126/scitranslmed.3000139
2. Isenberg JS, Maxhimer JB, Hyodo F, Pendrak ML, Ridnour LA, DeGraff WG, et al. Thrombospondin-1 and CD47 limit cell and tissue survival of radiation injury. Am J Pathol 2008; 173:1100-12; PMID:18787106; http://dx.doi.org/10.2353/ ajpath.2008.080237
3. Roberts DD, Miller TW, Rogers NM, Yao M, Isenberg JS. The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47. Matrix Biol 2012; 31:162-9; PMID:22266027; http://dx.doi.org/10.1016/j.matbio.2012.01.005
4. Isenberg JS, Martin-Manso G, Maxhimer JB, Roberts DD. Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies. Nat Rev Cancer 2009; 9:182-94; PMID:19194382; http://dx.doi.org/10. 1038/nrc2561
5. Isenberg JS, Qin Y, Maxhimer JB, Sipes JM, Despres D, Schnermann J, et al. Thrombospondin-1 and CD47 regulate blood pressure and cardiac responses to vasoactive stress. Matrix Biol 2009; 28:110-9; PMID:19284971; http://dx.doi.org/10.1016/j.matbio.2009.01.002
6. Isenberg JS, Romeo MJ, Maxhimer JB, Smedley J, Frazier WA, Roberts DD. Gene silencing of CD47 and antibody ligation of thrombospondin-1 enhance ischemic tissue survival in a porcine model: implications for human disease. Ann Surg 2008; 247:860-8; PMID:18438125; http://dx.doi.org/10.1097/SLA. 0b013e31816c4006
7. Maxhimer JB, Shih HB, Isenberg JS, Miller TW, Roberts DD. Thrombospondin-1/CD47 blockade following ischemia-reperfusion injury is tissue protective. Plast Reconstr Surg 2009; 124:1880-9; PMID:19952644; http://dx.doi.org/10.1097/PRS.0b013e3181bceec3
8. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi.org/10. 1146/annurev-genet-102808-114910
9. Klionsky DJ. Autophagy. Curr Biol 2005; 15:R282-3; PMID:15854889; http://dx.doi.org/10.1016/j.cub.2005.04.013
10. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003
11. Reggiori F, Klionsky DJ. Autophagosomes: biogenesis from scratch? Curr Opin Cell Biol 2005; 17:415-22; PMID:15978794; http://dx.doi.org/10.1016/j.ceb. 2005.06.007
12. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ 2005; 12(Suppl 2):1542-52; PMID:16247502; http://dx.doi.org/10.1038/sj.cdd.4401765
13. Cook KL, Shajahan AN, Clarke R. Autophagy and endocrine resistance in breast cancer. Expert Rev Anticancer Ther 2011; 11:1283-94; PMID:21916582; http://dx.doi.org/10.1586/era.11.111
14. Zois CE, Giatromanolaki A, Sivridis E, Papaiakovou M, Kainulainen H, Koukourakis MI. "Autophagic flux" in normal mouse tissues: focus on endogenous LC3A processing. Autophagy 2011; 7:1371-8; PMID:21997374; http://dx.doi.org/10.4161/auto.7.11.16664
15. Zois CE, Giatromanolaki A, Kainulainen H, Botaitis S, Torvinen S, Simopoulos C, et al. Lung autophagic response following exposure of mice to whole body irradiation, with and without amifostine. Biochem Biophys Res Commun 2011; 404:552-8; PMID:21145309; http://dx.doi.org/10.1016/j.bbrc.2010.12.024
16. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 2001; 61:439-44; PMID:11212227
17. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc 2006; 1:2315-9; PMID:17406473; http://dx.doi. org/10.1038/nprot.2006.339
18. Suk K, Sipes DG, Erickson KL. Enhancement of B-cell translocation gene-1 expression by prostaglandin E2 in macrophages and the relationship to proliferation. Immunology 1997; 91:121-9; PMID:9203975; http://dx.doi.org/10. 1046/j.1365-2567.1997.00235.x
19. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
20. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21; PMID:11099404; http://dx.doi.org/10. 1126/science.290.5497.1717
21. Levine B, Ranganathan R. Autophagy: Snapshot of the network. Nature 2010; 466:38-40; PMID:20596005; http://dx.doi.org/10.1038/466038a
22. Reinhold MI, Green JM, Lindberg FP, Ticchioni M, Brown EJ. Cell spreading distinguishes the mechanism of augmentation of T cell activation by integrinassociated protein/CD47 and CD28. Int Immunol 1999; 11:707-18; PMID:10330276; http://dx.doi.org/10.1093/intimm/11.5.707
23. Singh K, Matsuyama S, Drazba JA, Almasan A. Autophagy-dependent senescence in response to DNA damage and chronic apoptotic stress. Autophagy 2012; 8:236-51; PMID:22240589; http://dx.doi.org/10.4161/auto.8.2.18600
24. He C, Levine B. The Beclin 1 interactome. Curr Opin Cell Biol 2010; 22:140-9; PMID:20097051; http://dx.doi.org/10.1016/j.ceb.2010.01.001
25. Wilson EN, Bristol ML, Di X, Maltese WA, Koterba K, Beckman MJ, et al. A switch between cytoprotective and cytotoxic autophagy in the radiosensitization of breast tumor cells by chloroquine and vitamin D. Horm Cancer 2011; 2:272-85; PMID:21887591; http://dx.doi.org/10.1007/s12672-011-0081-7
26. Kim H, Bernard ME, Flickinger J, Epperly MW, Wang H, Dixon TM, et al. The autophagy-inducing drug carbamazepine is a radiation protector and mitigator. Int J Radiat Biol 2011; 87:1052-60; PMID:21728759; http://dx.doi.org/10.3109/ 09553002.2011.587860
27. Scheu S, Stetson DB, Reinhardt RL, Leber JH, Mohrs M, Locksley RM. Activation of the integrated stress response during T helper cell differentiation. Nat Immunol 2006; 7:644-51; PMID:16680145; http://dx.doi.org/ 10.1038/ni1338
28. Qin X, Sarnow P. Preferential translation of internal ribosome entry site-containing mRNAs during the mitotic cycle in mammalian cells. J Biol Chem 2004; 279:13721-8; PMID:14739278; http://dx.doi.org/10.1074/jbc.M312854200
29. Rzymski T, Harris AL. The unfolded protein response and integrated stress response to anoxia. Clin Cancer Res 2007; 13:2537-40; PMID:17473181; http://dx.doi.org/10.1158/1078-0432.CCR-06-2126
30. Lang KJ, Kappel A, Goodall GJ. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 2002; 13:1792-801; PMID:12006670; http://dx.doi.org/10.1091/mbc.02-02-0017
31. Khambu B, Uesugi M, Kawazoe Y. Translational repression stabilizes messenger RNA of autophagy-related genes. Genes Cells 2011; 16:857-67; PMID:21790910; http://dx.doi.org/10.1111/j.1365-2443.2011.01532.x
32. Bose JK, Huang CC, Shen CK. Regulation of autophagy by neuropathological protein TDP-43. J Biol Chem 2011; 286:44441-8; PMID:22052911; http://dx.doi.org/10.1074/jbc.M111.237115
33. Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, et al. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 2009; 5:816-23; PMID:19535919
34. Isenberg JS, Maxhimer JB, Powers P, Tsokos M, Frazier WA, Roberts DD. Treatment of liver ischemia-reperfusion injury by limiting thrombospondin-1/CD47 signaling. Surgery 2008; 144:752-61; PMID:19081017; http://dx.doi.org/10.1016/ j.surg.2008.07.009
35. Moreau K, Luo S, Rubinsztein DC. Cytoprotective roles for autophagy. Curr Opin Cell Biol 2010; 22:206-11; PMID:20045304; http://dx.doi.org/10.1016/j.ceb. 2009.12.002
36. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40:280-93; PMID:20965422; http://dx.doi.org/10.1016/j. molcel.2010.09.023
37. Hidvegi T, Ewing M, Hale P, Dippold C, Beckett C, Kemp C, et al. An autophagy-enhancing drug promotes degradation of mutant alpha1-antitrypsin Z and reduces hepatic fibrosis. Science 2010; 329:229-32; PMID:20522742; http://dx.doi.org/10.1126/science.1190354
38. Eisbruch A. Amifostine in the treatment of head and neck cancer: intravenous administration, subcutaneous administration, or none of the above. J Clin Oncol 2011; 29:119-21; PMID:21115854; http://dx.doi.org/10.1200/JCO.2010. 31.5051
39. Sarfati M, Fortin G, Raymond M, Susin S. CD47 in the immune response: role of thrombospondin and SIRP-alpha reverse signaling. Curr Drug Targets 2008; 9:842-50; PMID:18855618; http://dx.doi.org/10.2174/138945008785909310
40. Sagawa M, Shimizu T, Fukushima N, Kinoshita Y, Ohizumi I, Uno S, et al. A new disulfide-linked dimer of a single-chain antibody fragment against human CD47 induces apoptosis in lymphoid malignant cells via the hypoxia inducible factor-1á pathway. Cancer Sci 2011; 102:1208-15; PMID:21401803; http://dx.doi.org/10.1111/j.1349-7006.2011.01925.x
41. Bras M, Yuste VJ, Roué G, Barbier S, Sancho P, Virely C, et al. Drp1 mediates caspase-independent type III cell death in normal and leukemic cells. Mol Cell Biol 2007; 27:7073-88; PMID:17682056; http://dx.doi.org/10.1128/ MCB.02116-06
42. Saumet A, Slimane MB, Lanotte M, Lawler J, Dubernard V. Type 3 repeat/C-terminal domain of thrombospondin-1 triggers caspase-independent cell death through CD47/alphavbeta3 in promyelocytic leukemia NB4 cells. Blood 2005; 106:658-67; PMID:15784731; http://dx.doi.org/10.1182/blood-2004-09-3585
43. Kikuchi Y, Uno S, Kinoshita Y, Yoshimura Y, Iida S, Wakahara Y, et al. Apoptosis inducing bivalent single-chain antibody fragments against CD47 showed antitumor potency for multiple myeloma. Leuk Res 2005; 29:445-50; PMID:15725479; http://dx.doi.org/10.1016/j.leukres.2004.09.005
44. Manna PP, Frazier WA. CD47 mediates killing of breast tumor cells via Gi-dependent inhibition of protein kinase A. Cancer Res 2004; 64:1026-36; PMID:14871834; http://dx.doi.org/10.1158/0008-5472.CAN-03-1708
45. Johansson U, Higginbottom K, Londei M. CD47 ligation induces a rapid caspase-independent apoptosis-like cell death in human monocytes and dendritic cells. Scand J Immunol 2004; 59:40-9; PMID:14723620; http://dx.doi.org/10.1111/ j.0300-9475.2004.01355.x
46. Zeng X, Kinsella TJ. BNIP3 is essential for mediating 6-thioguanine- and 5-fluorouracil-induced autophagy following DNA mismatch repair processing. Cell Res 2010; 20:665-75; PMID:20368736; http://dx.doi.org/10.1038/cr.2010.40
47. White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res 2009; 15:5308-16; PMID:19706824; http://dx.doi.org/10. 1158/1078-0432.CCR-07-5023
48. Isenberg JS, Hyodo F, Pappan LK, Abu-Asab M, Tsokos M, Krishna MC, et al. Blocking thrombospondin-1/ CD47 signaling alleviates deleterious effects of aging on tissue responses to ischemia. Arterioscler Thromb Vasc Biol 2007; 27:2582-8; PMID:17916772; http://dx.doi.org/10.1161/ATVBAHA.107.155390
49. Thakar CV, Zahedi K, Revelo MP, Wang Z, Burnham CE, Barone S, et al. Identification of thrombospondin 1 (TSP-1) as a novel mediator of cell injury in kidney ischemia. J Clin Invest 2005; 115:3451-9; PMID:16294224; http://dx.doi.org/10.1172/JCI25461
50. Myers SA, DeVries WH, Andres KR, Gruenthal MJ, Benton RL, Hoying JB, et al. CD47 knockout mice exhibit improved recovery from spinal cord injury. Neurobiol Dis 2011; 42:21-34; PMID:21168495; http://dx.doi.org/10.1016/j.nbd. 2010.12.010
51. Jin G, Tsuji K, Xing C, Yang YG, Wang X, Lo EH. CD47 gene knockout protects against transient focal cerebral ischemia in mice. Exp Neurol 2009; 217:165-70; PMID:19233173; http://dx.doi.org/10.1016/j.expneurol.2009.02.004
52. Subramanian S, Boder ET, Discher DE. Phylogenetic divergence of CD47 interactions with human signal regulatory protein alpha reveals locus of species specificity. Implications for the binding site. J Biol Chem 2007; 282:1805-18; PMID:17098740; http://dx.doi.org/10.1074/jbc.M603923200
53. Sambrook J. Molecular Cloning: A Laboratory Manual. NY: Cold Spring Harbor Laboratory Press NY, 2001